JDPJournal Fall 2006

Volume 1 Fall 2006
The
Journal
The Journal of Developmental Processes

of
Developmental
Processes
Sponsored by the Interdisciplinary Council on

Developmental and Learning Disorders (ICDL),
the Council of Human Development, and the
Milton and Ethel Harris Research Initiative
www.icdl.com
www.councilhd.ca
www.mehri.ca
Vol. 1 Fall 2006
ISBN number: 0-9767758-4-0

Journal of Developmental Processes
Submission Guidelines
Description
The goal of the Journal of Developmental Processes is to provide a vehicle for
research and clinical studies that advance knowledge of the complexity inherent in all
developmental processes. The JDP encourages exchange of ideas across fields including,
but not limited to, animal behavior, anthropology, biology, education, linguistics, neuro-
science, occupational and speech and language therapy, primatology, psychiatry, psychol-
ogy, public policy, sociology, and social work.
The Journal is interested in both experimental and descriptive studies, including
basic research, detailed case reports, ethnographic analysis, and theoretical explorations.
Particularly welcome are innovative conceptual frameworks and methods that capture the
complexity of developmental processes as well as assessment procedures and interven-
tions that enable children and families to overcome mental health, developmental, social,
and learning challenges.
Submissions
Send queries and submissions on clinical aspects and applications to Asso-
ciate Editor Ira Glovinsky at ira1834@sbcglobal.net; all other queries and submissions,
and books for potential review, should go to Editor Barbara J. King at bjking@wm.edu
or Department of Anthropology, College of William and Mary, Williamsburg, VA, USA,
23187-8795.
Please submit manuscripts electronically, preferably in Microsoft Word® format.
Length is negotiable with the editor, but generally should not exceed 50 manuscript pages,
including references. Submit your contact information, including phone, fax, and postal
mailing address. Also enclose a cover letter indicating that the article has not been pub-
lished, and is not under consideration elsewhere.
Tables, figures, and photographs should be used sparingly. Please include a high
gloss black-and-white copy of the image as well as an electronic file in TIFF, EPS, or JPG
format. Clearly indicate where the image should appear, as well as a title and explanatory
note. Line art should have a resolution of 1200 dots per inch for good print quality.
References
References should be listed in alphabetical order. Each listed reference should be cited To purchase a copy of the Journal of Developmental Processes
in the text, and each text citation should be listed in the References. We follow the APA or to subscribe to future issues,
style, e.g.,
please visit www.icdl.com
Greenspan, S. I., & Shanker, S. G. (2004). The first idea: How symbols, language, and or call 301-656-2667 for information
intelligence evolved from our primate ancestors to modern humans. Cambridge,
MA: Da Capo.
Greenspan, S. I., & Shanker, S. G. (2005). Developmental Research. In E. S. Person,
A. M. Cooper, & G. O. Gabbard, American psychiatric publishing textbook of psy-
choanalysis (pp. 335–360). Washington, DC: American Psychiatric Publishing.
Greenspan, S. I., & Wieder, S. (1997). Developmental patterns and outcomes in infant and
children with disorders in relating and communicating: A chart review of 200
cases of children with autistic spectrum diagnosis. Journal of Developmental and
Learning Disorders, 1, 87–141.
THE JOURNAL OF DEVELOPMENTAL PROCESSES
Volume 1 2006
CONTENTS
Introductory Notes—Stanley I. Greenspan 1
A Welcome, and an Invitation, from the Editor—Barbara J. King 3
Dynamic Systems Research on Interindividual Communication:

The Transformation of Meaning-Making—Alan Fogel 7
Early Family Trauma and the Ontogeny of Glucocorticoid Stress

Response in the Human Child: Grandmother as a Secure Base—
Mark V. Flinn and David V. Leone 31
The Development of Spontaneous Gestures in Zoo-living Gorillas

and Sign-taught Gorillas: From Action and Location to Object
Representation—Joanne E. Tanner, Francine G. Patterson, and
Richard W. Byrne 69
The Kids Are Alright: Maternal Behavioral Interactions and Stress

Reactivity in Infants of Differentially Reared Rhesus Monkeys—
Peter G. Roma, Angela M. Ruggiero, Melanie L. Schwandt,
J. Dee Higley, and Stephen J. Suomi 103
The Literacy of Interaction: Are Infants and Young Children Receiving

a “Mental Diet” Conducive for Future Learning?—Pnina S. Klein 123
Toward a Behavior of Reciprocity—Morton Ann Gernsbacher 138
Book Review: Parenting for Primates—Barbara J. King 153
Bethesda, Maryland Copyright © 2006

Editor in Chief Associate Editor
Stanley I. Greenspan Ira Glovinsky
Chair, Interdisciplinary Council for The Interdisciplinary Center for the Family
Developmental and Learning Disorders West Bloomfield, Michigan, USA
Departments of Psychiatry, Behavioral Sciences, ira1834@sbcglobal.net
and Pediatrics
George Washington University Medical School Administrative Editor
Washington, DC, USA Jane Mild LaRoque
Lexington, Massachusetts, USA
Editor jmlaroque@rcn.com
Barbara J. King
Department of Anthropology Editorial Assistant
College of William and Mary Meghan Habas Siudzinski
Williamsburg, Virginia, USA College of William and Mary
bjking@wm.edu Williamsburg, Virginia, USA
megsudz@gmail.com
Associate Editor in Chief
Serena Wieder
Interdisciplinary Council on Developmental
and Learning Disorders
Bethesda, Maryland, USA
JDP Editorial Board

Margaret Bauman Robert Lickliter
The Ladders Program Department of Psychology
Harvard University Florida International University
Wellesley, Massachusetts, USA Miami, Florida, USA
Leon Cytryn Pedro Reygadas
Departments of Psychiatry, Behavioral Sciences, Department of Social Sciences and Humanities
and Pediatrics Autonomous University of San Luis Potosi
George Washington University San Luis Potosi, Mexico
Washington, DC, USA
Ricki G. Robinson
Alan Fogel Descanso Medical Center for Development &
Department of Psychology Learning
University of Utah University of Southern California
Salt Lake City, Utah, USA La Canada, California, USA
Gil Foley Rebecca Shahmoon Shanok
Department of Psychology Jewish Board of Family Services
Ferkauf Graduate School Child Development Center
Yeshiva University New York, New York, USA
Bronx, New York, USA
Stuart Shanker
Sima Gerber Distinguished Research Professor of Philosophy
Department of Linguistics and Communication and Psychology
Disorders Director, the Milton and Ethel Harris Research
Queens College, CUNY Initiative
Flushing, New York, USA York University
Toronto, Ontario, Canada
Morton Ann Gernsbacher
Department of Psychology Barbara Smuts
University of Wisconsin-Madison Department of Psychology
Madison, Wisconsin, USA University of Michigan
Ann Arbor, Michigan, USA
Barbara Kalmanson
Clinical Psychologist Richard Solomon
San Francisco, California, USA Ann Arbor Center for Developmental
and Behavioral Pediatrics
Pnina Klein Ann Arbor, Michigan, USA
School of Education
Bar-Ilan University Christina Toren
Ramat-Gan, Israel Department of Anthropology
University of St. Andrews
Marc Lewis St. Andrews, Scotland
Department of Human Development and
Applied Psychology Ann Turnbull
University of Toronto Beach Center on Disability
Canada The University of Kansas
Lawrence, Kansas, USA
The Journal gratefully acknowledges the financial support of the Milton and Ethel Harris Research
Initiative (MEHRI), York University, Toronto, Canada. For more information, please see
www.MEHRI.ca
Introductory Notes
Stanley I. Greenspan, MD
Editor in Chief
Interdisciplinary Council for Developmental Learning Disorders
Department of Psychiatry, Behavioral Sciences, and Pediatrics
George Washington University Medical School
Washington, DC
The Journal of Developmental and Learning Disorders has expanded its focus and be-
come the Journal of Developmental Processes (JDP). The Editor, Barbara J. King,
Professor of Anthropology at The College of William and Mary, embodies the spirit
of the Journal in her own outstanding work, and beautifully describes it in the edito-
rial that follows. The expanded editorial board and sponsoring organizations—the
Council of Human Development, the Milton and Ethel Harris Research Initiative, in
addition to the Interdisciplinary Council on Developmental and Learning Disorders—
reflect the broad focus of the Journal. As will readily be seen, the JDP includes all the
disciplines that contribute to our understanding of human development, the factors
that influence it, the mechanisms through which they work, and the enormous varia-
tions observed throughout the course of life. The Journal embraces clinical studies
and case descriptions in keeping with the traditions established by its predecessor, the
Journal of Developmental and Learning Disorders. It also, however, focuses on a
broad range of studies and narratives that are necessary for a full understanding of de-
velopmental processes. I want to welcome you to our new Journal and hope that you
will not only enjoy reading it, but will also become part of the growing group of col-
leagues that are actively contributing to our understanding of the full complexity of
human experience.
1
A Welcome, and an Invitation, from the Editor
Barbara J. King, Editor

Department of Anthropology
College of William and Mary
bjking@wm.edu
Capturing the continuous processes of change inherent in development, those stem-

ming from “all the delicate, transparent webs from which we have woven ourselves,”1
is a wondrous challenge for 21st century scientists. In the case of human development,
it is a challenge for clinicians and educators as well.
As 21st century science becomes increasingly high-tech, we may take approaches
to the study of development using complex population statistics, gene maps, neuro-
chemistry profiles, and MRI images. These avenues of research have much to teach
us, but are not enough in themselves. Living, breathing, ever-changing flesh-and-
blood individuals belong front and center in our research in all their beautiful or dis-
tressing deviation from “the norm,” whatever that may be. When we work to under-
stand how infants, juveniles, and subadults—in humans and other animals—come to
communicate, learn, and negotiate the rules of the social systems in which they live,
we learn a great deal by going beyond the statistically significant patterns in our data
to embrace all the ways of being, becoming, and behaving that we can identify.
To recognize and describe change as it occurs is critical, because change is always
occurring even as we study the organisms before us. The situation is not a dichoto-
mous one, with normative versus non-normative development as two mutually exclu-
sive pathways available for our scrutiny. An understanding of developmental systems
allows us to see that stresses of some sort will always impact individuals. When deal-
ing with human development, an important goal is to determine when and how best to
intervene in order to help children (and adults) who are struggling because of the
stresses of their own unique developmental profiles. The trick, both for clinical pro-
fessionals who may step in directly and for academics who may provide information
in aid of this intervention, is to identify the differences that make a difference (apolo-
gies to anthropologist Gregory Bateson for my mangling of the letter, but I think not
the spirit, of his famous phrase).
In short, scientists, clinicians, educators, and others who study aspects of develop-
ment may embrace an array of exciting options. We can seek to discover precisely how
mammalian/primate/human nurturing interactions that surround the genes affect de-
velopmental outcomes; how emotions are created by, and in turn help create, the
processes of the brain; and how the social, cultural, and indeed global interdependen-
cies that make up our world affect all living creatures in it.
1. David Grossman, Be My Knife (New York: Farrar, Straus, and Giroux, 1998), p. 69.
3
4 BARBARA J. KING
The central mission of the Journal of Developmental Processes is to reflect, and to

foster, these nuanced and diverse responses to the challenges of studying develop-
ment. The JDP wishes to publish a wide variety of theories and methods, more pow-
erful in the collective than in the singular, that are sensitive to the dynamic processes
of development.
The JDP aims to be interdisciplinary and international, but this is only a first step.
The ways in which we intend to make a distinctive contribution are reflected in our
mission statement. We welcome qualitative research reports as much as we do quan-
titative ones, and indeed hope to publish many examples where qualitative and quan-
titative approaches reinforce each other. Case studies, generated by both academic and
clinical research or reflection, will be a key part of the journal’s content, as will theo-
retically innovative articles and book essays. In short, the JDP is open to new, com-
prehensive approaches to development in a number of formats.
The six articles and single book essay in this inaugural issue reflect the principles
I have just described. Psychologist Alan Fogel leads off with a compelling and
provocative discussion of methodologies for studying how systems change over time,
not only in frequencies, durations, and sequential patterns, but also in meaning. An-
thropologists Mark V. Flinn and David V. Leone report results from field research on
the island of Dominica that elegantly brings together behavioral and hormonal assess-
ment of children’s stress responses. Primate researchers Joanne E. Tanner, Francine G.
Patterson, and Richard W. Byrne compare the development of gesturing in zoo-living
and sign-taught gorillas, with insightful analysis of the influence of a highly social
process that they call action-mapping.
Flinn and Leone’s theme of stress as measured hormonally and behaviorally is
echoed in a second article from primate studies, written by Peter G. Roma, Angela M.
Ruggerio, Melanie L. Schwandt, J. Dee Higley, and Stephen J. Suomi. Intriguingly,
and surprisingly, this research team found that, in a colony of rhesus monkeys, moth-
ers’ rearing condition did not affect infant stress responses.
The final two articles return us to the realm of human behavioral development.
Pnina S. Klein describes a developmental mediation approach available to parents and
educators to aid children’s learning; she identifies several significant ways in which
this approach differs from existing early intervention projects in many parts of the
world. Focusing on autism, Morton S. Gernsbacher writes about reciprocity, offering
incisive remarks about the far-reaching effects that professionals, peers, and parents
may see when they are encouraged to act reciprocally with autistic children. Finally,
rounding out the first issue and revisiting once more a broad primate level of develop-
ment, I discuss the strengths and weaknesses of Harriet Smith’s book Parenting for
Primates.
As this summary indicates, JDP’s first issue is diverse, and no single journal issue
could hope to be fully comprehensive on development. Yet more needs to be done. All
but two of the authors, one in Scotland and and another in Israel, work in North Amer-
ica. I want to publish the best work on development from Latin America, Asia, Africa,
and the Pacific as well. Results on nonhuman primates are well-represented, but
there’s room in these pages too for birds, cetaceans, dogs, elephants, rodents, and any
other species studied developmentally. Finally, I aim for broader representation of aca-
A Welcome, and an Invitation, from the Editor 5
demic and clinical fields and subfields, in terms of articles, book essays, and names to
broaden our pool of peer readers who may advise the editorial board on submitted
manuscripts.
Please consider this editorial an invitation to contact me with your ideas for arti-
cles, nominations, including self-nominations, for experts to join our reviewing pool,
and any suggestions and questions that might be appropriate as JDP undergoes the
early days of its own developmental process.
In closing, I would like to thank Stanley Greenspan, MD, and Serena Wieder, PhD,
(Associate Editor in Chief), whose vision is responsible for creating the JDP. I would
also like to thank Serena for her work on the clinical articles. The three of us, in turn,
acknowledge the skilled work of Jane Mild LaRoque, Sharon Markus, and Meghan
Habas Siudzinski. Grateful appreciation is offered to our sponsoring organizations: the
Interdisciplinary Council on Developmental and Learning Disorders, the Council of
Human Development, and the Milton and Ethel Harris Research Initiative.
Dynamic Systems Research on
Interindividual Communication:
The Transformation of Meaning-Making
Alan Fogel
Department of Psychology
University of Utah
alan.fogel@psych.utah.edu
Abstract: This paper presents a dynamic systems methodology for the study of interindi-
vidual communication in social systems. Since dynamic social systems are fluid, changing,
emergent, developing, and yield created information in a meaning-making process, it fol-
lows that dynamic systems research best serves scientific discovery by substantiating these
same processes in the method. The dynamic systems methods presented here place the sci-
entist in the system, not knowing the answer, but working through a dynamic process of en-
gagement with the system, toward an emergent understanding of the patterns of communi-
cation and their changes over time with respect to the limitations of the observer’s method
and point of view.
Introduction
Dynamic systems theory addresses the problem of describing the ways in which
complex systems change over time. The focus of this paper is to highlight the unique
conceptual and research issues that arise when change in social communication sys-
tems is the topic of investigation. Specifically, in addition to quantitative indices of
change in frequencies, durations, and sequential patterning of communicative behavior,
research on communication can also encompass the meaning in the system. Meaning,
similar to any other pattern formation process in a dynamic system, can be thought of
as emerging and stabilizing dynamically through a process of self-organization. This
paper presents a research model that includes both developmental changes in quantity
and in meaning. These terms are defined and the methods are explained and illustrated
in a lengthy research example.
The study of change is paradoxical. The phenomenon that one wishes to observe
in one moment is no longer the same in the next moment. Yet, as human observers, we
are capable of perceiving and describing when behavior at two or more moments in
time appears to be the “same” or “different” (Popper, 1968). This is particularly rele-
vant to the problem of studying communication because meaning can be defined as
7
8 ALAN FOGEL
the perception of a “difference” between two or more communicative actions. But the
meaning of the perceived difference can only become manifest in the changing actions
or interpretations of participants in a communication process. Meaning-making is thus
part of the way in which human observers interpret some complex series of changes
as “having” a pattern, structure, or order. Any time an observer declares the presence
of a pattern, in other words, the observer becomes a part of the dynamic system being
observed. The stars in a galaxy do not in fact have, own, or possess a pattern. The pat-
tern (the galaxy) emerges in the relationship of the stars to the observer.
The study of complex dynamic systems takes as a premise that individual compo-
nents and constituents are best understood as part of a collective in which each affects
the others to create pattern and order at the level of the collective, an order which may
not be obvious at the level of the behavior of each of the constituents. This paper takes
the perspective that the study of dynamic systems involves one additional constituent
to any collective that is being observed: the observer’s point of view. The observer, in
other words, is part of the description or model of the system. Although complex sys-
tems exist in the absence of the observer, the patterns and processes that are described,
counted, and analyzed emerge from the relationship between the observer and the sys-
tem. This point refers to the role of scientists on systems in which they are not partic-
ipants. Should they be participants, their behavior and presence becoming part of the
system, in addition to their point of view contributing to how that system comes to be
understood by others?
The pattern, furthermore, emerges over some finite period of time. One looks at
the world and patterns seem to appear instantaneously. There is, however, at least
some period of microseconds required for the brain and sense organs to organize the
perceptual flow into a flower, tree, or galaxy. Even that relatively rapid emergent
process, however, is founded upon an earlier, and considerably longer, period of en-
gagement in that person’s life, a period in which patterns were not apparent and
needed days, weeks, or months to be discovered through some process of engagement
with the world. The pattern coalesces and stabilizes into a consistent attractor in the
brain-behavior-sensory system, making the recognition of the pattern on future occa-
sions more rapid and efficient (Lewis, 1995; 2005; Thelen & Smith, 1994).
This longer process of meaning-making could, of course, be applied to an infant
or child who must discover through perception and action, or “re-create,” the mean-
ings of words and gestures via a process of co-regulation with adults (Fogel, 1993;
King, 2004). In this paper, however, we apply the same notion to the scientist. Faced
with a complex system whose patterns do not easily appear to the observer, patterns
may—through a process of prolonged engagement, discovery, and meaning-making—
finally emerge.
It is not the intention here to review the growing literature on dynamic systems re-
search and theory. Where needed, the principles of dynamic systems theory are briefly
mentioned. The central theme of dynamic systems theory is to understand how the pat-
terning of the collective is related to the co-regulation between the constituents. In the
view of dynamic systems theory, the constituents of a system act together to constrain
the multiple actions of other constituents so that the complex system organizes and re-
organizes over time into a series of semi-stable patterns of behavior called attractors
Dynamic Systems Research on Interindividual Communication 9
(Kelso, 1995; Kugler, Kelso, & Turvey, 1982; Prigogine & Stengers, 1984). Con-
stituents, in other words, change each other in the process of convergence toward an
attractor. Two people in a long-term partnership change each other in the process of
forming a “couple” with recognizable patterns and habits.
Each time an attractor is re-constituted, the actions within the attractor, the mi-
crolevel activity of the system, are somewhat different from the previous occurrence
of that same attractor. The concept of dynamic stability replaces the concept of struc-
ture, habit, and association in traditional theories of behavior regularities (Capra,
1996; Fogel, 1993; Thelen & Smith, 1994). The attractor occurs at an organizational,
collective, or macrolevel of activity, in which the observer’s perception of “sameness”
becomes possible.
In the behavioral sciences, complex systems occur for intraindividual, interindi-
vidual, ecological, and sociocultural relationships. The intraindividual system in-
volves relationships between the various systems of the body and mind, such as be-
tween genes and their cellular environment, between brain and behavior, between
muscles that act together to perform an action, or between emotion and intellect. The
interindividual system involves social relationships such as between parent-child,
close companions, teacher-student, supervisor-employee, therapist-client, romantic
partners, and business partners. The ecological system includes relationships between
humans and their physical and biological environment such as our relationships with
the plants, animals, and the earth. The sociocultural system contains all the relation-
ships within and between groups of people with intersecting histories; it takes in rela-
tions of international peace or conflict, systems of kinship and religion, of politics and
economics, institutions of education or medical care, systems of government and law.
The Paradox of Change and the Role of the Observer

Attractor patterns may become salient to observers in each of these systems. Any
type of stable behavior pattern in the intraindividual system, such as walking or smil-
ing, involves microlevel co-activity between muscular, skeletal, neurological, en-
docrine, and immune systems of the body. Greetings, leave-takings, topics of conver-
sation, and the like are seen as stable attractors in the interindividual system. Taking a
pet dog for a walk, or creating artificial ladders for migrating salmon to traverse dams
and other human structures on their way upstream, are examples of attractors in the
ecological system. Treaties, laws, elections, and classrooms are attractors in a sociocul-
tural system. In these examples, attractors are perceived when patterns of linkage be-
tween microlevel constituents recur with regularity and with relatively little variability.
In interindividual communication, for example, people can easily perceive and
label the attractor called “greeting” at the macrolevel, even though there are many dif-
ferent types of greetings (formal or informal, distant or intimate, face-to-face, or
through some electronic medium). These different types of greetings all show differ-
ences in the microlevel of activity within the perceived “sameness” of the attractor
pattern. Even within the same interindividual relationship over time, every face-to-
face greeting is somewhat different in the microlevel pattern of activity. The same pair
10 ALAN FOGEL
of romantic partners, for example, sometimes kisses, sometimes hugs, sometimes

nods, or does some combination of these and other actions. In sum,
• Dynamic systems are always changing.
• Patterns of stability can be perceived from the flow of change.
• “Change” and “stability” are emergent from the engagement of the observer
with the system.
• Science is the pattern of meanings that are made from the observer-world system.
This brief discussion highlights a series of methodological dilemmas that a scientist/
observer faces when attempting to understand and study changing dynamic systems.
• Is it possible for scientific meanings to transcend the particularities of how,
when, and by whom something is observed?
• Is it possible to capture and analyze a phenomenon that is always changing, that
is, is there any such thing as a “phenomenon” to be studied?
These questions may seem to be best left to philosophers rather than to scientists.
Shouldn’t scientists stick to being concrete and practical? Perhaps a scientist may wish
for such simplicity. After all, if people can perceive attractors readily, then it should
be a relatively easy task for a scientist to make recordings of all instances of greeting
patterns in a particular sample of humans or other animals, measure and count how
long that pattern lasts, how may times it occurs, under what circumstances it appears,
and when it is it likely to change. The scientist can also count the timing, duration, and
number of particular actions within the pattern, at the microlevel (the kisses, hugs,
nods, etc.). These can be counted separately for each partner, and statistical and sim-
ulation models can be used to verify the recurring stable patterns at the macrolevel.
The danger, however, is that this method runs the risk of freezing the phenomenon,
that is, of forgetting—after all is counted and analyzed—that patterns like greetings
are sustained by a dynamic process.
The main thesis of this paper is that macroscopic order in dynamic systems
emerges in the developing relationship between the constituents of the system and in
the developing relationship between the observer and the system. Without taking ac-
count of these evolving relationships, quantification can lead to reductionism. Quan-
tifying may lose the evolving process for the sake of trying to capture it. And when
this has been done, and the paper published in a respectable quantitative empirical sci-
entific journal, the scientist/observer has in fact affected the reader’s understanding of
the system by this mode of action on the system, which in the end, is the observer’s
choice and a point of view (Toren, 1996).
The result is analogous to trying to understand quantum mechanics by using New-
tonian classical mechanics. Quantum mechanics, as a theory of the subatomic world,
cannot serve as a theory of the macroscopic world of behavior. There is, however, an
analogy between Heisenberg’s uncertainty principle, and other “strange” quantum
phenomena, and the behavioral science of dynamic systems. By ignoring the role of
the observer, and by trying to impose the observer’s (unacknowledged) perception of
stability, we prematurely reify something that is inherently dynamic (because it is al-
ways changing).
Quantification per se, however, is not inherently concretizing and reifying if the
observer recognizes that measurement is simply one way of engaging in a scientific
relationship with a dynamic system. In this case, reduction to a quantity may be a use-
ful scientific tool so long as this act is placed in the context of other convergent acts
of meaning-making by the scientist. The dynamics of behavior, like the subatomic
realm, is a strange world that shifts in the way it appears depending upon our point of
view. Behavior is not an “it” or a “thing.” Behavior constitutes itself in the very
process of forming, acting, changing, and disappearing (Fogel, 1993; Morris, 2004).
Scientific language can literally create a world. To use the scientific term, the noun
“behavior” can easily create the illusion that there is a “thingness” to behavior, a sub-
stance, and a permanence.
The process of engagement with the written word in a scientific document is also
emergent and dynamic. A sociocultural landscape of mutual linguistic understanding
emerges (in the time frame of microseconds) when the reader engages with the text.
Behavior is created as a dynamic moment of shared meaning. There is a further
choice, however, taken by either the writer or the reader, to assume that what appears
in this dynamic moment of shared understanding is therefore substantial and concrete.
This turn toward reification is likely to better reflect the stance and judgment of the
observer than the changing and dynamic reality of the system being observed.
This is not a discussion of the fictitious and imaginary, as if the noun were some-
thing like “hobbit.” Behavior constitutes a domain we can call “reality,” so long as we
understand “reality” to be dynamically constituted, as alive and changing, and as dif-
ferent with respect to the point of view of the observer. This observation has the po-
tential to be profoundly disturbing. On the one hand, few could deny that behavior is
dynamically constituted, alive and changing, and that different people describe and in-
terpret it in different ways. On the other hand, few people are likely to explicitly rec-
ognize or accept that, therefore, behavior, while real, is not a concrete thing at all.
In English, the verb to know generally leads to the formation of a concrete, factual
body of knowledge. The verb to understand, however, refers to an open-ended, expe-
riential, emotional process of knowing that usually occurs between people as they en-
gage over time in close interindividual relationships. To understand in English is
equivalent to conocer (Spanish), conòscere (Italian), connaître (French), and conhecer
(Portuguese). The corresponding words for concrete knowing in these four languages
are saber, sapere, savoir, and saber. Research on the dynamics of meaning-making ad-
mits to an inability to know completely (since behavior is changing in the very act of
observing and conceptualizing), and instead seeks to engage in a long-term process
that may lead to understanding.
The idea that one can have complete knowledge comes from ancient Greek think-
ing which became the foundation of Western science, what Levinas (1969) calls “total-
izing.” Philosophers of intersubjectivity (Buber, 1958; Jopling, 1993; Levinas, 1969),
however, point out interindividual communication reflects what Levinas calls “infini-
tizing,” meaning that we can never completely know another person or completely de-
scribe behavior. In an infinitizing stance toward the other, there is no sense of being
directed or evaluated; only a feeling of union. One feels connected to the other and
meets the other without reserve and in the fullness of the other’s vulnerability to be
12 ALAN FOGEL
changed. Buber (1958) called these types of relationships “I-Thou” as opposed to the
totalizing stance of “I-It” relationships.
Scientists who take as the starting point the slipperiness and ineffability of the very
dynamics that they wish to study may aspire to shed light on the underlying dynam-
ics of behavior. No previous reification of behavior dynamics has succeeded in help-
ing us understand why some people contract deadly diseases, why war and violence
continue to flare in an enlightened global society, or why poverty and hunger are glob-
ally pervasive. Perhaps the answers lie in a dynamic understanding of how these prob-
lems develop over time. Perhaps there are no concrete answers, but rather a process of
learning how to understand and work with our unimaginably complex universe.
The Conceptualization of Change in Dynamic Systems Theory

In the end, the scientist/observer concerned with illuminating and respecting the
inherent dynamics of the system is compelled to shift away from a study of structure
to a study of process (Capra, 1996). One way out of the dilemma of conceptualizing
behavior as a thing is to replace the noun with a verb, “behaving.” Whether noun or
verb, naming may eventually lead to reification. Shifting to a verb, however, can be a
useful linguistic trope to remind us that the nature of systems is change, and that sta-
bility is in the eye of the beholder. Reading and studying dynamic systems requires an
active, inquisitive, and critical meta-awareness that the linguistic and mathematical
devices of science serve only as signifiers for that which cannot be completely signi-
fied. This paper is meant to be read with that type of meta-awareness.
The admonition that “the map is not the territory,” does not quite fit here since the
territory is typically seen as fixed. But territory changes with earthquakes, storms and
floods. A more radical shift (change) in the scientific stance is called for: from things-
in-themselves to transformations. Territory implies space and boundaries. Transforma-
tions imply time and change. As a prelude to the description of research methodology,
in the following section, three levels of change are discussed. These are derived from
research using the techniques to be presented in this paper.
Sequence vs. Process at the Microlevel (Level 1 Change)

Change at the microlevel involves a shift from one to another behavior within an at-
tractor. In mother-infant face-to-face play, for example, there is an iterative cycling in
both mother and infant of smiling and not smiling, mutual gaze and gaze elsewhere,
and other body movements and facial expressions typical of this type of play. Changes
occur as the dyad shifts from one to another mutual action. Each instance of this attrac-
tor that recurs over days or weeks also has a similar pattern of activity, yet it is changed
from the previous instance of this attractor. These microlevel changes are referred to as
Level 1 change, or ordinary variability within a stable attractor (Fogel, Garvey, Hsu, &
West-Stroming, 2006a).
Virtually all studies of microlevel change in the behavioral sciences reduce the
flow over time to a probabilistic sequence. Sequences have the form of A → B → C.
This scheme can become very complex, as when the behavior of multiple interacting
partners is tracked simultaneously. In this case, the behavior of each partner can be ob-
served to precede, follow, or be simultaneous with the other. A wide variety of statis-
tical and simulation models exists to conceptualize and analyze these sequences for
regularly recurring patterns. These tools have continued to become more mathemati-
cally sophisticated, capable of describing complex lead-lag relationships, timing fac-
tors in interaction, and other quantitative indices of social engagement and sensitivity
(cf. Jaffe, Beebe, Feldstein, Crown, & Jasnow, 2001; Lewis, Lamey, & Douglas, 1999;
Ryan, Gottman, Murray, Carrère, & Swanson, 2000; van Geert, 1998).
The use of any of these tools, however, can imply a reification of change is a lin-
ear sequence. This is because, once coded and statistically analyzed, significant prob-
abilities capture attention. The underlying dynamics are messier and less easy to un-
derstand and remember. But if behavior at any level of description is always changing,
and if those changes occur in the process of forming the relationships that ultimately
constitute the perceived attractor, then models of sequence, however, sophisticated,
may miss the very dynamics they presume to describe.
In research by the author and his colleagues, we have reported sequential data of the
following sort: Infant smiles are more likely occur during maternal smiles; infant smil-
ing tends to follow maternal smiling up until 4 months, after which infants begin to
smile in anticipation of the mother’s smile; infant smiles are more likely to occur in par-
ticular contexts and not others (e.g., in the climax rather than the setup of a peek-a-boo
game) (Fogel, Nelson-Goens, Hsu, & Shapiro, 2000; Messinger, Fogel, & Dickson,
2001). On the other hand, we have published qualitative research on mother-infant smil-
ing that shows how highly variable such sequences can be. Not only that, facial forms
of smiling, barely noticeable differences in the “intonation” of the expression but mean-
ingful to the participants, reflect the playfulness and creativity of the underlying dynam-
ics (Fogel, Nwokah, & Karns, 1993; Pantoja, Nelson-Goens, & Fogel, 2001). Neither
of these descriptions is the “right” or “correct” one. Rather, they reflect different points
of view of the observers and different processes of engagement with the data: one more
quantitative and the other more qualitative.
Our research attests that process is much more dynamic and more difficult to de-
scribe than structure. No behavior emerges fully formed from the brain without being
subject to conditions in the periphery of the body and in the local environment in the
very act of formation (Thelen & Smith, 1994). Words, gestures, and expressions can
be altered in their shape, intonation, size, explicitness, duration, clarity, force, and on
many other dimensions depending upon the ongoing and simultaneous flow of com-
municative actions. This is the so-called continuous process model of communication,
which is contrasted with a discrete state model of communication that is based on se-
quence rather than process (Fogel, 1993; King, 2004; Shanker & King, 2002).
These co-dynamics cannot always be modeled as a linear sequence. This is be-
cause, in some cases, communication functions via information (i.e., meaning-making)
rather than by a computation of physical or temporal parameters (Pattee, 1987). Facial
expressions, for example, dynamically alter the behavior of social partners. A tiny
14 ALAN FOGEL
facial movement requiring little energy can induce large expenditures of movement en-
ergy in the social partner, as when a smile elicits a partner’s heart rate change and ini-
tiates movements of approach. Intracellular communication via the different sequences
of bases in DNA and neural communication via different neurotransmitters are other
examples of informational dynamic systems (Capra, 1996; Oyama, 1985; Pattee, 1987).
This information approach has an emphasis on the mutuality between constituents
which change as they enter into relational processes, altering their identities in order
to establish the ground for a relationship. A facial expression, such as a smile, does not
contain discrete information about the smiler. Rather, the meaning of the smile de-
pends upon the relationship between the smiler and the partner. People do not typi-
cally smile unless the partner is perceived as receptive to opening that line of emo-
tional communication.
In digital and electronic systems, information is usually thought of as discrete bits
having a concrete value (either “on” or “off” in a binary system typical of most com-
puters). A dynamic system, however, requires a completely different conceptualization
of information that is not fixed in advance and not “transmitted.” Rather, information
is created in the process of communication and is always dynamically related to the
current state of the entire developing system (Fogel, 1993; Oyama, 1985). In other
words, meaning making is the outcome of a finite process of engagement.
In another example, long-term social partners develop between them informational
attractors involving unique patterns of speech and expression not shared outside the
relationship. Words and gestures of endearment for a romantic couple (sweetie, lover,
honey, etc.) mean (are informed by) the entire history of their communication, re-
creating particular feelings and perhaps further states of intimacy. Yet, words and ges-
tures are not fixed in form and usage. “Honey” can be spoken with love, anger, or im-
patience depending dynamically on the situation. “Honey,” while meaningful to the
partners, does not always mean the same thing because the information is created in
the moment of dynamically unfolding feelings and actions.
Sequence vs. Process at the Macrolevel (Level 2 Change)

Attractors at the macrolevel grow out of these co-dynamics at the microlevel and re-
flect qualitatively different modes of system organization (Kelso, 2000). Furthermore,
one of the tenets of dynamic systems theory is that out of ordinary variability (Level 1
change), there sometimes arise changes that are more salient, different, or innovative
(Level 2 change). Changes at Level 2 are innovations, perceived as different from the
ordinary variability of Level 1 change. Innovations are changes that play a different role
in the complex system than ordinary variability. They may precipitate a change from
one attractor to another, or even a developmental change (Level 3 change, see below)
in the entire system of attractors (Fogel et al., 2006a; Thelen & Smith, 1994).
No simple numerical index can fully describe the transition from one attractor to
another. The collective behavior of the states of H2O (i.e., ice, water, and steam) dif-
fer in quality. Ice has crystals and water does not. Water and steam have dynamic flow
patterns and stable ice does not. Although the different states can be represented by a
quantitative parameter, temperature or energy, this parameter does not in any way de-
scribe the complex dynamics at the micro- and macrolevels that constitute the differ-
ent states and the ways in which one state changes into another.
From a quantitative perspective, when a dynamic system is in a stable attractor, it
is in an energetically conservative mode where it maintains its stability. In order to
change from one attractor to another, for the system to re-organize, energy is required
to move the system from this stable state. As water is heated, for example, there is an
increasing disorganization of the water’s movements, a relatively chaotic state. At
some point, however, boiling water begins to form rolling patterns, a Level 2 change,
that more efficiently move the heat energy from the bottom of the vessel to the sur-
face of the water where it can convert to steam. The water finds a new pattern of self-
organization that most effectively dissipates the heat energy. In this kind of dissipative
system, new patterns of order—attractors—emerge as systems seek to conserve and
release energy in far from equilibrium states (Capra, 1996).
Because the ordinary variability (Level 1 change) of the microlevel system within
an attractor is dynamically changing in realtime, an innovation (Level 2 change) is a
“change in the pattern of change.” In informational terms, systems make transitions
when the change in the pattern of change is noticeable, that is, the change becomes in-
formative or meaningful to the constituents (Pattee, 1987). Information about system
change does not exist prior to the change, but rather is created in the moment when a
system “notices” a difference, what has been described in informational terms as “a
difference that makes a difference” (Bateson, 1975; Oyama, 1985).
Couples in a romantic courtship or dating relationship, for example, may maintain
a dynamically stable ordinary variability without any talk of a more serious commit-
ment. When such talk begins—about exclusivity or about marriage—it makes a very
big difference for the conduct of the ongoing ordinary variability. This innovation is
most likely to be germinated in the ordinary variability of the courtship relationship,
as partners may seek to make long-term meaning out of everyday exchanges. The sys-
tem begins to shift toward another kind of talk about that longer term commitment.
Once that new kind of talk is established, it becomes a new kind of ordinary variabil-
ity from which further innovations can be launched.
Sequence vs. Process in Developmental Change (Level 3 Change)

Developmental change is yet another level of the change process in social and be-
havioral systems, designated as Level 3 (Fogel et al., 2006a). At any given time, a social
behavioral system has a finite number of different attractors, such as different types of
play in the parent-child relationship. In development, the entire system of attractors—
the collective behavior of the system as a whole—changes. Developmental change is the
creation of new attractor patterns and the loss of others. Development is the destabiliza-
tion, re-organization, and re-stabilization of the collective system of historical attractors
(Fogel, 1993; Fogel et al., 2006a; Lewis, 1995; Thelen & Smith, 1994).
Another basic tenet of dynamic systems theory is that changes at the developmental
level grow out of changes at the micro- and macrolevels that occur through variations
and innovations. Some of these variations may increase the level of energy or infor-
mational variability beyond the boundaries of the existing attractors. These innovative
16 ALAN FOGEL
variations often occur spontaneously, such that development emerges from the activity
of the system itself (Fogel et al., 2006a; Thelen & Smith, 1994; van Geert, 1998). Dy-
namic systems, in other words, are historical. The available set of attractors serves as re-
sources for the system to create opportunities for developmental change. The same idea
is contained in Piaget’s (1954) thinking: that some chance discovery may eventually
change the existing system of schemes via assimilation and accommodation.
The problem of the emergence of new forms is at the very core of developmental
inquiry. How does something new emerge from something that has been there in rel-
atively stable form? Dynamic systems theory recognizes the emergence of innovation
or novelty as a fundamental feature of complex systems. Non-biological systems, such
as chemical reactions and the physical universe, develop over time because novel vari-
ability provokes the system into new stable attractors that are neither planned nor pre-
programmed (Laszlo, 2001; Prigogine & Stengers, 1984; Weimer, 1987). A growing
number of thinkers have embraced the idea that spontaneous emergence is at the heart
of behavioral and psychological change. In the behavioral sciences, this concept has
also been called discovery, creativity, construction of novelty, and transformation
(Carvalho & Pedrosa, 1998; Eckerman, 1993; Fogel, 1993; Gottlieb, 1992; 2003;
Lewis, 1995; Lock, 1980, 2000; Lyra, 1998; Mahoney & Moes, 1997; Nelson, 1997;
Overton, 2002; Schore, 2003; Stern, 1998; Thelen & Smith, 1994; Tronick, 1998;
Valsiner, 1997; 2001).
The indeterminacy in dynamic systems can produce historically unique trajectories
that partly account for the formation of individual differences (Fogel, 1990; Fogel &
Branco, 1997; Fogel, Lyra, & Valsiner, 1997; van Geert, 1997; Kellert, 1993; Thelen,
1990; Valsiner, 1997). Informational approaches to dynamic systems perspectives can
help us understand why historical changes in people, groups, or societies can never ex-
actly repeat, why every social system is unique, and why these differences are contin-
gent on the dynamics of the communication process and not always amenable to pre-
diction (Fogel, Lyra, & Valsiner, 1997; Gould, 1977).
Dynamic Systems Methods for the Study of System Change

The focus of dynamic systems theory is change. Research questions about change
dynamics can be formulated at all three levels of change. For any level, one can ask:
How does change occur? What mechanisms produce change? What conditions are
likely to promote the emergence of change? These questions may be cast in terms of
basic or applied research. Basic research might seek to uncover the processes of change
in naturally occurring social systems. Applied research—as in international policy,
therapeutic intervention, or education—may seek to uncover the basic principles of
change in order to promote desired changes in a system and avoid undesired changes.
Questions may be framed about the stability vs. instability of new attractor patterns
that emerge as a consequence of a naturally occurring or induced change process. Ed-
ucationally or therapeutically induced changes that do not last are less desirable than
ones that can be sustained over time. Research can seek to uncover the processes that
create lasting change as well as the processes that maintain systems in desirable states.
Does the emergence of new behavior patterns tend to suppress the old patterns or
to coexist with them? If a person is relieved of a phobic disorder or alcoholism through
therapy, is that phobia still lurking somewhere, ready to be reactivated under particular
environmental conditions? When a peace between warring nations is negotiated, under
what conditions will that peace last, and is there any likelihood that old hostilities will
re-appear?
Microgenetic Research Designs

The hallmark of dynamic systems research is the study of change while it is occur-
ring, instead of merely comparing “before” and “after” observations. The primary tool
for doing change research from a dynamic systems perspective is the microgenetic re-
search design (Fogel et al., 2006a; Lavelli, Pantoja, Hsu, Messinger, & Fogel, 2005;
Siegler, 1996). Microgenetic research designs are specifically intended to allow the re-
searcher to closely observe processes of change, instead of products or outcomes. Typ-
ically, some period is selected in which the system is expected to undergo a Level 2
or Level 3 change. Then observations are made on particular cases relatively fre-
quently before, during, and after the change in order to observe the relevant Level 1
changes that may contribute to the Level 2 or 3 change (see Figure 1).
Regardless of the researchers’ theoretical perspectives and the developmental do-
mains under investigation, microgenetic designs are defined by the following key
characteristics:
• Cases (particular systems of interest) are observed through a period of devel-
opmental change.
• Observations are conducted before, during, and after a period during which rapid
change in a particular domain occurs. That is, observation is not simply con-
t = observation interval
T = developmental interval
t < < T
FIGURE 1.
18 ALAN FOGEL
ducted before and after the change takes place. The change may be a sponta-
neous developmental change or it may be a planned intervention.
• There is an elevated density of observations within the transition period. That
is, observations are conducted at time intervals that are considerably shorter
than the time intervals required for the developmental change to occur. For in-
stance, if a developmental change takes place over several months, then obser-
vations should be conducted weekly or even more frequently.
• Observed behaviors are intensively analyzed, both qualitatively and quantita-
tively, with the goal of identifying the historical processes that give rise to the
developmental change.
The unit of analysis is one of the types of systems described earlier: intraindivid-
ual, interindividual, ecological, and sociocultural. In the interindividual system, for
example, as an individual develops, its relation to the external world changes, such
that its effective environment—the actual physical, biological, and social factors with
which it interacts—also changes. One of the challenges of systems research is to in-
terpret the concept of environment in such a way that it incorporates an appropriately
dynamic view of the changing relations between the developing individual and his or
her context. This requires observation across representative developmental contexts to
identify the range of behavioral capacities and developmental trends characteristic of
the organism-environment system.
Microgenetic research has the advantage of being able to trace the historical devel-
opment of change over time within the same system. The historical approach has been
applied using microgenetic research designs (Bruner, 1983; Fogel, 1990; Fogel et al.,
2006a; Granott & Parziale, 2002; Greenspan, 1997; King, 2004; Lavelli et al., 2005;
Overton, 2002; Rosenwald & Ochberg, 1992; Shanker & King, 2002; Siegler & Crow-
ley, 1991; Thelen & Smith, 1994; van Geert, 1998). These studies involve both quan-
titative tracking of developmental trajectories and qualitative analysis of life history
narratives that reveal developmental shifts in shared information relative to new be-
havior coordinations in interindividual systems.
Recent advances have given dynamic systems scientists new tools for the study of
change processes. There now exists a new class of statistical models called hierarchi-
cal linear models or multilevel models (Bryk & Raudenbush, 1992; Butt, Choi, &
Jaeger, 2005; Prosser, Rasbash, & Goldstein, 1991) that allow researchers to examine
developmental trajectories in microgenetic designs, made by tracking a key measure
over frequent observations, for the group as a whole and for each individual. There
have also been recent improvements in qualitative research methods, giving new cred-
ibility and rigor to the use of narrative descriptions of observed behavior and life his-
tory narratives (Denzin & Lincoln, 1994; Polkinghorne, 1995). These new quantita-
tive and qualitative methods fit perfectly with the focus of dynamic systems on change
over time in the qualitative macroscopic attractors.
In addition to observations of the natural evolution of systems, systems research
often includes systematic experimental intervention or manipulation to uncover and
identify the developmental resources necessary and sufficient to foster developmental
change. In the intraindividual and interindividual systems, these resources include
genes, cell and tissue interactions, sensory experience, diet and exercise, and social re-
lations with conspecifics, to name but a few.
Dynamic systems experimental interventions or manipulations attempt to discover
the differences that make an impact by following developing systems as they develop
and add or subtract features of normally occurring experience or activity to identify
those developmental resources and their relationships that are necessary and sufficient
to foster change. These differences are hypothesized to be innovations that have the
potential to alter the system. The key idea is that the experimental alteration must
never be so drastic as to destroy the possibility for the system to transform over time.
The following are examples of dynamic systems experimental procedures (Gottlieb &
Lickliter, 2004; Lickliter & Honeycutt, 2003).
1. Experiential attenuation is when features of normally occurring experience are
removed from the developmental context, allowing researchers to better identify
how change is influenced by specific developmental resources in real time.
2. Experiential enhancement is when additional experience is added to the in-
dividual’s developmental context. This can be done by experiential substitu-
tion, in which normally occurring experience is replaced with a different form
of experience, or experiential displacement, in which the temporal relations
between features of experience are shifted or rearranged to allow deeper in-
sight into the history or process of specific reorganizations.
These types of manipulations and the evaluation of their consequences on devel-
opmental change are often used in parallel with one another to explore the complex-
ity and contingency of developmental processes. Combining microgenetic observa-
tion, which documents the process of change, with experimental manipulation, which
identifies the developmental resources contributing to change, provides a powerful
method for identifying the conditions under which change is most likely to occur.
In summary, dynamic systems research:
1. seeks primarily to probe the systemic and simultaneous linkages in the network
of relationships that sustain particular patterns of development over time;
2. aims to uncover the possible pathways that lead to changes in certain undesir-
able patterns; and
3. attempts to discover the processes required to sustain and foster the develop-
ment and maintenance of a healthy developmental trajectory, or a more desir-
able network of relationships needed for effective decision-making and posi-
tive social change.
In intervention research, for example, systems don’t get “fixed” or “cured” with a
simple formula. Rather, the dysfunctional system must be allowed to transform slowly
over time, systemically, into a more functional system. In dynamic systems science,
we seek to understand the laws of transformation.
Qualitative Research and the Role of the Observer

In the traditional quantitative research paradigm, one constructs hypotheses at the
beginning of the study, carries out the planned observational or experimental proce-
dure on a randomly selected sample from the population, derives numerical or cate-
gorical measures, analyzes the data in a manner directly driven by the hypotheses, and
20 ALAN FOGEL
makes an interpretation. If the original hypothesis needs to be altered, the researcher

returns to the population to test another sample with a variant of the procedure, or to
re-code the data based on a different set of observational categories.
One of the central principles of qualitative research, in contrast, is an iterative, cycli-
cal approach to interpretation during the data sampling, coding, and analysis. Thus, hy-
potheses, methods, and interpretations inform each other and change each other as a
process, creating an inductive spiral known as the hermeneutic circle (Bromley, 1986;
Robson, 1993). The observer, neither naïve nor objective, becomes an informed and in-
volved scientist. Hermeneutic approaches have been used in case study, ethnographic,
rhetorical, phenomenological, feminist, and symbolic interactional methods in the hu-
manities and behavioral sciences (Bernstein, 1983; von Eckartsberg, 1986; Erickson,
1992; Gaskins, 1994; Lather, 1991; McCall & Wittner, 1990; Rogoff, Mistry, Goncu, &
Mosier, 1993; Schwandt, 1994).
The principles of qualitative research are similar to the principles of qualitative, in-
formational dynamic systems. In qualitative research, the investigator is part of the sys-
tem being studied and engages with the system itself or with the data recorded from the
system. A dynamic system is continually in a process of change in which no part of the
system is permanently objective or fixed. Even so, in a dynamic system, semi-stable at-
tractors can persist as the system cycles through iterations that, from the observer’s per-
spective, appear to be similar to each other. Similarly, there are no fixed hypotheses,
categories, or conclusions in qualitative research. The qualitative scientist cycles itera-
tively through the data, each pass revealing a new working hypothesis and a new way
to categorize. Yet eventually, these working interpretations coalesce into a semi-stable
model of the system. The interpretation of the data becomes an attractor in a scientific
system of information and communication. The iteration, interpretation, and revision
continue until the observers feel confident of an emerging consistency and until new
interpretations do not emerge during the process of reading and re-reading the data,
which has been called the constant comparative method (Patton, 1990; Strauss &
Corbin, 1990).
Credibility is a criterion used in qualitative research methods to evaluate whether
the investigation successfully captures the meaning for the participants. Credibility
parallels the notion of internal validity in quantitative methods. Observers are deemed
more credible if they have a prolonged engagement with the data, the participants, and
a record of persistent observation of the phenomenon under investigation (Denzin &
Lincoln, 1994; Savage-Rumbaugh & Fields, 2000). Credibility is also enhanced if the
investigators share excerpts of the original videos or transcriptions to allow the read-
ers to make their own interpretations of the material (Rogoff et al., 1993).
These research methods are designed to create, via a meaning-making process, a
semi-stable view of what is informative or meaningful for the participants in the so-
cial process. “The inquirer constructs a reading of the meaning-making process of the
people he or she studies . . . The activity of understanding unfolds as one looks over
one’s respondents’ shoulders at what they are doing” (Schwandt, 1994, p. 123).
Meaning making is equivalent to information creation in a qualitative dynamic
system. To “make meaning” or to “create information” refers to the detection of a dif-
ference that makes a difference. How can scientists be assured that their interpretation
of the subjects’ meanings are in accord with those of the subjects? At issue is the
extent to which the warrant for interpretation of participants’ meaning is based on:
(1) the investigator’s subjective identification with the participants using empathy,
(2) the investigator’s construction of the participants’ meaning system within their
own sociocultural context, or (3) the investigator’s linking of the interpretation of a
particular case with the history of interpretations of other such cases within the liter-
ary genre that defines the investigator’s field of inquiry (Bradley, 1994; Jansen &
Peshkin, 1992; Keegan & Gruber, 1994; Schwandt, 1994; Toren, 1996).
In practice, qualitative research involves all three of these warranting procedures.
Empathy is used, but it has a limit as a scientific tool since our participants are not the
same as ourselves. Observers “can only approximate others’ experiences and so gain
only limited access to their knowledge” (Belenky, Clinchy, Goldberger, & Tarule,
1986, p. 113). This sense of incompleteness, the inability to fully define and catego-
rize another person, “marks the tragic, perpetually inadequate aspect of social re-
search” (Reinharz, 1984, p. 365). This is perhaps especially the case when we study
non-verbal infants, non-human animals, or people from very different cultures.
The limits of empathy point out the tragic fragility of scientific interpretations of
behavior and stand in sharp contrast to the hubris of objectivist approaches. In the ob-
jectivist approach, the measures of individuals and groups are presumed to accurately
stand for the real thing. What’s more, the appeal to a value-free, objective science adds
to the warrant for making subjects of research into objects of study, less than fully
alive beings. The qualitative scientist, by admitting the limits of inquiry and the inde-
terminacy of the findings, may seem weak and non-scientific by comparison.
Qualitative research, however, is a demanding exercise in not knowing, a deliber-
ate attempt to hold back from premature interpretation and to capture the process of
emergence. By making a conscious choice to stand outside of the objectivity of
method, the qualitative scientist becomes a living part of the system. At the risk of
seeming biased, qualitative researchers opt to expose the inherent dynamics of the so-
cial process. They accept as truth that which emerges from a process, and they see
their own work as a reflection of the way in which the universe actually operates.
Qualitative investigators can rely on the literature in their field only so far because
much of that work is done from a normative and seemingly objective point of view.
There are also limits to the researchers’ ability to step outside their own sociocultu-
ral and disciplinary point of view. The key to successful qualitative research, however,
is to clarify one’s limitations and to engage in an active meaning-making process by
which those perspectives and limitations are clarified. Again, the goal is not some ideal
answer or result, but rather to engage in a process of meaning making that is likely to
converge on an emergent description of the data. That description is accompanied by a
description of the limits of the observer, as well as evidence for their credibility.
Research Example
It is difficult to present a complete dynamic systems research example in the short
space of this paper. Many more detailed examples of qualitative dynamic systems
22 ALAN FOGEL
research using these principles can be found in Fogel et al. (2006a), King (2004), and
Fogel, King, & Shanker (2006). In addition, a description of applied dynamic systems
research methods is given in Fogel, Greenspan, King, Lickliter, Reygadas, Shanker &
Toren (2006).
Here, an excerpt is presented from Fogel et al. (2006a) that illustrates the descrip-
tion of a developmental (Level 3) change in one mother-infant dyad during the period
between 2 and 6 months. The attractors of interindividual relationships are regularly re-
curring patterns of communication called frames. Frames are segments of co-action
that have a coherent theme, that take place in a specific location, and that involve par-
ticular forms of mutual co-orientation between participants. Because frames recur re-
peatedly over weeks and months, they have the features of an attractor in a dynamic
system since they are reconstituted dynamically and dyadically on each reappearance.
Frames are semi-stable, lasting for only a finite period in an interindividual relation-
ship. They emerge at one point in time and dissolve or disappear at another point in
time. In a romantic partnership, for example, engagement or betrothal is a frame that
has a limited time of life between courtship and marriage.
The communication between the 13 mother-infant dyads in this study was video-
taped weekly during the 4-month observation period, meeting the conditions for a mi-
crogenetic research design (Figure 1). These videos were coded into four mutually ex-
clusive and exhaustive relationship frames. The social frame was coded when the
topic of communication was face-to-face play without objects. The guided object
frame was coded when the mother took an active role in demonstrating and scaffold-
ing the infant’s use of objects. The non-guided object frame was coded when the in-
fant played with objects without the mother’s direct assistance but with her ongoing
attention and verbal commentary. The social-object mixed frame was coded when el-
ements both of face-to-face play and guided-object play appeared at the same time, as
when a mother used a toy to touch the infant’s face or body while vocalizing in an ex-
pressive manner typical of the social frame.
The durations of each of the frames, measured as a percentage of time in the ob-
servation session (sessions lasted 10 minutes) is shown graphically in Figure 2 for one
dyad, Betsy and her mother. Notice that the durations of the social and the guided-
object frames decline over this period, while the not-guided-object frame and the
social-object mixed frame increase in duration.
In this example, the focus is on the sessions in which developmental change is
most rapidly occurring, sessions 7 and 8, in which Betsy is 17 and 19 weeks old. Dur-
ing session 6, Betsy for the first time reaches for an object while looking at it. In ses-
sion 7, the social frame declines dramatically. Betsy continues to look at her mother
and smile during the other frames, thereby maintaining a connection with her mother,
and thus blending the social frame into the other frames. This is seen especially in the
rapid increase in duration of the social-object mixed frame. Sessions 7 and 8 are the
first time that the not-guided object frame emerges as an entirely new frame, separate
from the other object-related frames, in which Betsy explores objects without the
mother’s assistance (as in the guided object and social-object mixed frame).
With the increasing growth of the not-guided-object frame, the guided-object
frame, while actually declining quantitatively over time, continues to develop qualita-
DYAD: 13
100
Social
90
Guided Object
80
Not-Guided Object
70 Social-Object Mixed
% of Session
60
50
40
30
20
10
0
1 2 3 4 5 6 7 8 9 * * *
Session
FIGURE 2.
tively. The mother, for example, gives Betsy certain objects and helps her hold them
when needed.
The not-guided-object frame and the guided-object frame now occur in quick succession.
Object manipulation follows a sequence composed of: Betsy actively mouthing an object
(i.e., the not-guided-object frame), the mother introducing a new object to Betsy followed
by Betsy reaching for and grasping the new object (i.e., the guided-object frame), and then
Betsy manipulating the second object, at times actively mouthing it (i.e., the not-guided-
object frame). This sequential patterning between the guided-object and the not-guided-
object frames appears to constitute a form of historical recapitulation in which an already
existing historical frame (i.e., the guided-object frame) is maintained and makes transitions
with a newly emergent frame (i.e., not-guided-object frame).
Now that Betsy is becoming more skilled at manipulating objects on her own, a new or-
dinary variability characterizing the social-object mixed frame also emerges during visits 7
and 8. The mother now uses the object Betsy is holding, making it kiss Betsy’s face without
taking the object from her. It is as if Betsy is playing the object-touch games herself. Both
Betsy and her mother are also becoming more serious, smiling and laughing relatively little
and producing fewer vocalizations. The mother, for instance, uses far fewer sound effects
with objects during visits 7 and 8. The impression the observer gets is that the social-object
mixed frame is gradually becoming transformed as the not-guided-object frame emerges as
a new and distinct frame. In fact, certain characteristics of the not-guided-object frame (such
as helping Betsy play the object-touch games herself) appear to permeate the social-object
mixed frame. (Fogel et al., 2006a)
These two sessions not only show a quantitative change in the frame durations, but
there was also a qualitative change in the pattern of organization, both at the microlevel
within the frames and the macrolevel of sequencing between the frames for Betsy and
her mother. This complex system of linked changes constitutes a developmental (Level
3) change. The developmental change is not merely in the fact that the not-guided-
24 ALAN FOGEL
object frame emerges for the first time, but rather because the whole system of frames
seems to shape-shift in order to give birth to the new frame. All these changes are oc-
curring simultaneously, as a dynamic process rather than a simple sequence.
The not-guided-object frame begins to pervade these sessions with the “support” of the
guided-object frame and the social-object mixed frame. Compared to previous sessions, all
of the observed frames (i.e., not-guided-object frame, guided-object frame, and social-
object mixed frame) undergo coordinated changes as reflected by the emergence of a new
ordinary variability for each of these frames. Specifically, as Betsy becomes more object-
focused and fascinated with the new activity of examining the objects around her, the
mother adjusts her object-oriented behaviors and begins providing support to her infant’s
object exploration by handing them to Betsy.
The not-guided-object frame begins to become elaborated into a fully developed frame
as Betsy spends increasing amounts of time manipulating objects. This constitutes a newly
emergent frame that arises out of the innovations (Level 2 change: the mother places objects
in Betsy’s hands) within the guided-object frame and social-object mixed frame during ses-
sions 4, 5, and 6. At the same time, the guided-object frame expands its forms as illustrated
by the increasing variability in the way the mother presents objects to Betsy. The social-
object mixed frame also changes from its earlier quality of enjoyable social play to becom-
ing more focused on Betsy’s more serious examination of objects.
Furthermore, the dyad’s new ordinary variability (Level 1 change) during sessions 7 and
8 includes a patterned integration of the guided-object frame and the not-guided-object frame.
In this case, it is as if frames (i.e., guided-object frame and not-guided object frame) are blend-
ing together at the same time that a historical dynamic is recapitulated by the dyad.
All of these processes—the simultaneous re-organization of each of the frames in relation
to each other and the emergence of a new frame in the context of the blending and recapitula-
tion of frames—constitute what we consider to be the conditions of a developmental change
(Level 3 change). Innovations (Level 2 change), as seeds for developmental change, alter the
ordinary variability within frames on later occasions. This alteration, however, is of the same
kind as the innovation when the infant becomes more active across multiple modalities. In the
case of this developmental change, however, the entire pattern of communication changes
across the whole system: all the frames and transitions are involved. For reasons we do not yet
understand, the build-up and elaboration of innovations seems to reach a critical point at which
time the “old” or historical system can no longer contain the innovations within ordinary vari-
ability. At this time, the system spontaneously shifts to a new system-wide organization that
includes new frames, creative blending of old frames, and new actions within frames. It is im-
portant to note that we did not observe any single innovation or event that precipitated the de-
velopmental transition. (Fogel et al., 2006a)
Although the more detailed account cannot be given here, this excerpt shows the focus
on history and meaning, the role of the observer, and the complexity of the co-actions
across all three levels of change in the system. It also shows that a qualitative analy-
sis provides something that cannot be gleaned from the quantitative description alone.
The two methods, quantitative and qualitative, support and complement each other as
a description of the developmental change process.
Conclusions and Implications

If dynamic social systems are fluid, changing, emergent, and yield created infor-
mation in a meaning-making process, then dynamic systems research best serves sci-
entific discovery by substantiating these same processes in the method. Applying the
standards of research objectivity, with fixed measures and a priori hypotheses can
only limit and diminish the phenomenon under study. As a complement to qualitative
investigation, quantitative measures can enhance and deepen our understanding of
systems phenomena. Quantitative measurement and statistical analyses are seen as
one way of understanding, rather than the only way of understanding. Qualitative sys-
tems research seeks to place the scientist in the system, not knowing the answer. To
become a credible witness, the scientist works toward an emergent understanding, al-
lowing the reader to be part of the discovery process. In the end, the scientist and the
reader understand more, while remaining immersed in the boundless possibilities of
not knowing.
The closest disciplines to qualitative dynamic systems research are history, biog-
raphy, and narrative analysis. The historian tracks multiple and related processes
(frames) through time and attempts to understand how their co-actions and co-changes
illuminate, say, the processes occurring at the beginning or ending of a war. Dynamic
systems research can add to this enterprise by the use of the qualitative and quantita-
tive methods and the explicit decomposition of the system into levels of change, as de-
scribed in the above example.
Dynamic systems are inherently not predictable. The start or end of every war is dif-
ferent because the co-dynamics are always different and changing. Once a system en-
ters into a developmental change period, as in sessions 7 and 8 in the above example,
change is often rapid, spontaneous, unpredictable, and probably unstoppable. Notice in
Figure 2 that the developmental shift occurs in only 2 or 3 sessions. In the periods be-
fore and after sessions 7 and 8, the durations of the frames remain relatively stable.
Developmental change carries a certain momentum such that once the system
reaches a critical point, there is no turning back. On the other hand, in the larger study
of which this example is a part (cf., Fogel et al., 2006a), we found in all of our dyads
signatures of the impending change process in the weeks before it actually occurred:
the innovations that began to shake the system loose from its ordinary variability.
If this research model could be applied to social, economic, and political change
on a set of national and international cases, to take one example, it may be possible to
uncover the underlying dynamics that foreshadow (but not predict) a more precipitous
change. Once some of these predisposing factors are identified in naturalistic studies,
dynamic systems experiments could be done in which those factors are attenuated or
enhanced to diminish the likelihood of less desired subsequent changes and to enhance
the likelihood of more desired ones.
The same model of research could be applied to therapeutic and educational inter-
ventions, to the emergence of famine, to epidemics and other health crises, and to the
deterioration and wellness processes of the human body. The hope is to discover the
laws of change and the dynamics of transformation. How much can a system take be-
fore it breaks down? What is the process by which transformation occurs? Can devel-
opmental change be facilitated even during the rapid (and presumably irreversible) pe-
riod of change, or only earlier during the pre-change period? Why do some individuals
and systems seem to resist change and others embrace change? What are the differ-
ences that make a difference for a developmental change in any particular system?
26 ALAN FOGEL
The tools are now available to address these types of research questions, but these
methods are slower and cost more than conventional research. This is because it is nec-
essary to wait for the change to unfold, and many observations must be made in order
to track the change process. The gain in understanding, however, is likely to be high.
Qualitative dynamic systems research is ideal for translational applications. Mod-
els that are expressed in terms of statistical interactions between quantitative variables
are probabilistic and often far removed from the everyday process of meaning making
as a social system. New models and interventions that rely on an understanding of the
informational dynamics of the change process could be immediately applied to the
work of practitioners and participants because these models are expressed in terms of
the meanings that are already present in the system.
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Early Family Trauma and the Ontogeny of
Glucocorticoid Stress Response in the Human
Child: Grandmother as a Secure Base
Mark V. Flinn
Department of Anthropology and
Department of Psychological Sciences
University of Missouri
FlinnM@Missouri.edu
David V. Leone
Department of Anthropology
University of North Carolina
Abstract: Loss of a parent by death or divorce is among the most traumatic experiences
faced by a human child. Exposure to early family trauma (EFT) can have long-term effects
on the limbic hypothalamic-anterior pituitary-adrenal cortex (HPA) axis and other compo-
nents of neuroendocrine stress response. Because the HPA system has important immuno-
modulatory functions, children that have endured difficult family social conditions during
development may be at higher risk for immune dysfunction and other health problems.
Here we investigate the mediating effects of grandparental relationships, mostly maternal
grandmothers, on the ontogeny of HPA stress response among EFT children.
Sample and methods: A longitudinal eighteen-year study (1988–2006) of child health in

a rural community on the island of Dominica provides sequential biyearly data on salivary
cortisol, morbidity, growth, and social environment (N= 282 children, 26,738 saliva sam-
ples from children + 5,470 saliva samples from their parents and other kin, 89,109 health
observations, 46,788 anthropometric measurements, 42 months of residence in the com-
munity studying social environment). Patterns of cortisol response, extent of care from
grandparents, morbidity, growth, and immune function are examined for associations with
trauma at different periods during development.
Results: Grandparents are a common and important mediator of child wellbeing in this
community. EFT children with extensive grandparental care are more likely to recover nor-
mal HPA function than are EFT children with little or no grandparental care. Lengthy infor-
mal discussions with children and their caregivers over the past 18 years suggest that grand-
parents are important components of their social worlds, including roles as temporary and
permanent replacements for parents. EFT children with low contact rates with grandparents
have more erratic cortisol profiles, higher morbidity, more growth disruptions, and more be-
havioral problems than EFT children with extensive grandparental care.
31
32 MARK V. FLINN AND DAVID V. LEONE
Summary and conclusions: Grandparents appear to have significant mediating effects on

child development in this population. Intensive grandparental care is positively associated
with lower average cortisol, normal growth, and lower morbidity. No significant associ-
ations were found between grandparental care and parasite loads or average fluctuat-
ing asymmetry. Overall these results suggest the importance of grandparents, especially
maternal grandmothers, for children who have experienced early trauma in their family
environments.
Introduction: Grandparenting as an Evolved Human Adaptation

“I love my granbaby more than anything God put here on this earth” . . . “I love
Mama”1 . . . mutual hug and laugh. (Bwa Mawego2 grandmother and her granddaugh-
ter, from MVF fieldnotes, Oct. 10, 1992).
Grandparents and grandoffspring share 25% of their genes identical by descent, a
significant opportunity for kin selection. Few species, however, live in groups with
multiple overlapping generations of kin. Fewer still have significant social relation-
ships among individuals two or more generations apart—such as elephants (Lee,
1987), some cetaceans (Mesnick, Evans, Taylor, Hyde, Escorza-Trevino, & Dizon,
2003; Whitehead, 2003), and some primates (Goodall, 1986; Lancaster & King, 1992).
Humans appear rather exceptional in this regard. Grandparenting is cross-culturally
ubiquitous and pervasive (Murdock, 1967; e.g., Clarke, 1957; Sear, Mace, & McGre-
gor, 2000). Our life histories allow for significant generational overlaps, including an
apparent extended post-reproductive stage facilitated by the unique human physiolog-
ical adaptation of menopause (Alexander, 1974, 1987; Hawkes, 2003; Williams, 1957).
The neuroendocrinological mechanisms guiding attachment processes in grand-
relationships—such as the intense affiliation described in the anecdote above—are un-
certain. The maternal neuropeptide oxytocin is a likely candidate. Regardless, the sig-
nificance of emotional bonding between grandparents and grandchildren is beyond
doubt. The evolved functions are uncertain, but likely involve the extraordinary im-
portance of long-term extensive and intensive investment for the human child. The
emotional and cognitive processes that guide grand-relationships evolved because
they enhanced survival and eventual reproductive success of grandchildren.
Throughout human evolution, most children were likely to have benefited from the
extra care provided by grandparents in addition to the investment by the immediate
family. Children that for whatever reasons were not receiving much care from one or
both parents were at risk, and, therefore, especially dependent upon help from grand-
parents. In addition to the physical basics of food, protection, and hygienic care, de-
velopment of the human child is strongly influenced by the dynamics of the social en-
vironment (Dunn, 2004; Hetherington, 2003a, 2003b; Hinde & Stevenson-Hinde,
1987; Konner, 1991). Monitoring neuroendocrine stress response systems can provide
useful insights into how children are coping with social challenges. Here we first re-
1. This three year-old child referred to her grandmother as “Mama,” and her mother by her given name.
2. All place names and research participant names used here are pseudonyms to protect privacy rights.
Early Family Trauma and the Ontogeny of Glucocorticoid Stress Response 33
view the potential functions of physiological stress response to stimuli in the social en-
vironment. We then investigate the effects of grandparents on the ontogeny of stress
response among children that have endured the loss of a parent by death or separation.
The Paradox of Psychosocial Stress

Humans elevate levels of the stress hormone cortisol in response to social chal-
lenges (Dickerson & Kemeny, 2004; Gunnar, Bruce, & Donzella, 2000). The mag-
nitude and temporal pattern of cortisol release by the limbic hypothalamic-anterior
pituitary-adrenal cortex (HPA) system can be altered by traumatic early experiences
(Heim, Newport, Heit, Graham, Wilcox, Bonsall, Miller, & Nemeroff, 2000; Mirescu,
Peters, & Gould, 2004; Weaver, Cervoni, Champagne, D’Alessio, Sharma, Seckl,
Dymov, Szyf, & Meaney, 2004). High levels of the primary stress hormones cortisol,
corticotropin releasing hormone (CRH), and epinephrine may be toxic to developing
dendrites, neurons, and receptors in the hippocampus and other brain regions that are
involved in the negative feedback loop for cortisol regulation (Chen, Bender, Brun-
son, Pomper, Grigoriadis, Wurst, & Bararn, 2004; Sapolsky, Romero, & Munck,
2000). High levels of cortisol may also affect sensitivity of fear responses mediated
by the amygdala. Hence early trauma may lead to permanent HPA-cortisol dysregula-
tion. Because the HPA system has important immuno-modulatory functions (Ader,
Felten, & Cohen, 2006; Sapolsky, 2005), children that have endured difficult social
conditions during development may be at higher risk for immune dysfunction and
other health problems.
The sensitivity of the HPA system to social stimuli presents an evolutionary para-
dox: why release cortisol if it has negative effects on health? We do not have good ex-
planations for why natural selection favored links between the neuropsychological
mechanisms involved with assessment of the social environment and the neuroen-
docrine mechanisms that regulate stress hormones. We also do not understand why
these links are modifiable during development, such that early traumatic experiences
may permanently alter hormone response to social challenges. And finally, we do not
understand what factors, such as social support, may subsequently ameliorate the neg-
ative effects of early trauma on stress response (Caldji, Tannenbaum, Sharma, Fran-
cis, Plotsky, & Meaney, 1998; Cameron, Champagne, Parent, Fish, Ozaki-Kuroda, &
Meaney, 2005; Francis, Diorio, Plotsky, & Meaney, 2002; Lupien, Fiocco, Wan,
Maheu, Lord, Schramek, & Thanh Tu, 2005).
We approach these questions from an evolutionary paradigm that integrates prox-
imate physiological explanations with ontogeny, phylogeny, and adaptive function
(Tinbergen, 1963). Here we first briefly review the idea that childhood is an adapta-
tion for coping with an increasingly complex and dynamic social and cultural environ-
ment. We then explore relations between physiological stress response and the on-
togeny of social competencies. We posit that one of the important functions of the
stress response system, in connection with emotional states such as fear or anxiety, is
to manage the direction of mental processes to solving specific problems (Ademec,
Blundell, & Burton, 2005; Flinn, 2006b, 2006d; Huether, 1998; Kaiser & Sachser,
2005; Meaney, 2001; Pitman, 1989; Rodriguez Manzanares, Isoari, Carrer, & Molina,
2005). For example, in the relatively straightforward prey-predator situation of a
gazelle smelling a lion, a “freeze” response, focused sensory acuities, and neurologi-
cal circuits for escape behaviors may be enabled. The human child may face more
cognitively challenging problems that use more information processing capacity, such
as complex social interactions (Roth & Dicke, 2005). For example, when dealing with
the challenge of making friends on the first day of school, a child needs to allocate her
cognitive efforts to the tasks at hand: prepare for immediate contingencies by recall-
ing salient information, enhancing relevant sensory input, and pre-activating circuits
for appropriate actions. Stress hormones may enable not only the acute responses to
such challenges, but facilitate their modification during development as well. Parents
and grandparents may play an important role in this dynamic interplay between stress
response to social challenges and the ontogeny of a child’s coping mechanisms by pro-
viding both security and information.
Hypotheses are evaluated with analyses of data from an 18-year study of child
stress in a rural community on the island of Dominica. The longitudinal depth, large
sample size (30,122 salivary cortisol measures from 282 children and their care-
givers), and naturalistic paradigm provide a unique research design for investigating
relations between social environment and ontogeny of stress response. Empirical
analysis is complicated by the pleiotropic nature of the key stress hormone cortisol.
Moreover, the Dominica study does not have neurological data, hence direct or strong
demonstrations of causal links among stress response, neural plasticity, family envi-
ronment, grandparental care, and ontogeny of social competencies are not possible.
Our initial objective here is to review a plausible model that links stress response
to the neural plasticity that enables adaptation to the dynamic human social environ-
ment. We then assess the effects of early family trauma on the ontogeny of stress re-
sponse, and the potentially ameliorative effects of grandparental care. Understanding
these relations may have significant consequences for child development and public
health because it could provide new insights into associations among stress response,
social disparities, and perinatal programming, among other outcomes (Barker, 1998;
Dressler, Oths, & Gravely, 2005; Heim & Nemeroff, 2001; Maccari, Darnaudery,
Morley-Fletcher, Zuena, Cinque, & Van Reeth, 2003; Marmot, 2004).
HPA Stress Response to Social Events

Danny was roaming the Fond Vert area of the village with two of his closest
friends, James and Isaiah, on a rainy Saturday morning. They had eaten their fill of
mangoes, after pelting a heavily laden tree with stones for nearly an hour, taking turns
testing their skill at knocking down breakfast. Now Danny was up the cashew tree in
Mr. Pascal’s yard, tossing the yellow and red fruits to the smaller children below who
had gathered to benefit from this kindness. Suddenly the sharp voice of his stepfather
rang out from the nearby footpath. The bird-like chatter and laughter of the children
immediately stopped. Danny’s hand froze mid-way to its next prize, and his head
turned to face the direction of the yell with a mixed expression of surprise and fright.
Ordered down from the tree, Danny headed quickly home, head bowed in apparent
numb submission (vignette from MVF field notes, July 14, 1994). Danny’s salivary
cortisol level rose from 2.2 to 3.8 µg/dl in little more than an hour. That afternoon, his
secretory immunoglobulin-A levels dropped from 5.70 to 3.83 mg/dl. Three days later
he had common cold symptoms: runny nose, headache, and fever. His two compan-
ions resumed their morning play, exhibiting a normal circadian decline in cortisol, and
remained healthy over the next two weeks (Figure 1).
Danny had lost his father in a fishing accident when he was 3 years old. His rela-
tionships with his grandparents were not close; he visited them less than one hour a
week. His friend James also did not have a co-resident father, as a consequence of a
conjugal separation, but in contrast with Danny’s situation, James’ relationship with
his maternal grandmother was very close, as illustrated by the following vignette.
James was sitting contentedly sorting rice with Ma Tee-Jean, his maternal grand-
mother. He startled when I (MVF) kicked a rock on the path to forewarn them of my
approach into the household yard, and he inched closer to grandma, who put her arm
around him. James was dressed and ready for school. He had left his mother’s house
when an argument had broken out between his mother and stepfather last night, walk-
ing the 200 meters up the hill in the dark with his sister (MVF field notes, Sept 14,
1992). He was accustomed to this situation; James slept 44 out of 62 nights there in
this summer of 1992, splitting his time between both households for most of the past
10:10 July 13 10
3 17:35 July 17
Ordered down
Runny nose,
from tree
cough, oral
2 temp. = 101.2°F
s-IgA mg/dl
1
Cortisol z-score
–1
–2 0
13 14 15 16 17
July
FIGURE 1. Morning, mid-morning, and afternoon cortisol levels of Danny

and his two friends during summer 1994. Danny’s cortisol levels were ele-
vated and his s-IgA levels diminished after being reprimanded by his step-
father on the morning of July 13. Cortisol z-scores are standardized by five-
minute intervals since wake-up time to control for the circadian patterns of
cortisol; s-IgA levels are the raw values. Danny exhibits symptoms of an
upper respiratory infection with slight fever on the afternoon of July 20.
four years, since his father had left when James was three years old and his stepfather
had slowly moved in. James had always been close to his grandmother—whom he
called “Mama”—as well as his mother—whom he called by her given name Lily.
James’ cortisol levels were often elevated by family conflicts, but the solace he usu-
ally found at his grandmother’s often resulted in a return to normal levels.
These anecdotal case examples contribute to a common pattern. Children in this
rural Dominican community are more than twice as likely to become ill during the
week following a stressful event than during a week when they had not recently expe-
rienced any significant stressors (Flinn & England, 2003). Chronic elevation of corti-
sol levels may have negative consequences for health (Cohen, Doyle, Turner, Alper &
Skoner, 2003; Maier, Watkins, & Fleschner, 1994; Marmot & Wilkinson, 1999;
Mason, Buescher, Belfer, Artenstein, & Mougey, 1979). Morbidity and mortality rates
for children in the stressful environments of orphanages and hospitals, if lacking the
evolutionarily-normal intimacy and social contact of the family, can be a significant
public health concern worldwide. It is not lack of food or hygienic care, nor just the
occurrence of traumatic events that affect child health, but the lack of social support,
including parental warmth and other factors that influence emotional states (Belsky,
1997; Davidson, Jackson, & Kalin, 2001; Field, Diego, Hernandez-Reif, Schanberg,
& Kuhn, 2003). Why should this be so? Why do social interactions, and a child’s per-
ceptions of them, affect stress physiology and morbidity? And, more generally, why is
the social environment of such paramount importance in a child’s world? From the
Tinbergen perspective, these “why?” questions ultimately involve understanding the
evolutionary design of the ontogeny of the mind and brain of the human child (e.g.,
Belsky, 1997; Bjorklund & Pellegrini, 2002; Gilbert, 2005).
In Danny and James’ village, located on the east coast of the island of Dominica
where I have lived and studied part-time over the past eighteen years, most of a child’s
mental efforts seem focused on negotiating social relationships with parents, siblings,
grandparents, cousins and other kin, friends, teachers, bus drivers, neighbors, shop own-
ers, and so forth. Foraging for mangoes and guavas, hunting birds, or even fishing in the
sea from rock cliffs, are relatively simple cognitive enterprises, complicated by conflicts
with property owners, and decisions about which companions to garner and share calo-
ries with. The mind of the child seems more concerned with solving social puzzles than
with utilitarian concerns of collecting food. Other populations may have more difficult
subsistence practices that require more extensive learning (e.g., Bock, 2005), but the so-
cial chess game nonetheless appears ubiquitous and cognitively demanding in all cul-
tures (Blurton-Jones & Marlowe, 2002; Hewlett & Lamb, 2005), as it likely was during
human evolutionary history (Adolphs, 2003; Alexander, 1979, 1989; Baumeister, 2005;
Bowlby, 1969, 1973; Flinn, Geary, & Ward, 2005; Hinde, 1974).
Complex sociality appears to have been an important selective pressure shaping
the uniquely human combination of physically altricial but mentally and linguistically
precocial infancy, extended childhood, and extended adolescence, enabled by exten-
sive bi-parental and kin care (Alexander, 2005; Geary & Flinn, 2002; Flinn & Ward,
2005). Physiological stress response may help guide both the acute and long-term neu-
rological plasticity (Huether, Doering, Ruger, & Schussler, 1999) necessary for adapt-
ing to the dynamic aspects of human sociality (Flinn, 2006b). Grandparents may pro-
vide important advice and enhance a secure base for the stressful tasks involved in the
development of social competencies.
Evolution of the Extended Family

as a Nest for the Child’s Social Mind
The human family is extraordinary and unique in many respects (Alexander, 1989,
2005; Flinn, Ward, & Noone, 2005; Geary & Flinn, 2001; Lancaster & Lancaster,
1987). Humans are the only primate species to live in multi-male groups with com-
plex coalitions and extensive paternal care. The altricial infant is indicative of a pro-
tective environment provided by intense parental and alloparental care in the context
of kin groups (Alexander, 1990a; Chisholm, 1999; Hrdy, 1999, 2005; e.g., Ivey, 2000).
The human baby does not need to be physically precocial. Rather than investing in the
development of locomotion, defense, and food acquisition systems that function early
in ontogeny, the infant can work instead towards building a more effective adult phe-
notype. The brain continues rapid growth, and the corresponding cognitive competen-
cies largely direct attention toward the social environment. Plastic neural systems
adapt to the nuances of the local community (Alexander, 1990b; Bjorklund & Pelle-
grini, 2002; Geary & Bjorklund, 2000; Geary & Huffman, 2002). In contrast to the
slow development of ecological skills of movement, fighting, and feeding, the human
infant rapidly acquires skill with the complex communication system of human lan-
guage (Bloom, 2000; Fisher, 2005; Pinker, 1994; Sakai, 2005). The extraordinary
information-transfer abilities enabled by linguistic competency provide a conduit to
the knowledge available in other human minds. This emergent capability for intensive
and extensive communication potentiates (and presumably co-evolved with) the social
dynamics characteristic of human groups (Deacon, 1997a, 1997b; Dunbar, 1997,
1998). The recursive pattern recognition and abstract symbolic representation central
to linguistic competencies enable the open-ended, creative, and flexible information-
processing characteristic of humans—especially of children.
Parents and other kin such as grandparents may be especially important for the
child’s mental development of social and cultural maps because they can be relied
upon as landmarks who provide relatively honest information. From this perspective,
the evolutionary significance of the human family in regard to child development is
viewed more as a nest from which social skills may be acquired than just as an eco-
nomic unit centered on the sexual division of labor. An integration of the attachment
paradigm (Bowlby, 1969; Lamb, 2005; Lamb, Bornstein, & Teti, 2002) with ap-
proaches emphasizing relationship networks (e.g., Kerr & Bowen, 1988; Suomi,
2005) would be congruent with this evolutionary logic (Belsky, 1997).
Grandparental Relationships
Caregiving by individuals other than parents provides important benefits for in-
fants and juveniles in a variety of taxa. “Helpers” in birds, rodents, social carnivores,
elephants, and non-human primates enhance growth and survival (e.g., Alexander,
Noonan, & Crespi, 1991; Brown, 1987; Clutton-Brock, 2002; Lee, 1987; Mitani &
Watts, 1997). Kin selection and reciprocity appear to provide the evolutionary func-
tions for non-parental care providers. Among primates, intensive allomaternal care-
giving (e.g., feeding, carrying) is common in the callitrichids (e.g., Goldizen, 1987)
and the colobines. Allomaternal care among the cercopithecines (e.g., Fairbanks,
1990; Maestripieri, 1994) and hominoids (e.g., Goodall, 1986; Nishida, 1990) is usu-
ally limited to protection from conspecifics and predators. Practice care is generally
common among nulliparous females in social species (e.g., Hrdy, 1999). The preva-
lence of extensive alloparental care among humans (e.g., Flinn, 1989; Lahdenpera,
Lummaa, Helle, Tremblay, & Russell, 2004; McKenna, 1982; Sear, Mace, & McGre-
gor, 2000, 2003; Silk, 1990; Strassmann & Clarke, 1998; Tronick, Morelli, & Winn,
1987; Tronick, Morelli, & Ivey, 1992), particularly the importance of grandparents for
direct care (Alexander, 1979; Hawkes, 2003), represents a strong divergence from our
closest primate relatives.
The conditions responsible for the evolution of extensive alloparental care in hu-
mans are likely to include the importance of localized kin groups, altricial infants, pro-
longed childhood, extended generational overlap, and the cultural transmission of in-
formation (Alexander, 1989; Coe, 2003; Flinn & Ward, 2005; Geary & Flinn, 2001;
Hrdy, 2005). Grandparents appear to be the most significant of potential alloparental
caregivers (Hrdy, 2005).
The informational arms race that characterizes human social competition involves
substantial novelty (Flinn, 2004, 2006a; Flinn & Alexander, 2006; Flinn & Coe, 2006)
and hence requires unusual phenotypic plasticity. Although knowledge of the basic
neuroanatomical structures involved with human social aptitudes has increased dra-
matically (e.g., Allman, 1999; Damasio, 2003; Gallese, 2005; Moll, Zahn, de Oliveira-
Souza, Krueger, & Grafman, 2005), the mechanisms that guide their ontogeny remain
uncertain. Neuroendocrine stress response to stimuli in the social environment may
provide important clues.
Stress Hormone Profiles as an

Assessment of Caretaking Environment
Changing, unpredictable environments require adjustment of priorities. Growth,
immunity, digestion, and sex are irrelevant while being chased by a predator (Sapol-
sky 1994), or coping with a traumatic social event. Emergencies—large and small,
good and bad—perceived by the brain stimulate a variety of neuroendocrine systems.
Hundreds of different endogenous chemicals—steroid and peptide hormones, neuro-
transmitters, cytokines, and so forth—are released from secretory glands and cells in
response to information received and processed by the central nervous system (CNS).
The movement of these chemicals in plasma and other intercellular fluids communi-
cates information among cells and tissues, helping the body to respond appropriately
to varying environmental demands.
Physiological stress responses affect the allocation of energetic and other somatic
resources to different bodily functions via a complex assortment of endocrine and neu-
roendocrine mechanisms. Stress hormones help shunt blood, glucose, products of the
immune system, and other resources to cells and tissues necessary for the task at hand.
Chronic and traumatic stress can diminish long-term health, evidently because re-
sources are diverted away from important health functions, including cellular repair,
building muscle mass, immune response, and neuromodulation (Korte, Koolhaas,
Wingfield, & McEwen, 2005; Selye, 1976). Stress during childhood may be particu-
larly harmful because of the additional demands of growth and development, espe-
cially of the CNS (Rutter, 1991).
During the first few years of life the human brain more than doubles in size via an
extraordinary spurt of cell growth, migration, specialization, remodeling, and pruning.
The brain consumes almost half of the infant’s resting caloric requirements. The thy-
mus and other parts of the immune system undergo a similarly dramatic transforma-
tion, preparing defenses against a nearly infinite variety of pathogens, while selecting
out responses to the numerous molecular fingerprints of self-tissues. Even under the
best of circumstances successful outcome of these complex ontogenetic trajectories
would seem miraculous; the developing child, however, often faces a most imperfect
environment. Emotional and physical stressors—such as abuse, neglect, parental di-
vorce, strenuous work, exogenous toxins, inconsistent punishment, infectious disease,
and malnutrition—are powerful stimulants of physiological stress response with po-
tential effects on brain and immune development (e.g., Boyce, Adams, Tschann,
Cohen, Wara, & Gunnar, 1995; Fukunaga, Mizoi, Yamashita, Yamada, Yamamoto,
Tatsuno, & Nishi, 1992; Maccari et al., 2003; McEwen, 1995, 1998). But even com-
mon, everyday activities may be important.
Physiological responses to environmental stimuli that are cognitively perceived as
“stressful” are modulated by the limbic system (amygdala and hippocampus) and basal
ganglia that interact with the sympathetic and parasympathetic nervous systems and
several neuroendocrine axes. Here we are primarily concerned with what has tradition-
ally been termed the limbic hypothalamic-anterior pituitary-adrenal cortex system
(HPA). The HPA system affects a wide range of physiological functions in concert with
other neuroendocrine mechanisms and involves complex feedback regulation. The
HPA system regulates glucocorticoids, primarily cortisol, which is normally released
in seven to fifteen pulses during a 24-hour period (for reviews see: de Kloet, Sibug,
Helmerhorst, & Schmidt, 2005; Ellis, Essex, & Boyce, 2005; Gold & Chrousos, 2002;
Gray, 1982, 1987; McEwen, 1995; Sapolsky, 1992a, 1992b; Weiner, 1992).
Cortisol is a key hormone produced in response to physical and psychosocial stres-
sors in humans. Cortisol modulates a wide range of somatic functions, including:
(a) energy release (e.g., stimulation of hepatic gluconeogenesis in concert with
glucagon and inhibition of some effects of insulin), (b) immune activity (e.g., control
of inflammatory response and the cytokine cascade, particularly Il-2), (c) mental
activity (e.g., alertness, memory, and learning), (d) neural modification, (e) growth
(e.g., inhibition of growth hormone and somatomedins), and (f) reproductive function
(e.g., inhibition of gonadal steroids, including testosterone). These complex multiple
effects of cortisol muddle understanding of its adaptive functions. The demands of en-
ergy regulation must orchestrate with those of immune function, and so forth. Recep-
tor differentiation, competition with mineralocorticoids for binding sites, and other
mechanisms enable localized targeting (e.g., glucose uptake by active versus inactive
muscle tissues, neuropeptide directed immune response, modulation by antiglucocor-

ticoids, and cell-specific interactions with macrophages) of the above general physio-
logical effects (e.g., de Kloet et al., 2005). Cortisol regulation allows the body to re-
spond to changing environmental conditions by preparing for, and recovering from,
specific short term demands (Mason, 1971; Munck, Guyre, & Holbrook, 1984).
These temporary beneficial effects of glucocorticoid stress response, however, are
not without costs. Persistent activation of the HPA system is associated with immune
deficiency, cognitive impairment, inhibited growth, delayed sexual maturity, damage
to the hippocampus, enhanced sensitivity of amygdala fear circuits, and psychological
maladjustment (Ader, 2001; Dunn, 1995; McEwen & Magarinos, 1997; Sapolsky,
1996). Deleterious effects of high cortisol to neurons in the hippocampus appear to
occur after saturation of the high affinity mineralocorticoid receptors (MRs) and sub-
sequent extensive binding of the glucocorticoid receptors (GRs) (de Kloet et al., 2005;
Reul & de Kloet, 1985). Chronic stress may diminish cellular energy (Sapolsky, 1991;
Sapolsky & Stein, 1989) and produce complications for autoimmune protection
(Munck & Guyre, 1991). Stressful life events—such as divorce, death of a family
member, change of residence, or loss of a job—are associated with infectious disease
and other health problems during adulthood (Cohen et al., 2003; Maier et al., 1994;
Marmot & Wilkinson, 1999).
Current psychosocial stress research suggests that cortisol response is stimulated
by uncertainty that is perceived as significant and for which behavioral responses will
have unknown effects (Dickerson & Kemeny, 2004; Kemeny, 2003; Kirschbaum &
Hellhammer, 1994). In a child’s world, important events are going to happen. The
child does not know how to react so as to achieve desired outcomes, but is highly mo-
tivated to figure out what should be done. Cortisol release is associated with unpre-
dictable, uncontrollable events that require full alert readiness and mental anticipation.
In appropriate circumstances, temporary moderate increases in stress hormones (and
associated neurotransmitters such as dopamine) may enhance mental activity for short
periods in localized areas and prime memory storage, hence improving cognitive
processes for responding to social challenges (Beylin & Shors, 2003; Boyce & Ellis,
2005; Domes, Heinrichs, Reichwals, & Hautzinger, 2002; LeDoux, 2000, 2003; cf.
McEwen & Sapolsky, 1995; McGaugh, 2004). Mental processes unnecessary for ap-
propriate response may be inhibited, perhaps to reduce external and internal “noise”
(Servan-Schreiber, Printz, & Cohen, 1990; cf. Kirschbaum, Wolf, May, Wippich, &
Helhammer, 1996; Lupien et al., 2005).
Experimental studies that expose subjects to acute temporal stressors such as pub-
lic speaking or parachute jumping reliably elevate stress hormones (Dickerson & Ke-
meny, 2004). Relations between cortisol production and emotional distress in natural
settings, however, are difficult to assess because of temporal and interindividual vari-
ation in HPA response (Dabbs & Hopper, 1990; Ellis, Jackson, & Boyce, 2006; Kagan,
1992; Pollard, 1995; Nachmias, Gunnar, Mangelsdorf, Parritz, & Buss, 1996; Tennes
& Mason, 1982). Habituation may occur to repeated events for which a child or adult
acquires an effective mental model. Apparently “stressful” job environments may not
stimulate increased levels of stress hormones if individuals have adjusted to them. Ex-
pressions of behavioral distress (e.g., crying) among children are not reliably associ-
ated with elevated cortisol (Gunnar, 1992; cf. Ahnert, Gunnar, Lamb, & Barthel, 2004;
Flinn, 2006c), and some studies suggest that phobic individuals exhibit only moderate
rises in cortisol during clinical phobic episodes (Nesse, Curtis, Thyer, McCann,
Huber-Smith, & Knopf, 1985). Attenuation and below-normal levels of cortisol may
follow a day or more after emotionally charged events. Personality may affect HPA re-
sponse (and vice versa), because children with inhibited, anxious, or fearful tempera-
ments tend to have higher cortisol levels than extroverted children (Kagan, Resnick,
& Snidman, 1988; cf. Suomi, 1991; Hart, Gunnar, & Cicchetti, 1995; Higley &
Suomi, 1996; Nachmias et al., 1996).
Chronically stressed children may develop abnormal cortisol response, possibly
via changes in binding globulin levels, and/or reduced affinity or density of glucocor-
ticoid, CRH, oxytocin and vasopressin receptors in the brain (De Kloet, 1991; Fuchs
& Flugge, 1995). Early experience—such as perinatal stimulation of rats (Meaney,
Mitchell, Aitken, Bhat Agar, Bodnoff, Ivy, & Sarriev, 1991; Takahashi, 1992; Weaver
et al., 2004), some types of prenatal stress of rhesus macaques (Schneider, Coe, &
Lubach, 1992; Clarke 1993), maternal-infant attachment among humans (Spangler &
Grossmann, 1993), and sexual abuse among humans (De Bellis, Chrousos, Dorn,
Burke, Helmers, Kling, Trickett, & Putman, 1994; Heim et al., 2002)—may perma-
nently alter HPA response.
Further complications arise from interaction between HPA stress response and a
wide variety of other neuroendocrine and neuroimmune activities, including modula-
tion of catecholamines, melatonin, testosterone, serotonin, ß-endorphins, cytokines,
and enkephalins (de Kloet, 1991; Miller, Cohen, & Ritchey, 2002; Sapolsky, 1990b,
1992b). Changes in cortisol for energy allocation and modulation of immune function
may be confused with effects of psychosocial stress. Cortisol may be a co-factor prim-
ing dopamine, oxytocin, and vasopressin intracerebral binding sites that are associated
with the neuroplasticity of familial attachment in mammals (Carter, 2005; Fleming,
Steiner, & Corter, 1997), and hence may influence distress involving caretaker-child
relationships (see also Aragona, Liu, Yu, Curtis, Detwiler, Insel, & Wang, 2006;
Carter, 2003; Cushing & Kramer, 2005; Porges, 1998; Tennes, 1982; Wismer Fries,
Ziegler, Kurian, Jacoris, & Pollak, 2005). Synergistically, oxytocin has important ef-
fects on social cognition and fear (Heinrichs, Baumgartner, Kirschbaum, & Ehlert,
2003; Kirsch, Esslinger, Chen, Mier, Lis, Siddhanti, Gruppe, Mattay, Gallhofer, &
Meyer-Lindenberg, 2005). Other components of the HPA axis, such as corticotropin
releasing hormone (CRH) and melanocyte stimulating hormone, have additional
stress-related effects that are distinct from cortisol. Finally, a variety of hormones such
as estrogens and other endogenous chemicals—including “antiglucocorticoids”—
mediate specific actions of cortisol (e.g., Kaufer, Ogle, Pincus, Clark, Nicholas,
Dinkel, Dumas, Ferguson, Lee, Winters, & Sapolsky, 2004). Concurrent monitoring of
all these neuroendocrine activities would provide important information about stress
response, but is not possible in a non-clinical setting with current techniques.
Relations between stress-induced cortisol response and immunosuppression are
perhaps even more complex and enigmatic (Coe & Lubach, 2005; McEwen, 1998;
Sapolsky, 2005). Stress is associated with a variety of illness, including infectious dis-
ease, reactivation of latent herpes virus, cancer, and cardio-vascular problems. The
wide range of health effects of stress suggests that a number of immune mechanisms
are involved. Cortisol influences many functions of lymphocytes, macrophages, and
leukocytes, and as with energy use, may direct their movement to specific locations
and even modulate apoptosis (Costas et al., 1996). Cortisol also inhibits the produc-
tion of some cytokines (e.g., interleukin-1) and mediates several components of the in-
flammatory response. In concert with the sympathetic system, which generally down-
modulates lymphocyte and monocyte functions, HPA stress response affects all of the
major components of the immune system. However, the effects of neuroendocrine
stress response are not all inhibitory, and involve temporary up-regulation and/or lo-
calized enhancement of some immune functions (Dhabbar & McEwen, 2001; Jef-
feries, 1991; Coe & Lubach, 2005).
Stress response involves an optimal allocation problem (Sapolsky, 1990a, 1994). En-
ergy resources are diverted to muscular and immediate immune functions and other
short-term (stress emergency) functions, at cost to long-term functions of growth, devel-
opment, and building immunity. Under normal conditions of temporary stress, there
would be little effect on health. Indeed, there may be brief enhancement and directed traf-
ficking of immune (Dhabbar & McEwen, 2001) and cognitive function. Persistent stress
and associated hyper- or hypo-cortisolemia, however, is posited to result in pathological
immunosuppression, depletion of energy reserves, and damage to or inhibition of neuro-
genesis in parts of the hippocampus (e.g., Gould & Tanapat, 1999; Santarelli, Saxe,
Gross, Surget, Battaglia, Dulawa, Weistaub, Lee, Duman, Arancio, Belzung, & Hen,
2003; Sheline, Gado, & Kraemer, 2003). This perspective highlights the problems with
a stress response system that evolved to cope with short-term emergencies. The chronic
stress produced by modern human—or other primates with complex relationships—
social environments may present novel challenges that the system is not designed to han-
dle, hence potentially resulting in maladaptive pathology (Sapolsky, 1994, 2003).
This strict version of an environmental novelty hypothesis, however, is difficult to
reconcile with the long evolutionary histories of complex sociality in primates, and es-
pecially humans, accompanied by dramatic changes in the brain. Why, given all the
extensive modifications of the human brain over the past several million years, would
selection not have weeded out this apparent big mistake? Modern human environ-
ments have many novelties that elicit stress response, but social challenges in general
seem to have a much more ancient evolutionary depth, and may be a key selective
pressure for the large human brain. One possibility is that the demands of preparing
for potential dangers are an unavoidable costly insurance, akin to expensive febrile re-
sponse to pathogens that are usually benign—the “smoke-detector” principle (Nesse
& Young, 2000). The idea is that although physiological stress response to social chal-
lenges is costly, and most often wasteful, it may have helped our ancestors cope with
rare and unpredictable serious conflicts often enough to be maintained by selection.
The benefit/cost ratio could be improved by fine-tuning stress mechanisms in response
to environmental conditions during ontogeny.
A complementary approach suggests that neuroendocrine stress response may
guide adaptive neural reorganization, such as enhancing predator detection and avoid-
ance mechanisms (Buwalda, Kole, Veenema, Huininga, De Boer, Korte, & Koolhas,
2005; Dal Zatto, Marti, & Armario, 2003; LeDoux, 2000; Rodriguez Manzanares
et al., 2005; Meaney, 2001; Wiedenmayer, 2004). Exposure to cats that elevates glu-
cocorticoid levels can have long-term effects on the central amygdala (right side) in
mice, resulting in increased fear sensitization (Ademec et al., 2005; see also Knight,
Nguyen, & Bandettini, 2005). The potential evolutionary advantages of this neural
phenotypic plasticity are apparent (Rodriguez Manzanares et al., 2005). Prey benefit
from adjusting alertness to match the level of risk from predators in their environ-
ments. Post-Traumatic Stress Disorder (PTSD) appears analogous to these fear condi-
tioning models, and involves similar effects of noradrenergic (Pitman et al., 2002) and
glucocorticoid systems (Roozendaal, 2002; Roozendaal, Quirarte, & McGaugh, 2002)
on associative long-term potentiation of the amygdala. Social defeat also affects the
amygdala and hippocampus, but in different locations (Bartolomucci, Palanza, Sacer-
dote, Panerai, Sgoifo, Dantzar, Parmigiani, 2005; Buwalda, Felszhegy, Horvath,
Nyakas, de Boer, & Bohus, 2001; Koolhaas, de Boer, de Ruiter, Meerlo, & Sgoifo,
1997), suggesting that neural remodeling and LTP is targeted and domain-specific
(e.g., Pham, McEwen, Ledoux, & Nader, 2005; Rumpel, LeDoux, Zador, & Malinow,
2005). Glucocorticoids, perhaps in combination with peptide hormones and cate-
cholamines, appear to facilitate the targeting of domain-specific remodeling and long-
term potentiation (Huang & Herbert, 2006). The potentiating effects of cortisol on
emotional memories and other socially salient information may be of special sig-
nificance in humans (Fenker, Schott, Richardson-Klavehn, Heinze, & Düzel, 2005;
Jackson, Payne, Nadel, & Jacobs, 2006; Lupien et al., 2005; Pitman, 1989). The neu-
rological effects of stress response may underlie adaptation to both short-term contin-
gencies and guide long-term ontogenetic adjustments of behavioral strategies.
If physiological stress response promotes adaptive modification of neural circuits
in the limbic and higher associative centers that function to solve psychosocial prob-
lems (Huether et al., 1999), then the paradox of psychosocial stress would be partly
resolved. Temporary elevations of cortisol in response to social challenges could have
advantageous developmental effects involving synaptogenesis and neural reorganiza-
tion (Buchanan & Lovallo, 2001; Huether, 1996, 1998) if such changes are useful and
necessary for coping with the demands of an unpredictable and dynamic social envi-
ronment. Elevating stress hormones in response to social challenges makes evolution-
ary sense if it enhances specific acute mental functions and helps guide cortical re-
modeling of “developmental exuberance” (Flinn, 2006b; Innocenti & Price, 2005; Sur
& Rubenstein, 2005).
Chronic destabilization of neuronal networks in the hippocampus or cerebral cor-
tex, combined with enhanced fear circuits in the amygdala (e.g., Bauer, LeDoux, &
Nader, 2001; Phan, Fitzgerald, Nathan, & Tancer, 2006), however, could result in ap-
parently pathological conditions such as PTSD (Tupler & DeBellis, 2006; Yehuda,
2002) and some types of depression (Preussner, Baldwin, Dedovic, Renwick, Khalili
Mahani, Lord, Meaney, & Lupien, 2005). Even normal (but rather novel) everyday
stressors in modern societies, such as social discordance between what we desire and
what we have (Dressler & Bindon, 2000), might generate maladaptive HPA response.
Individual differences in perception, emotional control, rumination, reappraisal, self-
esteem, and social support networks seem likely co-factors (see also Ellis, Jackson, &
Boyce, 2006).
Testing these ideas about relations between physiological stress response, neural
remodeling, and adaptation to the social environment is not a simple or easy task (e.g.,
Pine, Fyer, Grun, Phelps, Szesko, & Koda, 2001). Cortisol can affect cognitive func-
tioning, and cognitive processing can affect cortisol response, all in an ongoing onto-
genetic dance. Teasing out the causes and effects in ontogenetic sequence requires
sequential data on physiological response profiles, environmental context, and
perception. Extensive research on hormonal stress response has been conducted in
clinical, experimental, school, and work settings (Dickerson & Kemeny, 2004; Gun-
nar, Tout, de Haan, Pierce, & Stansbury, 1997; Panter-Brick & Pollard, 1999; Stans-
bury & Gunnar, 1994; Weiner, 1992). We know relatively little, however, about stress
neuroendocrinology among children in normal everyday (“naturalistic”) environ-
ments, particularly in non-industrial societies (Panter-Brick, 1998). Investigation of
childhood stress and its effects on development has been hampered by the lack of non-
invasive techniques for measurement of stress hormones. Frequent collection of
plasma samples in non-clinical settings is not feasible. The development of saliva im-
munoassay techniques, however, presents new opportunities for research on stress re-
sponse to everyday life. Saliva is relatively easy to collect and store, especially under
adverse field conditions faced by anthropologists and psychologists working in natu-
ralistic research settings (Ellison, 1988). Longitudinal monitoring of a child’s daily ac-
tivities, stress hormones, and psychological conditions provides a powerful research
design for investigating naturally occurring stressors. Analyzing hormone levels from
saliva can be a useful tool for examining the child’s imperfect world and its devel-
opmental consequences, especially when accompanied by detailed ethnographic,
medical, and psychological information. Unfortunately, we do not yet have field tech-
niques for assessment of corresponding ontogenetic changes in the relevant neurolog-
ical mechanisms.
Social Worlds and the Ontogeny

of Stress Response: The Dominica Study
Assessment of relations among psychosocial stressors, hormonal stress response,
family environment, and health during child development is complex, requiring
(a) longitudinal monitoring of social environment, emotional states, hormone levels,
immune measures, and health, (b) control of extraneous effects from physical activity,
circadian rhythms, and food consumption, (c) knowledge of individual differences
in temperament, experience, and perception, and (d) awareness of specific social
and cultural contexts. Multi-disciplinary research that integrates human biology, psy-
chology, and ethnography is particularly well suited to these demands (Bogin, 1999;
Panter-Brick, 1998). Physiological and medical assessment in concert with ethnogra-
phy and coresidence with children and their families in anthropological study popula-
tions can provide intimate, prospective, longitudinal, naturalistic information that is
not feasible to collect in clinical studies. For the past eighteen years (1988–present)
we have conducted such research with the help of many colleagues and students and
the extraordinary cooperation of a wonderful study population.
The Study Village
“Bwa Mawego” is a rural community located on the east coast of Dominica. About
500 residents live in 160 structures/households that are loosely clumped into five
“hamlets” or neighborhoods. The population is of mixed African, Carib, and European
descent. The community is isolated because it sits at the dead-end of a rough road.
Part-time residence is common, with many individuals emigrating for temporary work
to other parts of Dominica, other Caribbean islands, the United States, the United
Kingdom, or Canada. Most residents cultivate bananas and/or bay leaves as cash
crops, and plantains, dasheen, and a variety of fruits and vegetables as subsistence
crops. Fish are caught by free-diving with spear-guns and from small boats (hand-built
wooden “canoes” of Carib design) using lines and nets. Land is communally “owned”
by kin groups, but parceled for long-term individual use.
Most village houses are strung close together along roads and tracks. Older homes
are constructed of wooden planks and shingles hewn by hand from local forest trees;
concrete block and galvanized roofing are more popular today. Most houses have one
or two sleeping rooms, with the kitchen and toilet as outbuildings. Children usually
sleep together on foam or rag mats. Wealthier households typically have “parlors” with
sitting furniture. Electricity became available in 1988; during the summer of 1995 about
70% of homes had “current,” 41% had telephones, 11% had refrigerators, and 7% had
televisions. Water is obtained from streams, spring catchments, and run-off from roofs;
public piped water became available in June 1999, but few households are connected.
The community of Bwa Mawego is appropriate for the study of relations between
a child’s social environment and physiological stress response for the following rea-
sons: (1) there is substantial variability among individuals in the factors under study
(i.e., family environments, social challenges, and stress response), (2) the village and
housing are relatively open, hence behavior is easily observable, (3) kin tend to reside
locally, (4) the number of economic variables is reduced relative to urban areas, (5)
the language and culture are familiar to the investigator, (6) there are useful medical
records, and (7) local residents welcome the research and are most helpful.
The study involved 282 children and their caregivers residing in 84 households.
This is a nearly complete sample (> 98%) of all children living in four of the five vil-
lage hamlets during the period of fieldwork.
Methods and Field Techniques

“. . . we finished getting the spit today! . . . maybe we should collect a couple more [dupli-
cate] samples tomorrow from a few of the kids . . . just to make sure the lab measures are
reliable . . . and to double-check that cortisol levels do not change much from day to day.”
(MVF field notes, July 18, 1989)
Our initial objective, back in 1989, was to assess what each child’s general stress
level was, as determined by a single measure of the level of cortisol in their saliva. The
idea was to see how this hormone was associated with a child’s family environment.
We assumed, rather naively, but in good academic company, that salivary cortisol
levels were a fairly stable “trait” character. What seemed like an unnecessarily cau-
tious decision at the time to collect and assay additional saliva samples from several
of the children resulted in a rather more complex study. We were quite surprised when
the results of the additional sample assays indicated that a child’s cortisol levels var-
ied substantially from one day to the next. Serendipity provided samples from two sib-
lings in good spirits one day, but sad and upset by a family quarrel the next, in con-
cert with field notes detailing the events. This temporal link between cortisol levels
and psychosocial states suggested a dramatic revision of research design. We also
were fortunate to have saliva samples from different times of day in this initial collec-
tion, and quickly recognized that very precise control of circadian patterns—in partic-
ular sleep schedules and wake-up times—was critical to accurate assessment of HPA
stress response (Flinn & England, 1992). More than 30,000 saliva samples later, it
seems we have more questions than answers.
In this study, sequential longitudinal monitoring is used to assess physiological
stress response to everyday events, including social challenges. Saliva is collected
from children by members of the research team at least twice a day, wherever the chil-
dren happen to be (usually at their household). This direct collection and observation
procedure avoids errors that can occur with at-home self- or parent-collection and re-
port protocols. The large sample size of cortisol measures for each child (>100 sam-
ples for most children) in a variety of naturalistic contexts provides a more extensive
and complex picture of HPA stress response than small sample designs.
Data analyses examine both long term (ten+ years) and short term (day-to-day,
hour-by-hour) associations among cortisol levels, family composition, socioeconomic
conditions, behavioral activities, events, temperament, growth, medical history, im-
mune measures, and illness. Physiological stress response is assessed by radioim-
munoassay (RIA) of cortisol levels in saliva. Analyses include mean values, varia-
tion, and day-to-day and hour-by-hour profiles of standardized (circadian control by
5-minute intervals from wake-up time) cortisol data (Flinn & England, 2003; Flinn &
Quinlan, in prep.). Family composition is assessed by age, sex, genealogical relation-
ship, and number of individuals in the caretaking household. Socioeconomic condi-
tions include household income, material possessions, land ownership, occupations,
and educational attainment. Caretaking is assessed by (a) frequencies and types of
behavioral interaction, (b) informant ratings of caretaking that children received, and
(c) informant interviews. Here we use a dichotomous (above median, below median)
composite measure of caretaking by grandparents (“GPC”). Immune response is as-
sessed by turbidimetric immunoassay of secretory-immunoglobulin A from saliva;
however, relatively few samples have been assayed (N = 212), and interpretation is
uncertain so inferences are preliminary. Health is assessed by (a) observed type, fre-
quency, and severity of medical problems (diarrhea, influenza, common cold, asthma,
abrasions, rashes, etc.), (b) informant (parents, teachers, neighbors) ratings, (c) med-
ical records, (d) growth (standard anthropometric measures, including height, weight,
and skinfolds) and fluctuating asymmetry patterns (Flinn, Leone, & Quinlan, 1999;
Leone, 2005) and (e) physical examination by a medical doctor. The primary measure
of health used is percentage of days ill, the proportion of days that a child was ob-
served (directly by researchers) with common benign temporary infectious disease
(89% were common-cold upper respiratory tract infections with nasal discharge,
cough, or myalgia—e.g., rhinovirus, adenovirus, parainfluenza, and influenza; 6%
were diarrheal; 5% were miscellaneous indeterminate—e.g., febrile without other
symptoms). Daily activities and emotional states are assessed from (a) caretaker and
child self-report questionnaires, and (b) systematic behavioral observation (focal fol-
low and instantaneous scan sampling). Multiple sources of information are cross-
checked to assess reliability (Bernard, Killwoth, Kronenfield, & Sailer, 1984).
In the following section we briefly review some of the results from this study that
may provide useful insights into the ontogeny of stress response to psychosocial chal-
lenges. We then turn to examining the effects that grandparents have in guiding this
aspect of child development.
Cortisol Response to Naturally Occurring Social Challenges

Our analyses of naturally occurring stressors in children’s lives in Bwa Mawego
indicate that social challenges are important stressors, with the emphasis upon the
family environment as both a primary source and mediator of stressful stimuli (Flinn
& England, 1995, 2003; Flinn, Turner, Quinlan, Decker, & England, 1996; Turner,
Flinn, & England, 1995). Temporary moderate increases in cortisol are associated with
common activities such as eating meals, active play (e.g., cricket), and hard work
(e.g., carrying loads of wood to bay oil stills) among healthy children. These moder-
ate stressors—“arousers” might be a more appropriate term—usually have rapid atten-
uation, with cortisol levels diminished to normal within an hour or two (some stres-
sors have characteristic temporal “signatures” of cortisol level and duration—see
Figure 5 for an example).
High-stress events (cortisol increases from 100% to 2000%), however, most com-
monly involved trauma from family conflict or change (Flinn & England, 2003). Pun-
ishment, quarreling, and residence change substantially increased cortisol levels,
whereas calm, affectionate contact is associated with diminished (–10% to –50%) cor-
tisol levels. Of all cortisol values that are more than two standard deviations above
mean levels (i.e., indicative of substantial stress), 19.2% are temporally associated
with traumatic family events (residence change of child or parent/caretaker, punish-
ment, “shame,” serious quarreling, and/or fighting) within a 24-hour period—for com-
parison, 12% are associated with minor family conflicts, 9.2% with peer conflicts or
school problems, 7.9% with illness, and 6.4% with physical exertion, the next highest
categories; 43.4% have no recorded abnormal event. In addition, 42.1% of traumatic
family events are temporally associated with substantially elevated cortisol (i.e.,
at least one of the saliva samples collected within 24 hours is > 2 SD above mean
levels)—other consistent predictors of elevated cortisol include illness with fever and
high profile competitive sports events. Chronic elevations of cortisol levels, as in the
example of the Franklin family (Figure 2), may also occur, but are more difficult to
assess quantitatively.
There is considerable variability among children in cortisol response to family dis-
turbances. Not all individuals have detectable changes in cortisol levels associated
3 family family
conflict returns
2
Cortisol (standardized)
–1
June 24 25 26 27 28 29 July 19 20 21 22
FIGURE 2. On June 28, 1992, a serious marital conflict erupted in the

“Franklin” household. “Amanda” was a 34-year-old mother of six children,
five of whom (ages 2, 3, 5, 8, and 14) were living with her and their father/
stepfather, “Pierre Franklin.” Amanda was angry with Pierre for spending
money on rum. Pierre was vexed with Amanda for “shaming” him in front of
his friends. He left the village for several weeks, staying with a relative in
town. His three genetic children (ages 2, 3, and 5) showed abnormal cortisol
levels (in this case, elevated) for a prolonged period following their father’s
departure. This pattern is typical: children usually became habituated to stress-
ful events, but absence of a parent often resulted in abnormal patterns of ele-
vated and/or subnormal cortisol levels. Following the return of their father, the
Franklin children’s cortisol levels resumed a more normal profile. Again, this
pattern is typical: children living in families with high levels of marital con-
flict (observed and reported serious quarreling, fighting, residence absence)
were more likely to have abnormal cortisol profiles than children living in
more amiable families were. Figure adapted from Flinn & England, 1997.
with family trauma. Some children had significantly elevated cortisol levels during
some episodes of family trauma but not during others. Cortisol response is not a sim-
ple or uniform phenomenon. Numerous factors, including preceding events, habitua-
tion, specific individual histories, context, and temperament, might affect how chil-
dren respond to particular situations.
Nonetheless, traumatic family events and social emotions such as guilt and shame
(Flinn, 2006c) were associated with elevated cortisol levels for all ages of children
more than any other factor that we examined. These results suggest that family inter-
actions were a critical psychosocial stressor in most children’s lives, although the sam-
ple collection during periods of relatively intense family interaction (early morning
and late afternoon) may have exaggerated this association.
Cortisol (standardized) 1
.5
–.5
Nuclear Nuclear Single Single Grand Grand Step Step Distant
father mother mother mother parents father father, relatives
abs > 50% + kin half-sibs
Household composition
FIGURE 3. Household composition and average cortisol levels of children. Vertical

lines represent 95% confidence intervals (1.97 × SE). Figure adapted from Flinn, 1999.
Children residing in bi-parental, single mother with kin, and grandparental house-
holds have moderate cortisol levels (Figure 3), with a higher proportion of elevations
occurring in the context of positive affect situations such as competitive play, physi-
cal work, and excitement regarding novel situations.
Although elevated cortisol levels are associated with traumatic events such as fam-
ily conflict, long-term stress may result in diminished cortisol response. In some
cases, chronically stressed children had blunted response to physical activities that
normally evoked cortisol elevation. Comparison of cortisol levels during “nonstress-
ful” periods (no reported or observed crying, punishment, anxiety, residence change,
family conflict, or health problem during the 24-hour period before saliva collection)
indicates a striking reduction and, in many cases, reversal of the family environment-
stress association (Flinn & England, 2003). Chronically stressed children sometimes
had subnormal cortisol levels when they were not in stressful situations. For example,
cortisol levels immediately after school (walking home from school) and during non-
competitive play were lower among some chronically stressed children (cf. Long,
Ungpakorn, & Harrison, 1993). Some chronically stressed children appeared socially
“tough” or withdrawn and exhibited little or no arousal to the novelty of the first few
days of the saliva collection procedure. These subnormal profiles may be similar in
some respects to those of individuals with Post-Traumatic Stress Disorder (e.g.,
Yehuda, Engel, Brand, Seckl, Marcus, & Berkowitz, 2005).
Although elevated cortisol levels in children are usually associated with negative
affect, events that involve excitement and positive affect can also stimulate stress re-
sponse (Flinn, 2006c). For example, cortisol levels on the day before Christmas were
more than one standard deviation above normal, with some of the children from two-
parent households and those having the most positive expectations exhibiting the
highest cortisol (Flinn, 2006e). Cortisol response appears sensitive to social chal-
lenges with different affective states. Other studies further suggest that the cognitive
effects of cortisol may vary with affective states, such as perceived social support (Ah-
nert et al., 2004; Quas, Bauer, & Boyce, 2004).
There are some age and sex differences in cortisol profiles, but it is difficult to as-
sess the extent to which this is a consequence of neurological differences (e.g., Butler,
Pan, Epstein, Protopopescu, Tuescher, Goldstein, Cloitre, Yang, Phelps, Gorman, Le-
Doux, Stern & Silbersweig, 2005), physical maturation processes, or the different social
environments experienced, for example, during adolescence as compared with early
childhood (Flinn, Turner, Quinlan, Decker, & England, 1996; Flinn & Quinlan, in prepa-
ration). For instance, young adult women have a higher incidence of depression and as-
sociated abnormal cortisol profiles than children or young men in this community.
The emerging picture of HPA stress response in naturalistic context from the Do-
minica study is one of sensitivity to social challenges, consistent with clinical and ex-
perimental studies. The results further suggest that family environments are an espe-
cially important source and mediator of stressful social challenges for children. In the
next section, data on the longitudinal effects of early traumatic experiences are exam-
ined to assess the domain-specificity of changes in stress response.
Ontogeny: The Early Trauma → HPA Dysfunction Hypothesis

“. . . the development of individual differences in behavioral and neuroendocrine responses
to stress can be influenced by events occurring at multiple stages in development . . .” (Fran-
cis, Diorio, Plotsky, & Meaney, 2002)
Early experiences can have profound and permanent effects on stress response.
Exposure to prenatal maternal stress, or prolonged separation from mother in rodents
and non-human primates, can result in lifelong changes in HPA stress response (Mac-
cari et al., 2003; Meaney 2001; Suomi, 1997; cf. Levine, 2005). Research on the de-
velopmental pathways has targeted the homeostatic mechanisms of the HPA system,
which appear sensitive to exposure to high levels of glucocorticoids during ontogeny.
Glucocorticoid receptors (GRs) in the hippocampus that are part of the negative feed-
back loop regulating release of CRH and ACTH can be damaged by the neurotoxic
levels of cortisol associated with traumatic events (Sapolsky, 1990b, 2005). Hence
early trauma is posited to result in permanent HPA dysregulation and hypercorti-
solemia, with consequent deleterious effects on the hippocampus, thymus, and other
key neural, metabolic, and immune system components (Mirescu et al., 2004; Zhang,
Parent, Weaver, & Meaney, 2004). These effects have additional consequences result-
ing from high density of GRs in the pre-frontal cortex in primates (DeKloet, Oitzl, &
Joels, 1999; Patel, Lopez, Lyons, Burke, Wallace, & Schatzberg, 2000; Sanchez,
Young, Plotsky, & Insel, 2000).
Finer-grained analysis of the epigenetic mechanisms involved with maternal ef-
fects on glucocorticoid negative feedback on CRH release indicates that DNA methy-
lation affects hippocampal GR exon 17 promoter activity (Weaver et al., 2004). The
Cortisol (standardized) 1.0
18
24
9
0
57
No EFT in utero 0–3 3–6
Age of first major trauma
FIGURE 4. Children exposed to early family trauma in utero or post-natal have higher
average (means for each child) cortisol levels at ages ten and above than children who
were not exposed to early trauma (no EFT). Sample sizes (# of children) are in bars.
Vertical lines represent 95% confidence intervals. Figure adapted from Flinn, 2006b.
permanence of DNA methylation, set during a sensitive period in the first week after
birth in the rat, is a mechanism connecting diminished maternal care (e.g., licking,
grooming, and arched-back nursing) with long-term elevations of HPA stress response.
The specific mechanisms affecting relations between exposure to trauma early in
development and subsequent HPA system function in humans are not as well docu-
mented as in animal studies. Nonetheless, a similar causal linkage appears plausible
(e.g., Essex, Klein, Cho, & Kalin, 2002; Heim et al., 2000; Lupien et al., 2005;
O’Conner, Heron, Golding, Glover, & ALSPAC study team, 2003; Teicher, Andersen,
Polcari, Anderson, Navalta, & Kim, 2003). Children in the Bwa Mawego study who
were exposed to the stress of hurricanes and political upheavals during infancy or in
utero do not have any apparent differences in cortisol profiles in comparison with chil-
dren who were not exposed to such stressors. Children exposed to the stress of
parental divorce, death, or abuse (hereafter “early family trauma” or EFT), however,
have significantly higher cortisol (Figure 4) levels at age ten than other children. EFT
children also have higher morbidity than non-EFT children (Flinn, 2006b). Based on
analogy with the non-human research discussed previously, two key factors could be
involved: (1) diminished hippocampal GR receptor functioning, resulting in less ef-
fective negative feedback regulation of cortisol levels; and (2) enhanced sensitivity to
perceived social threats, perhaps as a consequence of lower social competencies. Chil-
dren usually elevate cortisol in response to strenuous physical activity, but rapidly re-
turn to normal levels (Figure 5). If EFT has affected the negative feedback loop, then
recovery to normal cortisol levels would be slower. Resumption of normal cortisol
levels after physical stressors, however, appears similar regardless of early experience
of family trauma (Flinn, 2006b). Cortisol profiles following social stressors, however,
.75
Cortisol (µg/dl)
.50
.25
0
7:00 AM 12:00 PM 5:00 PM
FIGURE 5. Ten-hour cortisol profile of a 12-year-

old boy. Note elevation of cortisol levels at 10:00–
10:30 AM when he was helping his father carry
wood.
indicate that EFT children sustain elevated cortisol levels longer than non-EFT chil-
dren (Flinn, 2006b).
The enhanced HPA stress response of children in this community that were ex-
posed to EFT appears primarily focused on social challenges, suggesting that the on-
togenetic effects of early trauma on stress response may be domain-specific and even
context-specific. These results are consistent with studies of the effects of social de-
feat with non-human models (e.g., Kaiser & Sachser, 2005). In the following section
we examine the effects of close grandparental relationships on the stress response of
EFT children.
Ameliorative Effects of Grandparental Care

on the Ontogeny of Stress Response
Review of analyses of data in the previous section indicate that early family trauma
is associated with higher cortisol levels among children in this community. The differ-
ent cortisol response patterns to social and physical stressors suggest that domain-
specific mechanisms have been affected. In this section we examine whether close re-
lationships with grandparents during early childhood are associated with individual
differences among EFT children in several outcome measures. The general hypothesis
is that grandparental care (GPC) reduces psychosocial stress for grandchildren. The
negative effects of early family trauma on child development are therefore expected to
be moderated by GPC, as measured by cortisol levels, growth, and morbidity.
EFT children with high (above median) levels of GPC have lower average cortisol
levels (Figure 6a), lower morbidity (Figure 6b), and higher growth percentiles (Figure
6c), than EFT children with low GPC. EFT children that have high rates of grand-
parental care (GPC), however, do not have lower average fluctuating asymmetry (FA)
1.0
Cortisol (standardized)
Controls EFT children EFT children

(N = 57) w/high GPC w/low GPC
(N = 28) (N = 23)
FIGURE 6a. EFT children with high grandparental care (GPC) have lower average
cortisol levels than low GPC EFT children. Vertical lines represent 95% confidence
intervals.
10
% days ill, (standardized)
1.0
0
(N = 28) (N = 23)
FIGURE 6b. EFT children with high grandparental care (GPC) have lower average
morbidity levels than low GPC EFT children. Vertical lines represent 95% confidence
intervals.
(Figure 6d) or lower gastrointestinal parasite loads (Figure 6e) than EFT children with
low GPC. These results suggest that grandparental care may substantially ameliorate
some of the negative consequences of difficult family environments. These findings
are generally consistent with our subjective impressions from watching these children
over nearly two decades: that grandparental relationships are often of great importance
50
Growth percentile
40

(N = 28) (N = 23)
FIGURE 6c. EFT children with high grandparental care (GPC) have higher average
growth percentiles than low GPC EFT children. Vertical lines represent 95% confi-
dence intervals.
Fluctuating asymmetry (%)
2.5
2.0

(N = 28) (N = 23)
FIGURE 6d. EFT children with high grandparental care (GPC) do not have lower lev-
els of fluctuating asymmetry (FA) than low GPC EFT children. Vertical lines repre-
sent 95% confidence intervals.
for the development of emotional regulation, social skills, and self-confidence, espe-
cially for children in difficult family environments. What the specific mechanisms are,
and whether the effects are direct or indirect via support to the child’s mother, are not
discernable from these analyses.
40
Parasite loads (%)
20

(N = 28) (N = 23)
FIGURE 6e. EFT children with high grandparental care (GPC) do not have lower lev-
els of parasite loads than low GPC EFT children.
Conclusions
Grandparental care appears to be a significant mediator of HPA stress response and
associated growth and health problems among children that have experienced early
family trauma. Our observations suggest that maternal grandmothers are especially
important mediators, (Quinlan & Flinn, 2005), although a variety of other kin (e.g.,
aunts, siblings, grandfathers) may also contribute, and in special cases, may be pri-
mary caregivers (Flinn & Leone, 2006). These results are likely to be specific to the
context of the kin networks of this community (e.g., see Quinlan & Flinn, 2003), and
are likely to vary contingent on the specific patterns of kinship, although grandparent-
grandchild relationships appear to be broadly important (Lahdenpera et al., 2004; Sear
et al., 2000; Voland & Biese, 2002). These results are consistent with the hypotheses
that the importance of grandmothers in human evolution may involve their role as
providers of social information (e.g., emotional comfort, social competencies, tradi-
tions) (Coe, 2003) in addition to providing calories and protection (Alexander, 1974;
Hawkes, O’Connell, Blurton Jones, Alvarez, & Charnov, 1998).
Returning to the paradox of why natural selection favored sensitivity of stress re-
sponse to social stimuli in the human child, several points emerge. Human childhood
is a life history stage that appears necessary and useful for acquiring the information
and practice to build and refine the mental algorithms critical for negotiating the so-
cial coalitions that are key to success in our species. Mastering the social environment
presents special challenges for the human child. Social competence is difficult because
the target is constantly changing and similarly equipped with theory of mind and other
cognitive abilities. Results from the Dominica study indicate that family environment,
including care from grandparents, is a primary source and mediator of stressful events
in a child’s world. The sensitivity of stress physiology to the social environment may
facilitate adaptive responses to this most salient and dynamic puzzle, aided by infor-
mation and security provided by effective parental and grandparental care.
Children lacking such care may be at a disadvantage in developing the social com-
petencies necessary for coping with social challenges, and consequently may be at in-
creased risk for problems ranging from dysregulation of emotional control and in-
creased risk of psychopathology (Gilbert, 2001; Nesse, 1999), to broader health issues
associated with social and economic disparities (Adler, Boyce, Chesney, Cohen, Folk-
man, Kahn, & Syme, 1994; Dressler et al., 2005; Marmot & Wilkerson, 1999). The
potential for intergenerational cycles that perpetuate social relationships that affect
stress (Belsky, 2005; Belsky, Jaffee, Sligo, Woodward, & Silva, 2005; Fleming, Krae-
mer, Gonzalez, Lovic, Rees, & Melo, 2002; Fleming, O’Day, & Kraemer, 1999; Fran-
cis, Diorio, Liu, & Meaney, 1999; Maestripieri, Lindell, Ayala, Gold, & Higley, 2005)
and poor health are especially concerning. Under such circumstances, grandparents
helping their grandchildren cope with difficult events involving their parents, inter-
vening during times of critical need and stabilizing development, may be of critical
importance (e.g., Lussier, Deater-Deckard, Dunn, & Davies, 2002).
We are still far from identifying the specific mechanisms linking stress response to
the ontogenetic plasticity of components of the limbic system and pre-frontal cortex
that are involved with the acquisition of social competencies. An evolutionary devel-
opmental perspective can be useful in these efforts to understand this critical aspect of
a child’s world by integrating knowledge of physiological causes with the logic of
adaptive design by natural selection (Worthman, 1999). It reminds us that our biology
has been profoundly affected by our evolutionary history as fundamentally social
creatures, including, perhaps, a special reliance upon grandparents. Indeed, the mind
of the human child may have design features that enable its development as a group
project, guided by the multitudinous informational contributions of its ancestors and
co-descendants. Children without grandparental input may find themselves in worlds
that are more stressful because they lack the advice, traditions, good humor, soft laps,
and hugging arms by which to understand them.
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The Development of Spontaneous Gestures
in Zoo-living Gorillas and Sign-taught Gorillas:
From Action and Location to Object Representation
Joanne E. Tanner
Scottish Primate Research Group, and Collaborator,
Centre for Social Learning & Cognitive Evolution, School of Psychology
University of St. Andrews, Scotland
Francine G. Patterson
The Gorilla Foundation/Koko.org
Woodside, California
Richard W. Byrne
Centre for Social Learning & Cognitive Evolution,
Scottish Primate Research Group, School of Psychology
University of St. Andrews, Scotland
rwb@st-andrews.ac.uk
Abstract: We analyze the developmental sequence in which different types of representa-

tion appear in untaught signs in the repertoire of Koko, a signing gorilla, and in the ges-
tures developed by zoo-living gorillas at different ages. There is a progression in all the
subjects from pure action to iconic representation of action. The signing gorilla, in addi-
tion, depicts objects. This is done through hand shape, miming of an action related to the
use of an object, or by tracing the outline of an object. The various spatial mediums (i.e.,
on the body versus in open space) in which signs are performed assist in understanding of
the cognitive processes supporting ape representation and communication. The progres-
sion from ape “action mapping” to the level of representation found in human language
is viewed as a series of stages that follow logically upon each other in a continuum of de-
velopment, both in individuals and in possibly in the history of the hominoid family.
Introduction
Research in recent decades has shown that zoo-living apes create gestures other than
the obviously species-typical, and signing apes regularly employ signs that they have
themselves created, in addition to taught signs. We explore the relationship of sponta-
neous gestures by zoo-living gorillas to those created by a sign language-taught gorilla.1
1. In this paper we will use the word “sign” for human sign language taught to apes, and also for gestural in-
ventions by signing apes. “Gesture” refers to inventions by zoo gorillas.
69
70 JOANNE E. TANNER, FRANCINE G. PATTERSON AND RICHARD W. BYRNE
Particular attention is given to the development of iconic gestures because they re-
quire a type of understanding that can be linked to human representational abilities.
Here we define an iconic sign or gesture simply as one that depicts a physical aspect
of its referent. Zoo-living gorillas use iconic gestures for actions anticipated or desired
(Tanner & Byrne, 1996, 1999); in both species of chimpanzee as well, iconic gestures
have been observed both in untaught captives (Kohler, 1925; Yerkes, 1943; Hayes,
1951; Savage-Rumbaugh, Wilkerson, & Bakeman, 1977) and chimpanzees trained in
symbol systems other than sign language2 (Savage-Rumbaugh, 1986; Greenfield &
Savage-Rumbaugh, 1990, Savage-Rumbaugh & Lewin, 1994). Signing apes also cre-
ate novel iconic signs; unlike zoo captives, they spontaneously create signs to repre-
sent objects for which they have not been taught signs, and use such invented, un-
taught signs repeatedly and consistently (Gardner & Gardner, 1971; Patterson, 1980;
Patterson & Cohn, 1990; Miles, 1978, 1993; Miles, Mitchell, & Harper, 1996). The
usage of iconicity can be traced in the chronological development of gestures in indi-
vidual gorillas, and the forms the iconicity takes and what it represents are important
keys to understanding ape cognition.
We survey signs Patterson and Cohn (1990) list as invented by Koko during her first
ten years of sign language instruction, with particular attention to those that appear to
be iconic, and we note the types of iconicity that Koko uses and make comparisons with
zoo gorillas’ gestures. We assess modes of representation in terms of their order of ap-
pearance in Koko’s individual development, and compare the developmental progres-
sion and age of appearance of similar gestures in zoo gorillas. We consider the spatial
media in which gestures and signs are produced. We compare the usage of those ges-
tures or signs that take the same form in both zoo gorillas’ and Koko’s usage to learn
whether their “meanings” or functions are universal or variable. Though the gestures of
gorillas have not been extensively studied by other researchers until very recently,
where possible we incorporate any relevant data from other gorillas in zoos or the wild.
Subjects
Only two gorillas have been extensively taught a human sign language: Koko (a
zoo-born female lowland gorilla) and Michael (a wild-born male lowland gorilla, now
deceased). Koko resides at the Gorilla Foundation in Woodside, California. Koko was
born at the San Francisco Zoo on July 4th, 1971, and is the full sister of Kubie, a prin-
cipal subject of the first author’s zoo observations. Koko’s exposure to American Sign
Language (ASL) and constant interaction with human companions began at the age of
one year under the tutelage of the second author, Francine Patterson, who was at the
time a graduate student at Stanford University. Koko was simultaneously exposed to
a variant of American Sign Language and human (English) speech. Further detail of
the education of gorillas Koko and Michael and the entire ongoing project can be
found in Patterson (1978, 1979, 1980), Patterson & Linden (1981), Patterson & Cohn
(1990), Patterson & Gordon (1993, 2002), and Bonvillian & Patterson (1993, 1999).
2. Because the researchers working with these apes do not describe their gestures in physical detail, they can-
not be compared with those of signing apes or apes not taught a symbol system.
The Development of Spontaneous Gestures in Zoo-living Gorillas and Sign-taught Gorillas 71
Information regarding the gestures of zoo-living gorillas is drawn primarily from
Tanner & Byrne’s long-term study of the gorilla group at the San Francisco Zoo (Tan-
ner 1998, 2004; Tanner & Byrne 1993, 1996, 1999). See www.gorillagestures.info for
video examples of the San Francisco Zoo gorillas’ gestures and more about the re-
search on the gorilla group there. From 1988 until 1997 observations were made out-
doors at the San Francisco Zoo one morning each week for approximately three hours,
conditions permitting. Further observations, on a less regular basis, have continued
until this writing. The study team consisted of the first author and the camera opera-
tor, Charles L. Ernest. The general procedure was to videotape all social interaction
continuously wherever it was possible to use the video camera. Later, videotape was
analyzed and gestures were cataloged into a Filemaker™ database. As a working def-
inition, the term “gesture” applied to all discrete, non-locomotor limb and head move-
ments that appeared to be potentially communicative, regardless of receptive sensory
modality.
The subjects, the gorillas at the San Francisco Zoo, are members of a stable social
group; all of them have spent nearly all of their lives at this zoo. The San Francisco
Zoo’s present gorilla enclosure has been this group’s home since 1980. It has an out-
doors area of 2300 square meters, or 38 by 50 meters at maximum parameters. It is
covered with grass and other vegetation and contains large, climbable live trees as
well as several dead trees, large stumps, and two artificial rock hills including arches
and cave-like areas.
The group at the time of the beginning of the study included first- and second-
generation descendants of the wild-caught founder, Bwana, who had been at the zoo
since 1958. A wild-caught female, Pogo, human-reared in her early years, grew up at
the zoo with Bwana and is of about the same age. Two young females whose early
rearing was by humans in zoo nurseries, Bawang and Zura, joined the group in 1981
and 1982 respectively, after the deaths of two older females. Bawang is the mother of
Kubie’s offspring, Shango, Barney, and Nneka, who have all been mother-reared.
Bawang was always Kubie’s preferred mate, but when she was pregnant or involved
in caring for her first infant, Kubie switched his attentions and play activity to the
younger female, Zura. All of these gorillas have been subjects of the Tanner and Byrne
studies, but the interaction between Kubie and Zura received the most intense analy-
sis; by far the greatest amount of gesturing was done by these two gorillas.
Untaught Signs by Koko and Michael

Most of Koko’s and Michael’s earliest taught sign language vocabulary that reached
formal criteria3 of consistent usage was composed of iconic signs, in contrast to the
vocabulary of deaf children. As the gorillas’ vocabularies increased, the proportion of
3. Two sets of criteria were used: the Emitted criterion accepted as a vocabulary item each use of a recogniza-
ble sign used spontaneously in an appropriate context; the Patterson criterion accepted a sign only if it was observed
and recorded by two different observers to be used appropriately and spontaneously on at least half the days during
a period of a month. By the end of ten years, Koko had acquired 876 words by the Emitted criterion, 290 words by
the Patterson criterion. The spontaneously invented signs discussed in this paper all met the Emitted criterion.
iconic signs decreased, though it remained higher than that of the human children stud-
ied by Bonvillian and Patterson (1993). Bonvillian and Patterson, however, acknowl-
edge that the design of their study does not allow us to discern the influences from hu-
mans on the content of taught sign vocabulary. Also some taught iconic signs may
represent aspects of the referent that would not be recognized by the learner as iconic.
Here we will look only at signs that were created by the gorillas that were not part of
their taught American Sign Language vocabulary.
In summarizing the first ten years of Koko’s vocabulary development, Patterson
and Cohn (1990) list Koko’s entire vocabulary during these ten years and indicate
which of those signs were not taught, but used spontaneously by the gorilla. These
spontaneous creations were not a result of deliberate human reinforcement of chance
novelty; untaught signs were often not initially comprehended by Koko’s human com-
panions and were ignored or misunderstood until repeated context made the meaning
clear. Thus Koko’s untaught signs can be expected to be free from human influence in
choice of referents. In some cases, the inventions were for actions, objects, or concepts
for which Koko had not been taught a sign; others were for actions, objects, or con-
cepts for which she had been taught a sign but for which she strongly seemed to pre-
fer her own usage. Once acknowledged by humans as part of her vocabulary, untaught
signs were neither discouraged nor encouraged, but simply accepted as part of Koko’s
repertoire of signs. (It is, of course, possible that humans have failed to understand and
interpret some of Koko’s signs. Also, because iconic signs are easier for us to attempt
to translate, they might be over-represented in summarizing Koko’s vocabulary.)
We categorize, according to type of iconicity or other form of reference, fifty signs
that Patterson and Cohn (1990) characterized as “invented” by Koko. This was done
with the help of an unpublished, internal-use video created by Dr. Francine (Penny)
Patterson and Darlene Chan for Gorilla Foundation employees, unpublished lists of
Koko’s sign lexicon, published physical description of earliest signs (Patterson, 1978),
as well as the first and second authors’ personal experience and knowledge of Koko’s
signing. Not included are those listed as “natural” (Patterson & Cohn’s term for signs
or gestures they suspected to be species-typical) or “modulated or compounded”
(modulated means modifying the taught articulation of a sign; compounded means
combining aspects of taught signs to form a new sign). The total corpus of 50 signs,
with descriptions and categories, is included as an appendix. Table 1 summarizes the
referential categories of Koko’s untaught signs, and Table 2 their types of iconicity or
other modes of depiction. Plate 1 illustrates some of Koko’s untaught signs.
Table 1. Referents of Koko’s Untaught Signs (First 10 Years)

Total invented signs 50
Signs for objects 27 54%
Signs for actions 17 34%
Other signs 6 (2 for qualities, 2 for states of 12%
attention, 2 deictic [pointing])
Table 2. Types of Representation Used by Koko
Note that the categories of iconic representation of object shape and action
are not mutually exclusive: there were a few signs that involved elements of both.
Total signs using iconic mode of description 38 76% of total untaught signs
Signs depicting action iconically but not necessarily 27 54% of total untaught signs
representing an action; may represent an object by 70% of iconic untaught signs
depicting action on or with that object.
Signs depicting shape of an object iconically 15 30% of total untaught signs
40% of iconic untaught signs
Browse Eye makeup Frown
Unattention Bite Hair barrette
Plate 1. Some of Koko’s untaught signs
Of Koko’s untaught signs during the first ten years of her life, approximately half
represented objects and another third, actions (Table 1). Three-quarters of her un-
taught signs involved an iconic mode of depiction (Table 2). Among these, approxi-
mately 70% involved depiction of action, either of an action itself or of a customary
action upon an object. Though these untaught signs were predominantly signs for ob-
jects, more than half of these objects were not represented by depicting their shape,
but by an action performed upon or with them. For instance, modeling clay was signed
by a motion of rolling the palms together, as when rolling out clay; a hand puppet by
the motion of putting the puppet on the hand. Some action mimes listed as represent-
ing objects might seem to be just as well translated as signs for actions, not for ob-
jects. However, Koko often used them to request the object in question (by accompa-
nying pointing or reaching with eye contact), thus indicating that an object was the
referent of the action.
In some cases the signs might be interpreted either way; in American Sign Lan-
guage, many signs can represent either an object or an action depending on repetition
and other differences in production. An action can refer to an object, and an object de-
piction may be part of an action request. Also, the categories of action and object de-
piction are not necessarily mutually exclusive because it is possible to indicate a shape
and also an action in a single sign. An example is Koko’s sign for dental floss, where
Koko picked her teeth with an index finger (untaught), and then made the taught sign
for thread, which traces the shape of dental floss.
About 40% of Koko’s untaught iconic signs represented an object by depicting an
element of the shape of the object. Since it is usually impossible to represent the en-
tirety of an action or an object with the hands, a salient aspect must be chosen to rep-
resent it. Such condensation of depiction is an aspect of both ape and human signing.
Koko’s specific choices of forms of metonymy, i.e., representing an object or action by
depicting just a part of it, will not be the focus here though well worthy of further
study. (A description of the form of each untaught sign can be found in the Appendix.)
Here we consider metonymic signs simply as iconic. Because our primary interest
here is the cognitive processes leading to the physical representation, we consider a
sign that describes any part of the physical form of an action or object to be the result
of some kind of process of iconic representation. Koko’s means of representation are
discussed in detail later in the section entitled “Koko’s Modes of Invention.”
Some of Koko’s untaught signs were not iconic. One was a deictic (pointing) sign
that indicated the location of an object (Koko’s early “notice” sign, glossed as bird at
the time because she co-opted elements of this taught sign and used it in a deictic man-
ner). Another sign simply located a referent on the self (e.g., body hair indicated by
grasping hair between the fingers). Koko also created signs that involved cross-modal
transfer of English sounds to a sign;4 for instance, blowing forcefully at someone to
express that they “blew it,” that is, performed an action she wasn’t pleased with (she
was quite familiar with the colloquial expression, frequently used in the spoken En-
glish of her companions, often to scold her). In this case, the “sign” is itself a sound,
accompanied by characteristic body posture and facial expression. Some inventions
were “blended” from several taught signs (e.g., apricot = the sign for peach made with
an “A” hand shape like apple). A few were of unknown or indiscernible origin (like
Koko’s lip in reference to human females, performed by rubbing an index finger hor-
izontally on her lips).
4. A study of Koko’s response to alterations in vowels or consonants in spoken words illustrated that Koko
can accurately perceive the sounds of human speech (Goodreau, Patterson & Tam, 1996; Patterson & Goodreau,
1987; Goodreau, 1987).
Another frequent element of Koko’s untaught signs, as well as of taught signs she
has altered to her personal preference, is locating them on her body as opposed to
forming them in space away from the body. Of her untaught signs, 60% were placed
on the body location of the referent.
Michael, Koko’s male gorilla companion, also used untaught signs, and Koko sub-
sequently adopted some of these for her own use. Untaught signs originated by
Michael but co-opted by Koko during the first ten years of the project were hit-in-
mouth, hit-in face, and pull-out-hair, all mimes of the described actions.
From Action to Object in the Creation of Gestures and Signs:

Zoo Gorillas and a Signing Gorilla Compared
Action and location, the preferred ways of depiction in Koko’s untaught signs, are
also frequently used in gestures of the gorillas observed at the San Francisco Zoo
(Tanner & Byrne, 1993, 1996, 1999) to communicate about features of behavior and
the environment. For both signing and non-signing gorillas, action and location (as the
beginning or ending point of action) seem to be the basic building blocks for expres-
sion. It is a short journey from describing an action or indicating a location to describ-
ing an object, because the action and location of an object can be employed in describ-
ing it gesturally, as in many of Koko’s inventions; and the outlining of action is not far
from the action of outlining an object.
Zoo gorillas have been observed to create depictions of action of the self or an-
other gorilla, and gestures of similar types have, though very rarely, been observed in
the wild (Schaller, 1963). Gorillas in the wild have been observed to enact actions an-
ticipated of the self or desired of others; zoo gorillas have been observed to trace the
trajectory of such actions on another’s body or in space.5 Captive studies (Tanner
1998; Tanner & Byrne 1999) give the approximate ages at which different classes of
gestures appear (see Table 3).
Table 3 illustrates the progression in taught and untaught gorillas from depiction
purely of action, to object depiction with signs or gestures. The developmental pro-
gression of sign invention by Koko can be found in records of her first untaught signs
(Patterson, 1980); Table 3 is thus ordered chronologically. The chronology for zoo-
living gorillas and gorillas in the wild is less precise because of more limited observa-
tion. Only one earliest example is given for each class of depiction in Table 3; in most
cases there were other examples of each class, and in the discussion following, some
of these are mentioned. Additional signs for each classification can also be found in
the descriptions in the Appendix. For some categories “invented” signs by Koko are
not found in available records but instead are listed as “natural” gestures in an earlier
study. The dividing line between “natural” gesture and “invented” sign cannot be a
5. There have also been some observations in the wild, such as those found in Schaller (1963) and Robert
Campbell’s unpublished film for Dian Fossey at the National Geographic Society (viewed in entirety by the first
author), that can give us an idea of at what stage mountain gorillas in their native environment make certain kinds
of gestures.
Table 3. From Actions to Objects in Gesture and Sign Invention: First Appearances of
Different Kinds of Representation.
Signing
gorilla, age
What Zoo, wild in years and
sign or gorillas, months
gesture Example earliest age when first
describes or How Where (English Physical observed used or
indicates produced formed gloss) description to be used invented
location touch on an object knock fist contacts object zoo age 7 knocks, age
indicated to location (other than such as rock or tree; 1 but not to
other self or other eye contact and indicate
gorilla) response waiting to location to
other gorilla other
that index finger or fin-
gers contact object not seen 1.0
location extend in space that, there index finger not seen 1.0
indicated to finger extended from hand
other toward toward location
location
action upon enacted in space up arms raised to zoo age 1; 1.0
self desired request or anticipate wild infant
from other being picked up by
adult
action enacted non- on other’s move away light push to other’s zoo age 2; 1.0
desired of forcefully body body wild adults
other
action mimed on own tickle index strokes under- not seen 1.2
desired of body arm or sole of foot
other
action traced on body of turn around on other’s waist, arm zoo age 7 1.11
desired of other moves from one side
other of body to other
object hand shape, on own bracelet, cupped hand pats not seen 2.8
location body hand puppet wrist
action traced in space away, go arm swept toward zoo age 6; 2.9
desired of other wild all ages
other
action upon enacted on own bite biting self on hand zoo age 7; 2.10
other body or wrist wild
anticipated juvenile
object action on or with hands clay flat hands, top hand not seen 3.8
of an object in space in moves back and
mimed front of forth over other palm
body
negation altering on own Frown manipulate face zoo age 7 4
facial body (KOKO)
expression cover up face with
hide play- hands
face (ZURA)
object tracing of on own eyeglasses index fingers trace not seen 6.1
shape of body lines from eyes to
object back of ears
Table 3. (Continued)
Signing
gorilla, age
What Zoo, wild in years and
sign or gorillas, months
gesture Example earliest age when first
describes or How Where (English Physical observed used or
indicates produced formed gloss) description to be used invented
location on touch move arm in armswing arm swings from zoo age 7 6.4
self location space, to under space in front of
indicated to location on (walk up body to between legs
other own body bottom)
object formed by in space pickle thumb and index not seen 7+
static hand extended from both
shape only fists held in space
in front of body
object tracing of in space thread two little fingers not seen (used only
shape of touch then move when taught
object apart horizontally by humans)
Observations of gestures in the wild come from the following sources, but primarily the publications
of George Schaller and Dian Fossey: Baumgartel, 1976; Burbridge, 1928; Campbell unpublished
film; Denis, 1963; Fay, 1989; Fossey, 1979, 1983; Mori, 1983; Schaller 1963/1976, 1964.
Sources: Patterson (1980); Patterson, Tanner & Mayer (1987); Patterson & Cohn (1990); Tanner (1998)
Arranged chronologically by order of appearance in signing gorilla.
firm one, as learning and genetics are so entwined for any behavior and further, since
we do not have good observations of behavior for all groups of gorillas, especially in
the wild. A better designation, which we use throughout, is simply between human-
taught and untaught signs.
Koko’s earliest recorded untaught signs were listed as “natural” signs, though her
standard deictic sign, pointing with the index finger, has not been reported in untaught
gorillas. Further untaught signs seen early in the first year of instruction (age 12–24
months) were up, requesting an action upon the self by another; and tactile signs such
as a light push to another, indicating move away. By the end of the year a tactile sign
using a tracing motion on another’s body appeared, requesting a companion to turn
around.
Gorillas at the San Francisco Zoo have been observed to use all the “natural” un-
taught gestures performed by Koko in her first year of sign instruction, except for point-
ing with the index finger. Later in development knock or pound (using the fist) and slap
(open hand) are used by zoo gorillas to touch objects in a clearly deictic fashion, with
eye contact and waiting for response from the partner gorilla.6 Such usage was ob-
served repeatedly in a 7-year-old gorilla and her older play partner but may appear ear-
lier; Tanner’s zoo observations began when the younger of her principal subjects was
already age 7. Subsequent observations of younger zoo gorillas by Tanner and others
6. See Leavens, Hopkins, & Bard, (1996), Leavens & Hopkins (1998, 1999), for discussions of variability of
form in pointing by chimpanzees. The development of pointing in human children and the criteria for social
pointing have been discussed by many scholars, for instance Butterworth (1996) and Bates, Benigni, Bretherton,
Camaioni, & Volterra (1979).
(Pika, Liebal, & Tomasello, 2003) did not find such referencing, however. Likewise,
tactile gestures on another’s body, requesting directional movement of the other gorilla,
were rarely seen in zoo gorillas until age 7.7 Miming on the gesturer’s own body of the
specific action desired of another was not observed at all in zoo gorillas.
The earliest untaught signs recorded as invented by Koko are blow and tickle,
which depicted actions desired of another and appeared during her second and third
months of sign instruction, when she was just over a year old. The earliest appearance
of blow was putting her index finger to another’s mouth when the person stopped blow-
ing, perhaps simply pointing; Koko appeared to want the person to continue blowing.
Koko then began to request the action “blow” by holding a finger up to her own mouth,
transferring the features of another’s body to her own. Tickle was likewise indicated by
miming the action desired of another on her own body. Her next sign was a deictic sign,
performed with two index fingers held together at the tips. This sign was directed to-
ward interesting objects out of reach, but was glossed bird because it incorporated el-
ements of a bird sign a teacher first used. Subsequently, however, Koko employed it
for many referents other than the bird the teacher had originally been pointing out.
Koko’s next type of untaught sign did not appear until over a year later, during
which time her taught ASL signing progressed rapidly. This sign, at age 2 years 8
months, was bracelet, performed by a cupped hand patting the wrist, first used request-
ing a new bracelet she was shown. This was her first sign created for an object, and in-
volved an iconic hand shape depiction as well as contacting the part of her own body
where the object usually was worn, thus perhaps involving a tactile element as in ear-
lier signs such as tickle. She later extended the use of the bracelet sign, referring to a
hand puppet on a companion’s hand as well as using the sign for bracelets. This seems
to be an extension of the ability to point out location to another, which Koko did at the
age of just one year. It is requesting “something on my body, wrapped around this lo-
cation.” A zoo gorilla (Kubie) comes close to this in a unique observation when he pats
his shoulders, with eye contact, in interaction with another gorilla (Zura), resulting in
her approaching Kubie and placing her hands on his shoulders (Tanner & Ernest, 1989).
Koko’s next untaught sign, bite, appeared at age 2 years 10 months (see Plate 1).
She placed the side of her hand or index finger in her mouth to request biting play
from a companion. A similar gesture has been observed in both free-living and zoo ju-
venile gorillas and the first author has observed it in captive monkeys where a play
partner was not physically available. Like Koko’s earliest untaught signs, bite repro-
duced the action desired of another, on her own body. Around the same time, another
untaught sign, away or go, appeared. It differed from the earlier sign, up, in that it de-
picted in space motion desired from another, not motion anticipated for the self. A sim-
ilar gesture was used by zoo gorillas from age 6, and has been seen in the wild.
At age 3 years, 8 months, a new type of depiction appeared: Koko’s sign for clay.
Koko requested clay by miming the customary action performed on the object, rolling a
7. Tactile gestures consisting of reaching, stretching and touching are seen early on (also in gorillas studied
by King, 2004) but not tracing a path of action or suggesting motion in a certain direction as found in older go-
rillas by Tanner and Byrne (1999).
ball of clay between the hands. This could be interpreted as depicting the activity of play-
ing with clay rather than the object itself, but Koko used such signs to request objects.
During Koko’s first five years, all her iconic inventions reproduced action of or upon an
object, or objects were indicated by simply placing an appropriate hand shape on her
body. No signs depicting an object or its action have been observed in zoo gorillas.
At age 6 years a new mode of depiction appeared for Koko: tracing the shape of
an object. Koko created a sign for eyeglasses where index fingers traced a line from
the eye to the back of the ears. Eventually, Koko produced a total of 15 inventions de-
scribing objects that involved depicting the shape rather than the action of an object
(see Appendix). A form of active “tracing” of the form of an object was used in five
cases; in ten cases, her depictions of shape were produced instead by a descriptive
hand shape (e.g., extended finger for a straight or narrow object, cupped hand for a
rounded object, index and thumb extended for a small rectangular object) placed on
an appropriate body location. Among Koko’s 50 inventions from her first 10 years
(listed in Appendix), all signs that depicted an action were performed on appropriate
body locations, and nearly all that depicted a shape were also performed touching her
body. An exception was her later invention at age 7 of a sign for pickle (described in
Table 3), with appropriate hand shapes in the space in front of the body. The only cat-
egory of object representation not found among Koko’s untaught signs during her first
ten years is the tracing of an object in space away from the body, though she uses such
signs when taught. (Thread, a taught sign used in her untaught compound sign for den-
tal floss, is such a sign).
Also between age 6 and 7, Koko produced a sign glossed walk-up-bottom, request-
ing her male gorilla companion to touch or tickle her bottom. A similar gesture was
frequently observed in zoo gorillas, described as armswing under. For the zoo goril-
las as for Koko, this gesture appeared in adolescence. For the zoo gorilla Kubie, this
often included a tap to the other gorilla, and then swinging the arm to a location be-
tween the legs. His version actually was a phrase that can be glossed as “you come
under,” that is, a request to make contact with the gesturer gorilla’s genital area.8
To summarize, the chronological development of modes of representation in
Koko’s spontaneously created signs is as follows:
1) (from age 1–2 years) depicting actions on her own body, another’s body, or in
space, to represent activity desired of another; and pointing to objects or loca-
tions desired or noted
2) (from age 2.8) placing the hand-shape of an object on an appropriate body lo-
cation, to represent an object or action
3) (from age 3.8) miming an action performed with or on an object in order to
represent an object
4) (from age 6) tracing on her body the outline of an object to describe the object
5) (from age 7) tracing a shape in space away from the body or using a hand
shape held in space away from the body to describe an object
8. For more about gesture phrases, see Tanner 2004.

These last two were the rarest of Koko’s means of representing objects, though
these methods of depiction are common in American Sign Language and are em-
ployed in many of her taught signs.
Development of Gesture in Zoo Gorillas

In zoo gorillas, gestures were utilized to depict action or indicate location, as de-
scribed above for Koko at age 1–2 years onward, but appeared later in the zoo goril-
las. Tanner’s zoo observations began when the two principal subjects, Kubie and Zura,
were already young adults. The earliest information available on Kubie showed that
nearly all his adult repertoire of gestures at age 13 was already present at age 8, in the
context of sexual positioning and sexual play with an older and uncooperative female
(Keller, 1984). Some play gestures were present at age 2 years. Sue Parker (1999), in
a study when Kubie was an infant, lists Kubie’s play “enticements” which include
“slapping surface, arm waving, chest beating, foot stamping, tagging, hand clapping,
head waggling.” These gestures at age 2 do not appear to include gestures that indi-
cate location or depict directional motion, tactile or otherwise.
A gesture used as a “negative” was seen in the zoo gorilla Zura from age 7; this
was hide playface, used to suppress the urge to play and understood by her male play
partner, who responded by not approaching (Tanner & Byrne, 1993); other gestures
were used as negatives also (Tanner, 2004). Koko at age 4 used a facial alteration,
frown, to show annoyance, disgust or negativity toward activities or objects. Later she
used an unattention sign, hands covering face, to avoid things she did not want to see
or participate in.
Because it was impossible to know whether gestures observed in the adult zoo sub-
jects might originally have appeared earlier, the question of when different kinds of
gestures develop was addressed later through observation of two male infants, Shango
and Barney, born into the group during the course of the study (Tanner & Byrne, 1999).
Their earliest discrete gestures were audible ones produced by contact with a surface
(e.g., ground, rock, tree or own body), actions that were also included in Kubie’s early
gestures listed by Parker (1999). They used reaches and arm extensions toward their
mother or other gorillas or toward objects of interest that another gorilla possessed, but
without the eye contact and response waiting that are hallmarks of real indication.
(However, responses from older gorillas to arm extensions may eventually lead to
awareness of their efficacy and establish them as indicating gestures.) New gestures
gradually appeared in the older brother, Shango; he began to use a few tactile gestures,
but at age 6 still used neither the silent gestures in space nor self-indicating gestures
that the young adults used. Barney, the younger brother, began at age 2 to frequently
use the armshake gesture observed in his father, but older brother Shango almost never
used it. Armshake, by iconically depicting action, may show desire for another gorilla
to approach and take play action. Other gestures by adult Kubie indicated approach
was desired to various body locations; examples are head nod, armswing under, slap
shoulders, and extended palm. Some gestures indicated locations in the environment;
such indicating gestures were all observed in gorillas aged 6 years and above. Repre-
sentation of objects or individuals found in the gorillas’ environment seemed to be ab-
sent. In summary, the zoo gorillas, without any human instruction, would depict on
their own body, on another’s body, or in space, actions desired from another, and would
manually indicate objects or locations of concern, but mostly after age 6. These kinds
of gestures were produced by Koko by age 2.
Discussion: Koko’s Modes of Invention

Whether the tracing of a shape or use of a “frozen” hand shape is the more abstract
method of depiction is an open question, but depiction of an object with hand shape
appeared earliest for Koko. The hand shape was placed on the relevant body location,
a development that seems to follow on from pointing to locations by touching them.
Tracing would seem to be a more precise or detailed way of mapping a shape. Koko
used both tracing and hand shape modes of depiction in taught signs before using sim-
ilar modes in untaught signs. In both types of signs, the concept of one’s own body as
a mirror of something “out there” is necessary. Consistent with this, Koko has shown
the ability to use mirrors appropriately (Patterson & Cohn, 1994).
Another aspect of Koko’s untaught signs for objects is that nearly all of her 27 ob-
ject signs were for referents that she could, and presumably did, touch and handle. The
motion, previously experienced, of rolling clay is easily performed when the clay is
not in the hands. Another invention, barrette, (see plate) reproduces the motion of
touching the length of a barrette (hair clip). Thermometer places a finger under the
arm, just like the real thermometer touches the underarm when Koko is given veteri-
nary treatment. The early invention, stethoscope, combines the learned sign necklace
with the placing of fingers in the ears, a mirror reproduction of the doctor’s action,
also a tactile reproduction when allowed to handle the stethoscope herself. Active tac-
tile experience with objects appears to play a part in eliciting manual expressions rep-
resenting absent objects.
“Tracing” untaught signs were the latest to appear in Koko’s repertoire, only cre-
ated after 6 years of age. Long-hair refers to long-haired humans, and traces the hair-
line of a human’s long hair on her own body, again a mirroring of something seen out-
side of herself. Filmers/reporters is likewise a tracing sign on her body, delineating
the straps of camera equipment on news reporters who visited her.
Koko had two frequent signs that also appeared after age 6, woman (lip) and man
(foot), that are not clearly iconic. They did, however, perhaps draw upon characteris-
tics of men and of women that were particularly salient for Koko, thus employing
metonymy, the representation of an object or concept by depiction of only a part of the
object. Like many signs in human sign languages, lip and foot are opaque and arbi-
trary to anyone without an intimate knowledge of their origins (Kendon, 1988; Arm-
strong, Stokoe, & Wilcox, 1995). “Woman” (lip) is an index finger rubbed horizon-
tally back and forth across the lips. Perhaps this is related to lipstick, a similar motion
performed with the thumb. However, lip is similar to another earlier sign of unknown
origin, glossed note, which Koko used before pointing to something of interest; this
note sign dropped out of her vocabulary after early years. “Man” (foot) appeared after
she began to take sexual interest in a human visitor not amongst her caretakers, a lab-
oratory worker who wore heavy boots, and it has been speculated that Koko was using
the boots as a point of reference; this visitor also sometimes played a game tickling
Koko’s foot, and she may have extended her foot to him then. There is another possi-
ble derivation, however. A gesture observed several times in the zoo female Zura (see
Table 4), consisted of turning the rear toward and extending a foot back to another go-
rilla, a mounting reference possibly derived during development from a signal com-
monly used by a mother for a youngster to get on her back. Zura sometimes tapped
the sole of her extended foot with her index finger as part of this signal, sometimes
only tapping the foot without presenting the rear, in the context of sexual play. This
tap foot is identical to Koko’s “man” (foot) sign, which Koko used frequently in the
context of human men, but not, for instance, for a “family” member such as her “sur-
rogate father” Ronald Cohn. If the derivation suggested is correct, it would be an ex-
ample of an adaptation of a “natural” behavior to a new context.
Untaught signs created by Koko after her first ten years have not been formally de-
scribed in academic publications but many are described in articles in the Gorilla
Foundation’s semi-annual Journal. Signs now regularly glossed as above and below,
whose meaning at first eluded researchers, have become a standard part of Koko’s
repertoire (Patterson & Tanner, 1988). These depict spatial location by moving a flat
palm forward off the top of the head (above) or moving a flat palm from between the
legs when seated (below).9 Another sign noted only in recent years has been glossed
as take-off, referring to removal of clothing, lifting both flat hands quickly off the top
of the head. Koko has also continued to transfer sounds of human speech into signed
form, as in her frequent sign for vegetable browse (see Plate), a term for which she
was not given a sign. The spoken word was not used until a change in diet when
browse items of leafy green vegetables began to be distributed to Koko at intervals
throughout the day. Koko makes the browse sign by placing a fist (“S”-hand) on her
brow, with the tapping motion of the sign for “lettuce” from American Sign Language
(Menendez & Patterson, 1994).
As well as inventing signs for referents for which she had not been provided with
an ASL sign, Koko replaces some of her taught signs with untaught ones for the same
referent, perhaps because her own versions are more meaningful to her when clearly
iconically related to a referent or touching her body. Also, as previously noted, she
seems to prefer signs without intricate hand configurations, substituting signs easier
for gorilla hands to articulate, and signs that touch her body. An example is her usage
(a cross-modal transfer) of knee (tapping a finger on her knee) for “need,” for which
she had a taught sign; the ASL version of need is performed with a crooked index fin-
ger moving downward in the open space in front of the body. Another untaught sign
that makes use of gorilla anatomy is Koko’s exaggerated version of frown, using
her hands to pull her lower lip down rather than simply tracing downward lines at the
corner of the mouth as in the ASL sign. In many ASL signs she retains the motion and
place of a sign but changes or simplifies hand shape; in some she retains motion and
9. This depiction of the concept that something is located below something else seems to be a directional re-
versal of Koko’s walk-up-bottom sign and Kubie’s frequent armswing under gesture.
hand shape but changes the place, usually to her body or a surface in her environment
such as wall or floor.
Gestures Found in Both Signing Gorillas and Zoo Gorillas

The number of communicative gestures shared by taught and untaught gorillas
may be underestimated. Patterson and Tanner (1988) list untaught signs of Koko’s that
duplicate gestures described for one or more of the gorillas at the San Francisco Zoo.
Table 4 lists gestures of Koko’s that have also been observed in zoo gorillas or in the
wild. A few gestures listed here overlap with those listed among Koko’s “invented”
signs from Patterson and Cohn (1990); at the time of observation, these were not
known to be used by other gorillas. Though not all have been seen in all gorillas, most
have been observed in more than one zoo gorilla. Some of the gestures have not been
reported in gorillas other than Koko and the San Francisco Zoo gorillas and may be
similar because of a capacity of gorillas (and other apes) to form iconic gestures,
rather than the gestures themselves being genetically predetermined. Similar gestures
have been observed in other ape species (Fouts, 1997; Miles, 1978, 1993), and often
have different functions both in different species and for individuals within a species
(Tanner, 1998). Functions of many gestures are similar for both Koko and the zoo go-
rillas, but there are also some differences. All these shared gestures are social in func-
tion, used in interaction with other individuals to regulate actions and locations of
activity. For Koko, such gestures were incorporated into her signed discourses and
thus were used linguistically regardless of their origin. Non-sign-taught apes, who
have been trained with lexigrams or computers, also incorporate “species-typical”
gestures into their communications (Savage-Rumbaugh, 1986; Greenfield & Savage-
Rumbaugh, 1990). For the zoo gorillas too, gestures often did not stand alone but were
incorporated into strings of other gestures (Tanner, 2004).
General Discussion
A gorilla tutored in sign language and gorillas living in a zoo both create signs or
gestures that depict and invite action and point out objects and locations, but signs that
refer to objects themselves are invented only by the signing gorilla. Many of the un-
taught signs of signing apes and the gestures of non-signing apes have iconic charac-
teristics. Iconic descriptions can be formed in several different ways, depending on
what aspect of an action or object is chosen as salient, i.e., what kind of metonymy is
employed. Gestures describing similar actions or objects, therefore, may vary within
and between different groups of apes (Tanner, 1998). On the other hand, some gestures
or signs that are physically very similar are shared between signing and non-signing
apes but may not have the same functions; these may be iconic gestures that are sim-
ilar in appearance because they describe similar material, or may be hitherto little
known species-typical gestures elicited by a relevant social environment (see Table 4).
Table 4. Koko’s Untaught Gestures Seen in Other Gorillas

Koko’s untaught Koko’s usage Where
signs also observed with Gorilla Usage at observed
in other gorillas Foundation gloss San Francisco Zoo (zoo, wild)
armcross (glossed as catch) used in activi- play contexts; function otherwise zoos and
ties involving tossing and catch- unknown wild
ing of objects; chase games,
playing hard to get; also request-
ing embrace or desirable objects
armshake (glossed as play or hurry) play invitation, readiness for activity; SF Zoo,
invitation to play; also expression sometimes warning or threat (only not in
of excitement or impatience used this way by one individual) wild
armswing under (glossed as walk-up-bottom) invitation for contact in sexual play SF Zoo,
sexual solicitation or request for not in
tickling of bottom wild
away (glossed as stop) to stop advance agonistic contexts, avoidance of zoos and
of another individual contact wild
backhand (glossed as darn) expresses gaining attention in play situations, zoos and
annoyance or frustration also used in agonistic display or wild
protest
bite in playful excitement, referring in play, before or after biting play zoos and
to biting wild
chestbeat excitement, agitation, but also in excitement, agitation, attention zoos and
a more controlled form glossed getting wild
as gorilla
circle hands (glossed as gentle) request for unknown, but seen in play contexts zoos and
gentle behavior wild
clap playfulness or excitement in play, often solitary and before zoos and
performing a physical action like wild
jumping or balancing
deictic (pointing) (glossed as me, you, that, there, designating other or self as object or zoos and
gestures your) designating numerous agent of action; also designating loca- wild
referents and locations; Koko tions. Performed with open hand,
performs points with extended knuckles or fist. Glossed as chest fist
index finger. Your is performed pat, tap other, pound, extended palm
with outstretched palm, may
designate another’s property or
turn for action.
extended palm (glossed as come-gimme) invitation to contact or request for zoos and
(could be included requesting objects or the food wild
with deictic gestures) approach of other individuals
facewipe (glossed as toilet, b.s.) expression annoyance, avoidance SF Zoo
of disbelief, uncertainty or
annoyance
foot designating the body part, also seen in a zoo gorilla, a variation of one SF
referring to human males foot back sexual invitation performed Zoo
by tapping the foot with the hand gorilla
hand between legs (glossed as below) performed play, sexual invitation (usually patting SF Zoo,
seated; hand moving out from motion) Rio
under body designates location Grande
below or under another object. Zoo
When forceful slapping motion, a
masturbation activity.
Table 4. (Continued)
Koko’s untaught Koko’s usage Where
signs also observed with Gorilla Usage at observed
in other gorillas Foundation gloss San Francisco Zoo (zoo, wild)
hands behind back (glossed as walk-up-back) inviting play activity or approach zoos
requesting companions fingers from companion seated behind self
walked up back, tickling
head nod (glossed as yes) agreement, inviting approach or visual attention one SF
assent of other gorilla Zoo gorilla,
wild
head shake, head (glossed as no) dissent head shake used in playful contexts; zoos and
turn head turn sometimes avoidance wild
or possible request for change of
direction
knock, pound attention getting, or cross-modal get visual attention in playful context; zoos and
(fist hand shape) transfer of English “obnoxious” indicate location or direction wild
slap surface (for Koko, glossed as pound) play or chase invitation zoos and
(flat hand) play invitation of challenge; wild
referential use to request attention getter
pounding on her back
tactile gestures indicate movement desired from indicate movement desired from an- zoos and
another by non-forceful contact other by non-forceful contact or mo- wild
or motion upon other’s body; can tion upon other’s body; can take
take many different forms: can many different forms: moving hand
take many different forms: mov- down back vertically or across hori-
ing hand down back vertically zontally, patting, gentle pulling of
or across horizontally, patting, hand, light push away, and others
gentle pulling of hand, light push
away, and others
up for movement upward; request to request or intention to move upward zoos and
be picked up wild
Observations of gestures in the wild come from the following sources, but primarily the publications
of George Schaller and Dian Fossey: Baumgartel, 1976; Burbridge, 1928; Campbell unpublished
film; Denis, 1963; Fay, 1989; Fossey, 1979, 1983; Mori, 1983; Schaller 1963/1976, 1964.
(Koko’s usages from Patterson, 1980; Patterson & Tanner, 1988; zoo data from Tanner, 1998)
The fact that some of the gestures performed by signing apes resemble those of
apes in the wild has been seized upon by some as evidence that apes do not really learn
human sign languages, but only perform gestures that they would “naturally” use any-
way (Pinker, 1994; Wallman, 1992). The accumulation of evidence does not support
contentions that signing apes do not really use sign language but only adapt their
species-typical gestures. “Natural” or species-typical gestures are indeed used by
symbol-taught apes, but they may often elaborate upon them and have opportunities
to use them in a greater variety of contexts than do apes in the zoo or in the wild. In
addition to such species-typical gestures, apes with different upbringings are likely to
invent gestures similar to each other’s, given a common ability for iconic representa-
tion, similar anatomies, and similar material to describe. In addition, signing apes, of
course, use a large vocabulary of taught standard sign language in addition to species-
typical gestures and untaught signs. Even when modified by anatomy of the ape hand,
much of this signing is nothing like their “natural” gestures. Few gestures resembling
American Sign Language signs are spontaneously formed by untaught apes, who use
a limited number of hand shapes compared to apes taught ASL.10
The iconic gestures a signing gorilla creates are more numerous and elaborate than
those of zoo captives, probably because of intensive exposure to symbolic modes of
communication and interaction with humans. Early input may alter brain utilization in
humans (for instance, a heightened sense of pitch in humans blind since infancy,
Gougoux, Lepore, Lassonde, Voss, Zatorre, & Belin, 2004) and no doubt in apes (Bard
& Vauclair, 1984; Povinelli, 1994). A recent experiment with marmosets (South Amer-
ican monkeys) showed that in only one month, those monkeys housed in larger and
more enriched environments actually developed denser neuron growth and had more
of the synaptic proteins the brain uses in relaying messages between neurons, in con-
trast to control subjects housed in minimal caged situations (Kozorovitskiy, Gross,
Kopil, Battaglia, McBreen, Stranahan, & Gould, 2005).
Where great apes have been shown to possess capacities once reserved for hu-
mans, such as the ability to imitate goal-directed actions and understand their reflec-
tion in mirrors and employ referential pointing, the apes have often been individuals
raised by humans (discussions of the strong claim that human-rearing “enculturates”
apes, giving them human capacities they do not naturally develop, are found in sev-
eral chapters in Parker, Mitchell, & Boccia, 1994). Skills salient in humans would be
likely to be more utilized in apes with a good deal of exposure to humans (Povinelli,
1994; Gomez, 2004). Iconic representation is, after all, related to imitation in that it is
a form of mime, and requires the taking of another’s perspective when depicting an
action or object outside the self as well as kinesthetic/visual matching (Mitchell, 1994;
Byrne, 1995). Expressing, in iconic fashion, action desired from another appears rel-
atively late in Koko’s inventions (age 2) and even later in zoo gorillas’ development
(age 6–7). Request for another’s action upon the gesturer’s own body appears earlier.
Gestures requesting action of another require understanding of the other as an inde-
pendent agent and also an understanding of the other’s point of view. For instance, the
gorilla must have an awareness that the visual attention of the partner is necessary for
communicating with gestures; such understanding was present in the adolescent zoo
gorillas studied by Tanner and Byrne (and in younger gorillas; see Gomez, 1990,
1991, 1994, 1996).
Koko moves further than zoo subjects with her untaught signs: from depicting so-
cial action, to use of a “still” image to represent an object, to reproduction of custom-
ary behavioral action upon an object to represent that object, then to tracing the out-
line of an object. Thus there is a transition from pure behavior and “intention
movements” to representation of proposed action from others (rather than one’s own
action), and finally to non-action representation of objects.
Signing apes and zoo captives have in common action and location as the most
prevalent descriptive elements used in forming their gestural creations, even those un-
10. American Sign Language has nineteen primary hand shapes plus twice as many variations; a deaf human
child untutored in sign language created nine hand shapes (Goldin-Meadow, 1984). Untutored gorillas seem per-
haps to have three: open palm, fist, and knuckle hand.
taught signs of the gorilla Koko that represent objects. This may be because of the go-
rilla’s limited comfort with the intricate hand shapes utilized in human sign language
that would more precisely describe object shape, but are not suited to gorilla anatomy.
Alternatively, however, preference for action as a descriptive mode may be related to
cognitive processing. The brain has specialized cells for visual reception of hand and
limb movement that respond strongly to hand-object interactions (Perrett et al., 1989).
More recently neurons termed mirror neurons have been found to react to actions per-
formed on objects, but do not react to an object alone, or to the same action performed
without an object involved (Gallese, Fadiga, Fogassi, & Rizzolatti, 1996; Rizzolatti,
Fadiga, Fogassi, & Gallese, 1996; Rizzolatti & Arbib, 1998; see Rizzolatti & Craig-
hero, 2004, for a review of mirror neuron research, and Roy & Arbib, 2005; Arbib,
2002, 2005, regarding implications for language production and perception). Most re-
cently, research has shown that the understanding of others’ manual actions is influ-
enced by context (objects nearby) that implies what the subject’s intention might be
(Iacoboni, Molnar-Szakzac, Gallese, Buccioni, Mazziotta, & Rizzolatti, 2005). The
implication that actions are understood through their context and that objects are un-
derstood through the actions performed on or with them aligns well with the fact that
the majority of Koko’s untaught signs for objects were made by portraying a custom-
ary action associated with the object.
Within the framework of the function of mirror neurons, Arbib provides a scenario
that neatly parallels the progression we have found in moving from zoo gorillas’ spon-
taneous gestures depicting action, to Koko’s inventions for objects. Demonstrating
how bridging from action to language could take place, Arbib (2002) provides a hy-
pothetical sequence for development of gesture in evolutionary history that moves
from pragmatic action towards a goal object, to imitation of such actions (required in
order for Koko to establish an iconic sign for new objects/actions), to pantomime pro-
duced away from the goal object (what Koko does when establishing a new sign in her
vocabulary, getting the observer to focus on a specific action, or an object associated
with it). The next stages Arbib posits are: abstracting gestures from their pragmatic
origins, which is what happens when Koko makes a (metonymic) choice of what as-
pect of action to use to henceforth represent the target action or object; then using the
new sign in compounds with other previously established taught or untaught signs, as
she does. Koko presumably jumps up to the latter phases, not found in zoo gorillas or
other untaught apes, because her enculturation with human communication enhances
her understanding of shared attention and conventions of language.
The predominance of descriptive action in untaught signs may be biologically fa-
cilitated by the mirror neuron system; proximately, it may be due to the fact that it is
through shared action that social discourse takes place between gorilla and gorilla, or
gorilla and human companion in Koko’s case. For Koko, the introduction of a new and
unfamiliar object like a stethoscope or modeling clay would be meaningless without
a demonstration of the usage of that object, and it is that usage that makes the object
come alive as a part of the shared interaction involving it.
In Koko’s development, actions were depicted earlier than hand-shape object
descriptions, and tracing of outlines of objects was latest to appear. Tracing a shape is
cognitively very close to drawing or writing (as noted by Edwards, 1979). Koko is
able to paint depictions of objects that are correctly placed in their relative spatial and
size locations and to select appropriate paint colors, but her paintings are not always
detailed in reproduction of shape (for a photograph of a painting and its model see Pat-
terson, 1985).11 Because the tracing of shapes for Koko seems to be most comfortably
and extensively performed on the surface of her own body, there might also be a tac-
tile element involved in some of her signs; the hand shape for glasses, for instance,
might involve a tactile memory of touching the frames of glasses on one’s head, or for
scarf, the feeling of a scarf covering her head. Koko, in her learned ASL signs, was
taught numerous signs for objects that were not touchable, or could not be touched by
her: examples might be clouds, sun, tree, and house. These signs, however, are not
among her most frequent spontaneously used vocabulary items.
Though a tactile element is part of many of Koko’s untaught gestures, some of
these signs apparently originate from transfer of a visual feature observed on someone
else onto herself, as in her sign for filmers/reporters (tracing the outline of the straps
seen on camera bags). Transferring features observed on someone else to one’s own
body is rather like touching oneself on a location observed in a mirror. For humans,
feeling that one is actually tracing the outline of an object in a tactile manner when
putting it on paper has been shown to produce accurate and natural artistic depictions,
even by those with no artistic training; most people, however, instead perform the in-
termediary step of mentally representing, or visualizing, an object to oneself and only
after this drawing it on paper (Edwards, 1979). In the zoo gorillas, tracing of motion
on another gorilla’s body is a frequent medium of requests for action. This tactile
propensity, born from physical interaction, may underlie many of the inventions of
both the zoo gorillas and Koko. The model object was present when Koko first cre-
ated her “shape tracing” signs, but she also used them later in the absence of the orig-
inal model, implying memory of either the shape of the object or her previous actions.
Gorilla gestures, both of zoo and signing gorillas, seem to arise from an under-
standing of paths of action that can be tactile, visual or locomotor. Underlying the ges-
tural abilities of all great apes is the anatomical characteristic of rotational movement
of the joints, a characteristic that humans share, derived originally as an adaptation to
brachiation under tree limbs and arboreal “clambering.” The locomotor adaptations
permitting brachiation in apes allow a much greater flexibility of limb control than
possessed by monkeys, which potentially has consequences for all manual activities
(Morbeck, 1994). Several theories have been put forward that specifically relate ape
cognition to demands of the physical environment (reviewed in Byrne, 1997). Parker
and Gibson (1977, 1979; see also Bard, 1990) propose that seasonal foraging, on foods
that require extraction from a matrix, selected for tool-using propensities and abilities.
Povinelli and Cant (1995) (see also Chevalier-Skolnikoff, Galdikas, & Skolnikoff,
1982, p. 643) propose that arboreal clambering, by an animal too large to risk a fall,
selected for the ability to imagine itself in a detached, objective way and thus plan safe
routes through the canopy, dealing with constantly changing conditions in transferring
11. Chimpanzees and other apes have also painted; for a most extensive illustrated discussion, see Morris,
1961, and Hoyt’s (1941) early description for the gorilla Toto.
from tree to tree. Orangutans use supports that are flimsy relative to their weight much
more often than do monkeys in the same habitat, and use multiple supports, whereas
monkeys prefer single supports. On this theory, viewing the self as an object led to the
ability in apes to recognize their own selves reflected in a mirror.
Both the extractive foraging and complex locomotion accounts focus on a single
modern species (the tool-using chimpanzee, the arboreal clambering orangutan) as
models of the common ape ancestor, making them difficult to test against comparative
data. Byrne (1997, 1998, 2000, in press) proposes that feeding competition from sym-
patric monkeys—smaller animals with lower metabolic needs, more efficient long-
range travel, and ability to eat less ripe fruit—selected for skills in manual foraging,
allowing apes to exploit foods unavailable to their competitors, such as insects within
mounds or trees, and plants defended by spines or stings. All modern apes feed in
ways that are manually skillful compared with monkeys, involving complex, hierar-
chically organized techniques that are unlikely to be invented by a solitary individual
(Byrne, 2002). Critical to skill acquisition, then, is the ape’s ability to decipher the
skilled manual actions of others and thereby learn novel techniques (Byrne & Rus-
son,1998; Byrne, 2003; Whiten, Horner, de Waal, 2005). Behavior parsing and hierar-
chical program-building abilities, functioning to allow apes to exploit a wider range
of foods by allowing traditions of skill to accumulate by social learning, have been ex-
plicitly related to the origins of gestural communication (Byrne, 2000, in press).
Building up hierarchically structured action-plans, from simpler building blocks of
actions in the ape’s extensive manual repertoire, is seen as the evolutionary origin of
the syntactic structuring of language components. However, none of these theories
deals specifically with the iconic abilities that have been a prominent focus of the
present analysis. Iconic gestures are anticipations of action, including actions of oth-
ers as well as anticipated or previously experienced actions of the agent itself, that the
gesturing gorilla must be able to represent mentally and then express through a kind
of mime. Moreover, the gorilla is apparently able to translate between different scales,
expressing desired large-scale body movements of others by using the smaller com-
pass of its own hand gestures.
We propose that action mapping in three-dimensional space is an important capa-
bility of all great apes. Action mapping can be defined as the mental ability to picture
motion in space, predict its results before performing it, and translate from the large-
scale of real world motions of bodies (whether observed, remembered, or anticipated)
into the smaller scale of hand movements that iconically describe them. The capacity
to map seamlessly from observed bodily motions to corresponding actions of the self
appears closely related to the “active intermodal matching” theory, proposed by Melt-
zoff & Moore (1977) (Meltzoff, 1996) to underlie the ability of very young children
to copy the facial gestures of adults. They suggest that humans are born equipped with
the ability to match their own muscular movements with the movements they see oth-
ers make, a 1:1 system of correspondence that bridges across modalities. The action
mapping concept also is supported by the existence of mirror neurons and their func-
tions, as discussed earlier. In a communicative context, as in gorilla gesturing, action
mapping would mean mentally picturing motion in space and its possible results (ei-
ther on the basis of memory or anticipatory planning) and then performing it, without
the need for any step-by-step shaping process. In communication, action in real space
can be “miniaturized,” mapped in hands or arms.12
Though it seems that many gestures may be mapped directly to the hands from ac-
tion in the real world, some form of imitative process is often posited as a way in which
novel communication might be propagated. Let us look at the evidence for imitation, or
any kind of social learning, of gestures. Frans de Waal describes the spread of a behav-
ioral tradition in captive chimpanzees (de Waal & Seres, 1997). The capacity to repro-
duce nonfunctional limb motions demonstrated by a human in a “do as I do” task has
been shown in captive chimpanzees (Custance et al., 1995) and also in gorillas (Byrne
& Tanner, 2006 in press). Orangutans imitate elaborate human activities, sometimes in-
volving a series of several actions (Russon & Galdikas, 1993), and imitation at a pro-
gram level seems to be the best explanation for the complex, hierarchically-organized,
and highly plant-specific feeding techniques seen in mountain gorillas (Byrne & Byrne,
1993; Byrne & Russon, 1998). For gorillas raised in a signing environment, imitation
of a human’s signs is a frequent way of learning new signs, even in a gorilla not for-
mally taught signs. Ndume, an adult male gorilla brought to the Gorilla Foundation to
be a companion to Koko, was never formally taught any sign language, but began grad-
ually to use some of the same signs that Koko and her gorilla companion Michael had
been taught, and to compound signs (Patterson & Gordon, 2002; Patterson, 2005).
At the zoo, some evidence speaks against imitation as a way of learning gestures.
Many of the gestures shared by all the gorillas in the San Francisco group are gener-
ally accepted as species-typical. The use of a few gestures by some but not all mem-
bers of the group remains unexplained. The gesture armshake, for instance, is not seen
in all gorillas, though it has been recorded at several zoos and was used by several
members of the San Francisco Zoo group. Kubie’s son, Shango, who at an early age
watched many of the play sessions between Kubie and Zura during which armshake
was frequent, never developed armshake as a part of his gestural repertoire, and it has
only very rarely been observed in his mother, Bawang. On the other hand, Shango’s
younger brother Barney armshakes frequently and seemed to move from, in earliest
observations, using armshake in a solitary way, to using it socially. Pika et al. (2003)
found some gestures that were widespread among members of one zoo group studied,
but not found at all in another group elsewhere. Stoinski (2006) in a survey of goril-
las in different zoos found that numerous behaviors, including gestures, varied consid-
erably from zoo to zoo, indicating each zoo had its own set of potentially cultural
behaviors.
Another indication of gorillas’ capacity to remember and reproduce actions comes
from the observation of repeated sequences of actions, gestural and otherwise, by go-
rillas in the San Francisco Zoo group (Tanner, 1998), in contexts of play and display.
Though they involved the reproduction of a gorilla’s own previous actions, not those
of another, these sequences show that the memory capacity necessary for reproduction
of complex activities is available for the gorilla. Ability to reproduce complex se-
quences of functional activities makes sense in the action mapping context.
12. Gestures in adults are miniaturized in comparison to those of young children (McNeill, 1992).
The work of Tomasello and colleagues posits ontogenetic ritualization, a process
of fading or shaping frequently performed actions in repeated interactions with an-
other individual, as the main process through which ape gesture is created (Tomasello,
Kruger, Farrar, & Evans,1985; Tomasello, Gust, &, Frost, 1989; Tomasello, Savage-
Rumbaugh, & Kruger, 1993; Tomasello, Call, Nagell, Olguin, & Carpenter, 1994;
Tomasello, 1999 for an overview). The adaptive explanation of action mapping is a
simpler one than ontogenetic ritualization, which as a process has been deduced but
never actually observed in full. In the experience of the present authors, ontogenetic
ritualization is not a completely satisfying explanation of all inventions by zoo goril-
las or by signing gorillas. Instead, much invention appears to begin not with shaping
of a functional action directed toward another gorilla, but with one of these two
processes: (1) a spontaneous natural body movement (perhaps a sign or gesture such
as armshake) is expanded or altered when re-used in varying situations of social inter-
action, eventually gaining meaning through repeated interactions, or (2), an iconic
movement is produced by putting into manual motion an action mentally anticipated
or desired. For Koko, this, with manual reproduction of shapes of objects as well as
actions, was the primary method of invention. Such gestures or signs, generated by ei-
ther process, may vary in scope, size, and dynamic according to context, as do signs
in human sign languages. Type (1) invention is not entirely removed from the idea of
ontogenetic ritualization though it need not begin with a functional action; type (2),
however, would be generated by action mapping without any need for a ritualization
process. Koko’s gestures, above, below and browse, discussed earlier in this paper
were all spontaneously used by the gorilla well before human companions understood
them, thus no shaping process could exist. In the zoo, Barney’s usage of armshake ap-
peared to develop from spontaneous use of an idiosyncratic, but anatomically feasible
movement, used at first in a solitary context and only later developed in social con-
texts. It is also not impossible that the two kinds of gesture creation described above
could both be used in forming one meaningful gestural motion, though an example has
not been found at present.
Pointing and other deictic gesture is not well explained by ontogenetic ritualiza-
tion. There are too many variations in size, scope, location, and orientation of gestures
indicating locations for each gesture to be likely to be individually ritualized. Like-
wise, though zoo gorillas’ tactile iconic gestures may appear to be “faded” from force-
ful actions, new gestures constantly appear in different directions and dimensions,
with no two exactly alike. It is unlikely that each gesture would be individually faded.
Many untaught gorilla gestures combine action mapping with the deictic principle of
locating a sign appropriately in a certain location, on one’s own body or on another’s
body. An example from zoo gorilla Kubie, come shoulders, involved patting both his
shoulders with his palms, to which play partner Zura responded by approaching and
placing her hands on his shoulders (Tanner & Ernest, 1989). Koko also early gener-
ated an untaught “pointing” sign. The taught sign “bird,” used by her instructor to
point out a bird seen through the window was co-opted by Koko as a sign for various
animals and novel objects on the other side of the window. Koko used both index fin-
gers to point in a configuration similar to the original sign performed by the instruc-
tor, an extended thumb and index finger.
At the San Francisco Zoo, Kubie used his established repertoire of gestures with
several gorillas and was later understood by new individuals. He used most of the
same repertoire of gestures he used with Zura in his interactions with two other fe-
males in the group during other time periods years apart. His most frequent gestures
were all used regularly over a period of more than seven years, though proportions of
the different gesture types used with each female varied. Apparently different recipi-
ents were able to interpret his actions and the resulting interactions were favorable
often enough that it benefited each new pair to establish such communication. Action
mapping as a cognitive ability shared by apes explains this mutual understanding of
iconic gesture between different partners without any need for re-shaping.
Thus, though gorillas in the zoo group varied in their repertoires of gestures, with
some gestures being shared with other gorillas, and others unique to individuals, the
gorillas still seemed to have developed a mutually understood system of communica-
tion. This was particularly striking in Kubie and Zura’s interactions; their gestures
often alternated in a turn-taking conversational manner and seemed to be used to make
decisions about type, timing, and location of play as well as simply promoting contact
(Tanner, 2004).
Koko’s untaught signs for objects are unlikely to be explained as “faded” from ac-
tion, but they can be understood as formed by an ability to map and mirror visual input
with the hands. Ontogenetic ritualization “takes two” to shape gestures for mutual in-
teraction, but originating a sign for an object does not require interaction for its inven-
tion, only to establish it as a mutual communicative element. Shared cognition and
shared backgrounds along with shared interaction with objects, make understanding
of such signs possible. Koko’s newly untaught iconic signs thus eventually make good
sense, once decoded by human companions.
Because anatomy and behavior evolve in interaction with the environment, the
contexts in which gestures most frequently take place are important in understanding
what their ultimate function might be. The gestures observed in zoo gorillas were at
their highest frequencies in play and quasi-sexual situations, and pygmy chimpanzees
(also known as bonobos) in captivity used iconic gestures to settle on copulatory po-
sitioning (Savage & Rumbaugh, 1977). Further, Crawford (1937) saw the spontaneous
emergence of much gesturing in an artificial context where two chimpanzees had to
cooperate and coordinate their movements in order to receive food rewards. Signing
chimpanzees, when observed through remote videotaping with no humans present,
conversed with signs and gestures about play, grooming, and other social matters but
hardly at all about food and eating or discipline and dominance (Fouts & Fouts, 1989).
What all these situations of rich communication have in common is the necessity of
coordination of movement around the environment, or cooperation in movement. The
term co-regulation in the manner of Alan Fogel’s mothers and children could just as
well be applied (Fogel, 1993). Visual and tactile gestures proliferate when mainte-
nance of close contact with another, or closely coordinated movement, is necessary for
interaction to be successful (King, 2004).
Gestures and signs also obviously thrive when an environment is vested with con-
specifics and objects with which interaction is desirable and pleasurable; Greenspan
and Shanker (2004) describe the importance of function and emotion and how com-
plementary they are in the development of communication. In a study of the pragmatic
functions of Koko’s signing during her first year of instruction (between age 1 and 2
years), the categories found to be used by human children were all used by Koko;
these included labeling, repeating, answering, requesting action, requesting an answer,
calling, greeting, and protesting (Patterson, Tanner, & Mayer, 1988). A glance at the
list of Koko’s inventions (Appendix) shows that her untaught signs were for things
and activities in her environment that Koko was interested in, but for which she had
not been taught a sign. She needed signs in order to maintain shared attention with her
companions, and so generated ones of her own invention. In some cases, her signs
were emotional comments, such as her unlisten, unattention, frown, and blew-it signs.
Koko and her gorilla companion Michael’s sign acquisition has been compared to
that of signing human children in several studies by Bonvillian and Patterson (1993,
1999). Similarities were found in type of vocabulary content, acquisition of referen-
tial signing, and in the generation of various non-sign gestures. Differences were
found in rates and patterns of early language and gestural milestones, with gorillas
reaching many of these milestones but at a slower rate than children. The same could
be said for the zoo gorillas in comparison to the sign-instructed gorillas. Comparison
of the untaught signs of Koko, a signing gorilla, and gestures of zoo gorillas shows a
continuum of representation, where a signing gorilla moves further than the zoo goril-
las along a line that proceeds from behavior directed at immediate goals, to represen-
tation of desired action, to representation of objects.
Gesture may well be the structural foundation upon which language is built, and
we can find in gesture the thread of evolutionary continuity between animal action and
human language (King, 1999; Byrne, in press). The present study shows that it is
likely that in the history of our hominoid ancestors, the earliest iconic depictions were
of action rather than objects, just as we find in apes. Because such iconic capacity is
present in gorillas, and surely in orangutans, given their related ability to imitate and
to use human sign language (Russon & Galdikas, 1993; Miles & Harper, 1994; Miles
et al., 1996; Shapiro & Galdikas, 1995), it was most likely present 10 million years
ago in the common ancestor of hominoids. New means of communication, when they
occurred in our ape ancestors, would certainly have achieved increased success for in-
dividuals in social, and ultimately, sexual relationships. Such behavior would surely
have selective value, and over generations result in gestures becoming increasingly
frequent and complex. Through the condensation of real activity to something repre-
senting it, in forms progressively more removed from the original, hominid commu-
nication have, over millions of years, reached the arbitrariness that is a characteristic
of human language. But not all of human language even today is purely arbitrary. We
can still see glimpses, particularly in sign languages, of the development of language
from the raw materials of action (Armstrong et al., 1995). The creation and usage by
gorillas of special repertoires of gestures gives us a window into the developmental
processes and environmental pressures that might have led an ancestor ape to further
refinement of iconic communication, and its eventual expansion to human gestures of
the mouth.
Credits: The authors wish to thank Barbara King, Christa Nunes, and two anonymous
reviewers for their time spent reading this paper and for their helpful suggestions. The
first author wishes to thank Charles L. Ernest, her husband, for his video documenta-
tion since 1988 of the San Francisco Zoo gorillas and their gestures, as well as contin-
ual technical support of all kinds.
Appendix
Koko’s untaught signs: first 10 years
(Signs from Patterson & Cohn, 1990, analysis of iconic characteristics by first author)
Key:
O: object
A: action
D: deictic
IS: iconic for shape of object
IA: iconic for an action
BL: indicates (self) body location of referent
BLO: on body of other person or gorilla
CMT: cross-modal transfer from English sounds
D: deictic; pointing
U: unknown derivation
FA: functional action
Gloss in English Physical form Type of iconicity or Kind of
and classification of untaught sign other type of reference representation
apricot “A” hand shape with motion like cross-modal transfer from CMT
O “peach” sign (hand brushed English sound as well as
down cheek) compounding signs
barrette index finger draws line forward draws shape of object, also IS, BL
O above ear where barrette is usu- places on body location
ally placed
bird (notice) index fingers, held together at deictic D
D tips, point to location of object
of interest that is out of reach
bite teeth bite index finger side of iconic for action IA
A hand
blew-it loud exhalation: blowing sound cross-modal transfer from CMT
A directed at offending person English sound
blow blows on index finger held verti- iconic for action IA
A cally in front of mouth
body hair fluffing up hair on the body by indicating part of body BL
O rubbing both hands up and down
on body
bracelet cupped hand encircles and pats iconic for shape of object, IS, BL
O wrist placed on body location

clay palms together, move back and iconic for action, on cus- IA, BL
O forth in circular rolling motion tomary body location
dental floss pick index on teeth plus thread iconic for shape and action, IA, IS, BL
O sign (two little fingers touch on body location
then move apart horizontally)
drip-chin mime with index the action of iconic for action, on body IA, BL
A liquid rolling down chin location
dripping index imitates motion of drip- iconic for action IA
A ping liquid on cheek
earphones thumb and index of both hands iconic for shape of object, IS, BL
O move down body from ears placed on body location
eye makeup index finger strokes horizontally iconic for action, placed on IA, BL
O across eyelid body location
fake-sneeze imitates sound and motion of iconic for action IA
A sneezing
fake-tooth taps upper or lower rear tooth body location BL
O with index
fang tap lower canine teeth with iconic for shape of object, IS, BL
(Halloween toy) hooked index fingers placed on body location
O thumb and index of both hands iconic for shape of object, IS, BL
filmers, reporters move down body where camera placed on body location
O straps are located
frown lower lip pulled down over chin iconic for shape, placed on IS, BL
O with fingers body location
glasses thumb and index pinch at iconic for shape of object, IS, BL
O temples placed on body location
grate imitating motion of grating a iconic for action IA
A vegetable; fist moves across
palm of other hand
hair bow index and thumb of both hands iconic for shape of object, IS, BL
O placed on head placed on body location
inhale index from mouth down to iconic for internal path of IA, BL
A stomach an action in body
kiss-hand kiss on hand iconic for action IA
A
long hair index fingers trace hairline from iconic for shape of object, IS, BL
O ears to below shoulder placed on body location
man, male (foot) taps bottom of foot with index unknown U
O
nail file tip of bent index moves back and iconic for action, placed on IA, BL
O forth across finger of other hand body location

note (something moves index horizontally across unknown U

in environment) lips before pointing to some-
D thing
obnoxious knock sharply on wall or floor cross-modal transfer from CMT
QUALITY English sound “nox” in
obnoxious
pickle thumb and index extended from outlining shape of object IS
O both fists held in space in front
of body
poke jab with index iconic for action IA
A
poke-stomach poke stomach with index iconic for action on body IA, BL
A location
puppet open hand moves down over fist iconic for action (putting IA, BL
O of other hand hand puppet over hand),
placed on body location
runny nose index traces path of liquid run- iconic for action IA, BL
O ning from nose
scarf palms of open hands down sides iconic for shape, body IS, BL
O of head location
scraper fingers of open hand make scrap- iconic for action IA
O ing motion across other hand
sip tips of index and thumb touch iconic for action, body IA, BL
A lips location
smooth smoothing motion of open palms iconic for action IA
QUALITY up legs
stethoscope index fingers in ears iconic for shape, body IS, BL
O location
strangle hands grasp neck iconic for action, on body IA, BL
A location
thermometer puts extended index finger under iconic for shape, on body IS, BL
O arm location
tickle index makes tickling motion iconic for action, on body IA, BL
A under arm location
turn-around open hand brought around from iconic for action IA, BLO
A one side of waist to other on
other’s body
unattention palms of both open hands placed functional action FA
STATE over face

under-eye index moved horizontally iconic for action, on body IA, BL

makeup under eye location
O
unlisten palms cover ears functional action FA
STATE
Viewmaster one hand open palm like compound sign at body location BL, IS
O mask, other hand thumb and
index at eye like camera
walk-up-my-back in seated position, hands iconic for action, on body IA, BL
A placed behind back, palms location
up, and bounced
walk-up-my- arm with open hand swings iconic for action, on body IA, BL
bottom under body between legs location
A
woman (lip) rubs index horizontally back iconic for action (applying lip- IA, BLO
O and forth across lips stick) on body location
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The Kids Are Alright: Maternal Behavioral
Interactions and Stress Reactivity in Infants of
Differentially Reared Rhesus Monkeys
Peter G. Roma
American University
Angela M. Ruggiero
National Institute of Child Health and Human Development
Melanie L. Schwandt and J. Dee Higley

National Institute on Alcohol Abuse and Alcoholism
Stephen J. Suomi
National Institute of Child Health and Human Development
Abstract: Behavioral interactions and infant stress reactivity were investigated in 120
mother-infant pairs of rhesus monkeys (Macaca mulatta). The mothers themselves were ei-
ther mother-reared (MR), surrogate-peer reared (SPR), or peer-reared (PR). Focal obser-
vations and isolation stress tests were conducted throughout post-natal months 1–6 of the
infants’ lives, followed by a standardized 4-week social separation regimen. PR mothers
engaged in more grooming than MR mothers during months 4 and 6, and more rejections
than both other groups during months 3 and 5. Although all infants were mother-reared,
D 14 and 30 cortisol responses in infants of MR and SPR mothers resembled their mother’s
responses at that age, a pattern that corresponded inversely with levels of mother-infant
mutual ventral contact during month 1. Despite observed differences in maternal behav-
ior and evidence of non-genomic cross-generational transmission of early cortisol reactiv-
ity, infant stress responses throughout later infancy did not vary as a function of the
mother’s rearing condition.
Maternal Behavioral Interactions and Stress Reactivity

in Infants of Differentially Reared Rhesus Monkeys
The impact of early adverse experience on biobehavioral development in humans
and other animals is well documented. Extensive evidence from the human literature
103
104 PETER G. ROMA, ET AL.
indicates heightened vulnerability to psychopathology stemming from early childhood

loss and trauma (e.g., Agid, Kohn, & Lerer, 2000; Heim, Plotsky, & Nemeroff, 2004),
with the resulting alterations in stress physiology exacerbating this and other health
risks (e.g., Christoffel & Forsyth, 1989; Goeders, 2003; Vanitallie, 2002). Analogous
findings have also been observed in correlational and experimental animal models
(e.g., Brake, Zhang, Diorio, Meaney, & Gratton, 2004; McIntosh, Anisman, & Merali,
1999; Sánchez, Ladd, & Plotsky, 2001).
One particular topic that has attracted considerable attention is the effects of early
experience on social development, and in this context, nonhuman primate models
have generated a compelling body of research. In virtually all primate species, includ-
ing humans, some of the most salient early environmental experiences are social in na-
ture, particularly within the domain of the mother-infant relationship. Among the most
poignant demonstrations of this are the classic studies of “motherless-mother” mon-
keys conducted by Harlow and colleagues at the University of Wisconsin Primate
Laboratory (see Ruppenthal, Arling, Harlow, Sackett, & Suomi, 1976 and Suomi &
Ripp, 1983, for thorough reviews). In this work, infant rhesus monkeys (Macaca mu-
latta) were reared for at least the first six months of life devoid of contact with any
conspecifics. When later introduced to socially reared peers, the isolate-reared mon-
keys appeared overwhelmed and typically remained socially inept unless “rehabili-
tated” by interaction with younger monkeys of equal social sophistication. When some
of these isolate-reared females subsequently became mothers (“motherless mothers,”
according to Harlow) most were grossly incompetent and often abusive in caring for
their infants. Somewhat less severe deficits were exhibited by most motherless moth-
ers who had been reared in increasingly complex social environments, such as peer-
only rearing (see Novak & Sackett, 2006).
These studies are often cited as clear examples of how socially impoverished rear-
ing can produce deficits in subsequent maternal care, with devastating cross-genera-
tional results for the infants. However, in their 10-year follow-up survey of motherless
mothers, Ruppenthal et al. (1976) described some remarkable trends underscoring the
robustness of species-appropriate maternal behavior in females reared without a real
monkey mother. The most striking effect was that of parity. Without any human inter-
vention, motherless mothers were well more than twice as likely to provide adequate
care for their second and third infants versus their first, and more than three times as
likely to adequately care for their fourth and fifth infants.
In addition to parity, a number of other variables were also shown to increase the
likelihood of adequate parenting among motherless-mother monkeys, and ever since
then active efforts have been made to integrate these factors into primate nursery-
rearing paradigms (Suomi & Ripp, 1983), including those employed in the Laboratory
of Comparative Ethology (LCE) at the National Institute of Child Health and Human
Development (NICHD). Perhaps the most important variable has been the opportunity
to engage in species-typical social interactions throughout development. At LCE,
mother-reared (MR) infants are reared by their mothers in groups with other adults and
their offspring, an arrangement that provides ample opportunity for relatively normal
biobehavioral development. Nursery-reared infants are either peer-reared (PR) or
surrogate-peer reared (SPR). The former condition is essentially identical to that used
The Kids Are Alright 105
in the Harlow laboratory, where age-matched infants live exclusively with each other
in groups of four. Surrogate-peer rearing involves individual housing with an inani-
mate surrogate, but includes daily socialization sessions with other SPR infants begin-
ning after the first month of life.
Although the original motherless-mother work identified sometimes dramatic rear-
ing effects on maternal behavior, contemporary nursery-rearing conditions have re-
ceived relatively little attention in this regard; moreover, few investigations have ex-
tended analyses of rearing effects to developmental outcomes in the mothers’ infants,
with the obvious exception of the abusive and infanticidal primiparous isolate-reared
mothers. Champoux, Byrne, DeLizio, and Suomi (1992) did show that despite some
differences in rejection rates and social contact, multiparous peer- and isolate-reared
rhesus mothers were largely indistinguishable from their mother-reared counterparts
in most other aspects of their maternal behavior. Also, Sackett, Ruppenthal, and Davis
(2002) recently compared health and reproductive data from nearly 1,200 MR and
over 500 SPR pigtailed macaques (Macaca nemestrina), but found virtually no differ-
ences between rearing conditions in terms of growth, injury, survival probability, or
reproductive success. Taken together, these results suggest that some modern labora-
tory rearing practices may be successful in ensuring infant health in the absence of
care by the biological mother. However, Sackett, Ruppenthal, and Davis’ data did not
specifically address maternal behavior of their differentially reared monkeys, whereas
Champoux, Byrne, DeLizio, and Suomi’s did not include SPR mothers or assess ef-
fects of maternal rearing on any aspect of infant biobehavioral development. The pur-
pose of the present study is to address these issues.
In addition to extensive mother-infant behavioral observations, the LCE research
program investigating biobehavioral development in rhesus monkeys is unique be-
cause it includes standardized longitudinal assessments of stress reactivity throughout
infancy, namely activation of the hypothalamic-pituitary-adrenal (HPA) axis in re-
sponse to psychosocial stressors. This combination provides numerous opportunities
to assess early environmental influences on biobehavioral development across gener-
ations. As such, the specific goals for the present study were to determine 1) if and
how contemporary laboratory rearing affects subsequent mother-infant behavioral in-
teractions, 2) if and how a mother’s own rearing history influences her infant’s HPA
axis reactivity, and 3) if direct relationships exist between individual differences in
maternal care and infant stress reactivity within groups of differentially reared rhesus
monkey mothers.
Method
Subjects
Data were analyzed from a total of 120 mother-infant pairs of rhesus monkeys
(Macaca mulatta) collected over eight consecutive birth-year cohorts; the infant sub-
ject pool was composed of 74 males and 46 females. All mothers and their infants were
group housed in combined indoor-outdoor pens with another 6–8 adult females from
the same cohort as each other and with their infants from the same cohort as each other.
Each group also included two adult males who sired their respective group’s infants.
All animals had ad libitum access to water and monkey chow with regular supplements
of fresh fruit and grains. All procedures described in this report were in compliance
with the Animal Welfare Act (1966) and Public Health Service Policy, and all proto-
cols were approved by the NICHD and NIAAA Animal Care and Use Committees.
Mothers’ Rearing Conditions

All of the infants included in this study were reared by their mothers (biological or
adoptive); however, the mothers themselves were reared as infants under one of three
conditions: Mother-Reared (MR, n = 40), Surrogate-Peer Reared (SPR, n = 20), or
Peer-Reared (PR, n = 18). Each of these rearing conditions was described in detail by
Shannon, Champoux, and Suomi (1998) and is summarized briefly here.
MR mothers were reared in the same conditions as their own infants (described
above). The SPR and PR females were removed from their mothers 1–3 days post-par-
tum and assigned to their respective nursery-rearing groups. All nursery-reared infants
were housed in clear plastic cages with constant access to a polypropylene surrogate
outfitted with a heating pad and covered with fleece cloth until post-natal day 15. On
day 15, each individual infant was moved with her surrogate (minus the heating pad)
to a larger wire mesh cage.
Nursery-reared infants were assigned to mixed-sex groups of four; when the
youngest group member reached 37 days of age, the SPR infants began regular social-
ization sessions in a separate large play cage. SPR socialization took place each week-
day for two hours, after which the infants were returned to their respective individual
home cages. When the youngest member of a PR group reached 37 days of age, all of
the infants from that group began permanent social housing in a large primate cage.
The SPR infants had access to their surrogates for the duration of their stay in the nurs-
ery while the PR groups’ surrogates were removed when the infants reached 4 months
of age.
At approximately 7 months of age, all subjects were moved into large peer groups,
each containing several MR, PR, and SPR age-mates of both sexes. All of the subjects
remained in these or subsequently reconstituted peer groups until adulthood.
Mother-Infant Behavioral Observations

Although the mothers described in this report were initially reared under system-
atically different conditions, all of their infants included in this study were mother-
reared. In order to assess rearing effects on subsequent maternal care, a subset of be-
haviors from an extensive mother-infant ethogram were analyzed. Each mother-infant
pair was observed twice a week from week 1 to week 24 of the infant’s life. Observa-
tion sessions consisted of a 5-minute focal observation period of the infant followed
immediately by a 5 minute focal observation period of the mother. Observation ses-
sions were conducted by trained observers on various weekdays and at various times
Table 1. Operational Definitions and Scoring Criteria for Mother-Infant Behavioral
Interactions
Behavior Description
Grooming Cleaning/grooming of infant by mother or vice-versa; includes
scratching, biting, licking, or rubbing. Must be scored
simultaneously with either Mutual Ventral or Social Contact.
Recorded as duration (seconds).
Mutual Ventral Infant is belly-to-belly with mother and/or on the nipple. Infant
cannot be in Social Contact with any other animal or engage in
locomotion, but mother can. Recorded as duration (seconds).
Social Contact Sitting, standing, locomoting, or lying within arms reach of mother
or infant, depending on which is the focal animal. Social Contact is
superseded by Mutual Ventral. Recorded as duration (seconds).
Reject/Withdrawal Mother or infant rejects approaches made by the other for mutual
ventral contact. Also scored if there is mutual ventral contact and one
of the animals attempts to break but the other does not want to.
Recorded as frequency (number of occurrences).
between 0900 hr and 1600 hr. The behaviors of interest for our study were: Grooming
between mother and infant, Mutual Ventral contact between mother and infant, Social
Contact between mother and infant, and Reject/Withdrawal between mother and in-
fant. The operational definitions and scoring criteria for these behaviors are outlined
in Table 1 (the entire mother-infant ethogram is available upon request).
Infant Stress Reactivity

Blood samples were obtained from each infant via femoral venipuncture on day
(D) 14 and 30 and month (M) 2, M3, M4, and M5 of life. In all cases, the infants were
hand-caught from their home groups. The D14 and D30 samples were obtained after
the infants underwent a 30-minute neurobehavioral assessment that required handling,
restraint, and gentle physical manipulation by a human experimenter (Schneider,
Champoux, & Moore, 2006). The M2 samples were taken immediately after the in-
fants were retrieved from their groups, and served as a relative baseline. The M3, M4,
and M5 samples were obtained after a 30-minute period where each infant was iso-
lated in a wire cage in a room out of tactile, visual, and auditory contact with all other
animals and experimenters. Since blood sampling coincided with cerebrospinal fluid
(CSF) sampling (blood was obtained before CSF), the infants were anesthetized with
ketamine hydrochloride (10 mg/kg, IM) before any samples were taken.
Between months 6 and 8 of age, each infant underwent a 4-week social separation
regimen. On D1 of this procedure, mother-infant pairs were hand-caught, physically
separated from each other, and blood samples were taken immediately from the infants
(baseline). Each infant was then individually held in a quadrant of a large primate cage
along with three other maternally-separated infants with whom they shared auditory
and olfactory, but limited visual and no tactile contact. At one hour post-separation,
each infant was removed from its holding cage and another blood sample was taken
(H1); after this sampling, the infants were returned to their respective holding cages.
Finally, a third blood sample was taken two hours post-separation (H2) in the same
fashion as the H1 sampling. The Baseline, H1, and H2 blood samples were taken while
the monkeys were fully awake, and provided the opportunity to assess acute stress ef-
fects on HPA axis activity. Following the H2 sampling, the infants were returned to
their holding cages where they remained for three days. On day 4, each infant was
anesthetized (15 mg/kg ketamine, IM) followed by blood and CSF sampling (H96); the
H96 sampling provided the opportunity to assess the impact of a chronic stressor on
HPA axis output. On D5, the infants were reunited with their mothers in their respec-
tive home groups, where they remained for three days. Following the 3-day reunion
period, the 4-day separation and 3-day reunion sequence was repeated until a total of
four full cycles was completed over the course of 28 days.
All blood samples were kept on ice until centrifugation (within three hours after
extraction), after which the plasma was transferred to cyrotubes and immediately
flash-frozen in liquid nitrogen. Samples were then stored in a –80° C freezer until
shipped for assay. Levels of plasma adrenocorticotropic hormone (ACTH) and total
cortisol were determined via radioimmunoassay by a commercial assay facility; inter-
and intra-assay coefficients of variation were ≤ 10%. ACTH values were expressed in
picograms per milliliter (pg/ml) and cortisol values were expressed in micrograms per
deciliter (µg/dl).
Data Analyses
Most of the infants studied were reared by multiparous mothers over successive
years; specifically, the 120 infant subjects were reared by 78 different mothers. Of the
120 infants, a total of 57 (47.5%) were reared by primiparous mothers, whereas a total
of 75 infants (62.5%) were reared by females who were or would later become multi-
parous. Maternal parity notwithstanding, the data from each mother-infant pair were
considered independent of each other; therefore, each dyad was treated as an inde-
pendent case for analyses. Data were analyzed using Analyses of Variance (ANOVA),
paired-samples t-tests, planned least-significant difference (LSD) between-groups
comparisons, and Pearson product-moment correlations as described in detail below.
Statistical significance was set at α = .05 for all analyses (2-tailed when applicable).
Mother-Infant Behavioral Interactions

Since all of the behaviors analyzed involved interaction between mother and infant,
and both members of each mother-infant pair were observed in immediate succession,
the values for each behavior at each week were the sum of the combined 10-minute
mother-infant scoring episode. The behavioral data were analyzed by post-natal month
of the infant’s life, with the mean value per session during weeks 1–4 serving as the
single data point for month 1, followed by the mean of weeks 5–8 representing M2,
weeks 9–12 for M3, weeks 13–16 for M4, weeks 17–20 for M5, and weeks 21–24 for
M6. Each behavior was analyzed via 3 × 6 mixed ANOVA with a between-groups fac-
tor of Mother’s Rearing (MR, SPR, or PR) and a within-group factor of Infant’s Age
(1, 2, 3, 4, 5, and 6 months). Main effects of age were followed by paired-samples
t-tests comparing overall means of consecutive months. All ANOVAs were then fol-
lowed by planned LSD comparisons at each month to identify differences in maternal
behavior as a function of how the mothers were reared.

Separate one-way ANOVAs with a between-groups factor of Mother’s Rearing
were performed on the ACTH and cortisol values at D14, D30, M2, M3, M4, and M5.
All ANOVAs were followed by planned LSD comparisons. For the social separations,
the average of each infant’s ACTH and cortisol during Baseline, H1, H2, and H96
across all four separation cycles served as the data points for analyses (cf. Barr, New-
man, Shannon, Parker, Dvoskin, & Becker, 2004). The ACTH and cortisol data were
each analyzed via 3 × 4 mixed ANOVA with a between-groups factor of Mother’s
Rearing and a within-group factor of Phase of separation procedure (Baseline, H1, H2,
and H96). Main effects of Phase were followed by paired-samples t-tests comparing
overall means of consecutive phases. Both ANOVAs were then followed by planned
LSD comparisons at each phase.
Individual Differences
A number of studies from the animal literature have demonstrated clear relation-
ships between individual differences in early maternal behavior and subsequent stress
reactivity in offspring. The best known and most widely reproduced relationship is the
negative one between licking/grooming behavior in rat dams (Rattus norvegicus) and
subsequent neuroendocrine responses to stress in their pups (see Meaney, 2001). How-
ever, individual differences in maternal care among nonhuman primates are regularly
observed (Fairbanks, 1996; Maestripieri, Lindell, Ayala, Gold, & Higley, 2005), and
in order to determine if analogous relationships existed in differentially-reared rhesus
monkey mothers and their infants, a series of correlational analyses was conducted via
Pearson product-moment correlations. Specifically, mean mother-infant grooming be-
havior during each month of each infant’s life was plotted against the infants’ corre-
sponding ACTH and cortisol values for that month. Also, to assess whether early ma-
ternal care can predict stress reactivity in later infancy, month 1 grooming behavior
was correlated with mean ACTH and cortisol responses to each phase of the separa-
tion procedure. All of the above mentioned correlational analyses were performed sep-
arately for infants of MR, SPR, and PR mothers.
Results
Mother-Infant Behavioral Interactions

No significant main or interaction effects were produced by the grooming ANOVA
(Fs < .376, ps > .222); however, the planned LSD comparisons showed the PR mother-
infant pairs engaging in significantly more grooming behavior than the MR group dur-
ing months 4 and 6 (ps < .044).
The Mutual Ventral ANOVA only yielded significant main effects of Infant’s Age
and Mother’s Rearing (Fs > 3.375, ps < .039). Paired-samples t-tests revealed signifi-
cant overall decreases in Mutual Ventral from months 1–2 and 2-3 (ts > 7.000, ps <
.001), but no differences after M3 (absolute ts < .825, ps > .410). LSD comparisons re-
vealed that the SPR mother-infant pairs spent more time in mutual ventral contact ver-
sus the MR group during M1 and versus the MR and PR groups during M4 (ps < .019).
The only significant term in the Social Contact ANOVA was Infant’s Age
(F(5,535) = 23.317, p < .0000000001; all other Fs < .801, ps > .630). Paired-samples
t-tests revealed a significant overall increase from M1–2 (t(119) = –10.455, p < .001),
but no differences after M2 (absolute ts < 1.276, ps > .060). LSD comparisons showed
no between-groups differences in Social Contact during any month.
As with Social Contact, the only significant term in the Rejections ANOVA was
Infant’s Age (F(5,545) = 7.177, p < .000002; all other Fs < 1.681, ps > .104). Paired-
samples t-tests revealed significant overall increases from M2-M3 and M3-M4
(absolute t(199)s > 2.017, ps < .047), but no differences between M1-M2 or after M4
(absolute ts < 1.455, ps > .148). However, LSD comparisons showed that the PR
mother-infant pairs engaged in more rejections than both the MR and SPR groups dur-
ing months 3 and 5 (ps < .029). These and all other mother-infant behavioral interac-
tions and group comparisons are summarized in Figure 1.

The one-way ANOVAs for ACTH produced no significant main effects of
Mother’s Rearing at D14, D30, M2, M3, M4, or M5 (Fs < 1.675, ps > .191); these
findings were confirmed by the planned LSD comparisons (ps > .078). However, sim-
ilar analyses of cortisol yielded a significant main effect at D14 (F(2,108) = 4.909,
p = .009) and a trend at D30 (F(2,108) = 2.371, p = .098), but no effects at any other
time point (Fs < 2.242, ps > .110). As illustrated in Figure 2, LSD comparisons
showed that the infants of SPR mothers had significantly lower cortisol output versus
infants of MR and PR mothers on D14 and versus infants of MR mothers on D30
(ps < .030; SPR vs. PR at D30 p = .059).
The mixed ANOVA on ACTH during the separation regimen generated only a sig-
nificant main effect of Phase (F(3,345) = 136.823, p < .0000000001; all other Fs <
1.764, ps > .122). Paired-samples t-tests revealed a significant overall increase in
ACTH output from Baseline-H1, and decreases from H1-H2 and from H2-H96;
H96 was also significantly lower than Baseline (absolute ts > 4.334, ps < .001). LSD
Grooming Mutual Ventral
* 300 *
28 *
25 250
22 *#
19 200
16
150
(mean secs + SEM)

(mean secs + SEM)
13
Time Spent per Session

10 100
1 2 3 4 5 6 1 2 3 4 5 6
Social Contact Rejections

*†
50 0.6 *†
0.5
40
0.4
30 0.3
0.2
(mean + SEM)
20
The Kids Are Alright
0.1
(mean secs + SEM)

Number per Session

10 0.0
1 2 3 4 5 6 1 2 3 4 5 6
Infants’ Age in Months

Mother’s Rearing Condition
Mother-Reared Surrogate-Peer Reared Peer-Reared
FIGURE 1. Mother-infant behavioral interactions as a function of mother’s rearing condition. Overall mean levels of Grooming did not
vary as a function of infant’s age; however, Mutual Ventral significantly decreased from M1-M2 and M2-M3, Social Contact increased
from M1-M2, and Rejections increased from M2-M3 and M3-M4. Each MR, SPR, and PR bar represents the respective mean of 56–57,
23, and 31–32 mother-infant pairs. Within each month, significant difference versus the MR group is indicated by *, significant differ-
111
ence versus the SPR group is indicated by †, and significant difference versus the PR group is indicated by #.
Infants’ ACTH
450
370
Mean pg/ml + SEM
290
210
130
50
D14 D30 M2 (Baseline) M3 M4 M5
Infants’ Cortisol
60
†
†
52 †
Mean µg/dl + SEM
44
36
*
28
20
D14 D20 M2 (Baseline) M3 M4 M5
Infants’ Age in Months

FIGURE 2. Physiological stress reactivity across infancy as a function of mother’s

rearing condition. The top panel represents mean plasma ACTH values, the bottom
panel represents mean plasma cortisol values. The D14 and D30 samples were taken
after an experimenter-administered 30-minute neurobehavioral assessment, the M2
Baseline sample was taken immediately after capture, and the M3, M4, and M5 sam-
ples were taken after a 20-minute isolation stress challenge. Each MR, SPR, and PR
bar represents the respective mean of 56–62, 23–26, and 29–32 infants. Within each
time point, significant difference versus the MR group is indicated by *, significant
difference versus the SPR group is indicated by †, and significant difference versus the
PR group is indicated by #.
comparisons showed that the infants of SPR mothers had significantly lower ACTH
versus infants of MR mothers at H2 only (p = .016; other ps > .054).
The mixed ANOVA of separation-induced cortisol also only yielded a significant
main effect of Phase (F(3,351) = 555.648, p < .0000000001; all other Fs < .706, ps >
.645). Paired-samples t-tests revealed significant increases from Baseline-H1 and H1-
H2 as well as a significant decrease from H2-H96; H96 was also significantly higher
than Baseline (absolute ts > 5.631, ps < .001). LSD comparisons revealed no between-
groups differences in cortisol output at any phase of the separation procedure (ps >
.232). The results of the separation analyses are depicted in Figure 3.
Individual Differences
The results of the correlational analyses are summarized in Tables 2 and 3. Monthly
grooming rates were generally not associated with infant HPA axis activity at each
month; however, grooming during the first month of life was positively correlated with
D30 cortisol output among infants of MR females (r (59) = .530, p = .000016) and neg-
atively correlated with D30 ACTH output among infants of PR females (r (29) = –.491,
p = .007; all other absolute rs < .305, ps > .138). A dissociation between grooming dur-
ing the 1st month of life and infants’ subsequent responses to separation stress was also
observed, except for a modest but significant positive relationship with H2 ACTH lev-
els among the infants of SPR mothers (r (26) = .444, p = .023; all other rs < .317, ps
> .077). The statistically significant relationships between maternal care and infant
stress reactivity are presented in Figure 4.
Discussion
The purpose of this study was to explore the influence of contemporary laboratory
rearing conditions on maternal behavior in adult rhesus monkeys and to determine
how rearing effects may impact biobehavioral development in these mothers’ infants.
Given the fairly comprehensive collection of variables and the relatively large sample
size, perhaps the most striking result was the general lack of differences in maternal
behavior or infant stress reactivity as a function of maternal rearing condition. Espe-
cially in light of the original motherless-monkey work and more recent investigations
of potentially detrimental effects of nursery rearing (e.g., Barr et al., 2004; Bastian,
Sponberg, Suomi, & Higley, 2003; Higley, Suomi, & Linnoila, 1992), it is somewhat
surprising that even the mother-reared mothers failed to emerge as superior caretak-
ers, if not producers of infants with superior coping skills.
The behavioral data showed that all three groups of mothers engaged in generally
species-normative patterns of interaction with their infants, exhibiting high levels of
mutual ventral contact in early infancy, giving way to increasing levels of social con-
tact, and culminating in increased rejections as weaning approached. The most patent
deviation from the overall pattern among these behaviors was in the PR mothers’ ten-
dency to reject their 3–5-month old infants with a frequency reserved by the other two
Infants’ ACTH
400
330
Mean pg/ml + SEM
†
260
190
120
50
Baseline Hr 1 Hr 2 Hr 96
Infants’ Cortisol
80
70
Mean µg/dl + SEM
60
50
40
30
Baseline Hr 1 Hr 2 Hr 96
Phase of Separation
FIGURE 3. Infants’ physiological stress reactivity to a social separation procedure as

a function of mother’s rearing condition. The top panel represents mean plasma ACTH
values while the bottom panel represents mean plasma cortisol values from blood
sampled immediately after capture (Baseline) and 1, 2, and 96 hours post-separation.
Each MR, SPR, and PR bar represents the respective mean of 56–62, 23–26, and 29–
32 infants. Within each time point, significant difference versus the MR group is indi-
cated by *, significant difference versus the SPR group is indicated by †, and signifi-
cant difference versus the PR group is indicated by #.
Table 2. Correlations between mother-infant grooming and infant monthly HPA axis
responses.
Infants’ HPA Axis Responses at Corresponding Month of Life
Infants of Infants of Infants of
Grooming
MR Mothers SPR Mothers PR Mothers
During Infants’
Month of Life ACTH Cortisol ACTH Cortisol ACTH Cortisol
1 .023 .530*** –.041 .129 –.491** .164
2 (Baseline) –.207 .001 .304 .091 –.124 –.157
3 –.146 –.022 .002 .144 –.252 .138
4 –.080 .211 .065 –.174 .291 –.024
5 –.105 .148 –.081 .179 .291 .093
Note: Each value represents Pearson r correlation coefficient. Significant correlations are in bold: **p = .007,
***p = .000016.
Table 3. Relationships between M1 grooming and infant HPA axis responses to separation
stress.
Relationship with M1 Grooming
Infants of Infants of Infants of
Phase of
MR Mothers SPR Mothers PR Mothers
Separation
Procedure ACTH Cortisol ACTH Cortisol ACTH Cortisol
Baseline .089 .119 .046 –.044 .182 .316
Hour 1 .123 .177 .266 .098 .143 .307
Hour 2 .048 .013 .444* .294 .172 .243
Hour 96 –.050 .126 –.023 .255 –.070 .277
Note: Each value represents Pearson r correlation coefficient. Significant correlation is bolded (p = .023).
groups for month 6. However, and somewhat paradoxically, the PR mothers also en-
gaged in more grooming behavior than their MR counterparts during the latter half of
their infants’ rearing. It is uncertain why this pattern appeared—one possibility is that
the PR monkeys’ propensity for physical contact could have provoked more rejection
responses from their MR infants as the infants grew increasingly independent—but
perhaps a more relevant question than “why?” is “did it matter?”, and at least in terms
of infant stress reactivity, our physiological data suggest that it did not.
The HPA axis data were concordant with the behavioral data in that no one group
of infants appeared particularly well- or ill-suited to cope with the isolation and sepa-
ration stress challenges. The infants of PR mothers did not differ from their MR or
SPR counterparts in HPA axis reactivity during the later months when PR mothers re-
jected their infants more frequently. In fact, infants of PR mothers involved in rela-
tively high levels of grooming during the first month of life showed relatively low
ACTH levels that month, whereas infants of high-grooming MR mothers actually
showed increased cortisol levels (see Figure 4). The former result echoes the rodent
literature if one assumes linear causality between maternal grooming and infant HPA
Individual Differences in Maternal Care and Infant Stress Reactivity

Infants’ Day 30 ACTH
Mother-Reared Mothers
1050
900
750
600
450
300
150
r (56) = .023, ns
0
0 20 40 60 80
Surrogate-Peer Reared Mothers
600
500
400
300
200
100
r (23) = .041, ns
0
0 10 20 30 40 50 60 70
Peer-Reared Mothers
900
800
700
600
500
400
300
200
r (29) = .491, p = .007
100
0
0 20 40 60 80 100 120
Mean Grooming per Session During Infants’ 1st Month of Life
FIGURE 4. Individual differences in maternal care and infant stress reactivity. Indi-
vidual differences in mother-infant Grooming during the infant’s first month of life
served as the predictor variable for these graphs. Each column of graphs corresponds
to a different outcome variable among the infants of MR (●, n = 56–62), SPR (▲, n =
23–26), or PR (■, n = 29–32) mothers, respectively. Statistically significant correla-
tions within any combination of outcome variable and mother’s rearing condition are
indicated by an underlined graph title.

Infants’ Day 30 Cortisol
100
80
60
40
r (59) = .530, p = .000016

20
0 20 40 60 80

80
60
40
r (23) = .129, ns
20
0 20 40 60 80
Peer-Reared Mothers
80
70
60
50
40
r (29) = .396, ns
30
0 20 40 60 80 100 120
FIGURE 4. (Continued)

Infants’ Hr 2 ACTH During Separations
700
600
500
400
300
200
100 r (62) = .048, ns
0
0 20 40 60 80

400
300
200
100
r (26) = .444, p = .023

0
0 20 40 60 80
Peer-Reared Mothers
400
300
200
100
r (32) = .172, ns
0
0 20 40 60 80
FIGURE 4. (Continued)
axis reactivity (cf. Francis, Diorio, Liu, & Meaney, 1999); however, the latter result is
less readily explained, unless already high-reactive infants of MR mothers tended to
elicit more maternal grooming than their low-reactive peers (cf. Stern, 1997). This in-
terpretation is difficult to verify with our existing dataset, but seems reasonable given
the fact that infants of MR and PR mothers did not actually differ at the group level in
their mean D14 or D30 HPA measures.
In addition to the early grooming correlations, perhaps the most intriguing result
of the HPA analyses was the relationship between infants of MR and SPR mothers at
the D14 and D30 samplings. In their 1998 study employing the same procedures as
those we used, Shannon et al. reported significantly higher cortisol values in MR ver-
sus nursery-reared infants that were virtually identical (within 5 µg/dl) to those seen
in our infants of MR and SPR mothers (see their Figure 1 and our Figure 2 bottom
panel). The critical point here is that all of the infants in our study were mother-reared,
yet the infants of MR and SPR mothers exhibited cortisol patterns resembling those
produced by their mothers’ rearing conditions.
Since the patterns of early cortisol reactivity Shannon et al. reported were pro-
duced by the rearing conditions to which the monkeys were assigned, they cannot be
primarily attributed to genetic factors. To account for their findings, Shannon et al. ar-
gued quite sensibly that MR infants were not only subjected to the stress of the neona-
tal assessment procedure, but to the stress of capture and maternal separation, whereas
the nursery-reared infants were more acclimated to human handling and did not expe-
rience disruptive capture and separation. However, the infants in our study were all as-
signed to the same mother-reared environment, so there were no differences in proce-
dure that could account for our findings. Nonetheless, the pattern of early cortisol
reactivity in infants of SPR mothers was still identical to their own mothers and dif-
ferent from the infants of MR mothers. Taken together, these results suggest a cross-
generational transmission of early stress reactivity, but by different non-genomic
means for both acquisition in SPR mother and transmission to her MR infant.
The patterns of early stress reactivity in MR and SPR mothers can be explained by
their own differential rearing, but the identical patterns seen in their mother-reared in-
fants cannot. This point coupled with the fact that the first month of a rhesus infant’s
life is spent almost exclusively on or in very close proximity to mother leaves mater-
nal behavior as the most likely means of cross-generational transmission. Although
mother-infant grooming behavior did not vary as a function of mother’s rearing, the
SPR mothers did engage in more mutual ventral contact with their infants during the
first month of life compared to their MR and PR counterparts—a pattern that corre-
sponds inversely with the D14 and D30 cortisol data. More conclusive verification of
this relationship would, of course, require further study, but as conceptually intriguing
as these findings might be, there still remains the issue of functional consequences. As
with the behavioral tendencies produced by the mothers’ differential rearing, the ap-
parent cross-generational alterations in their infants’ early HPA axis regulation were
inconsequential when challenged later in infancy.
So overall, what can we conclude about modern laboratory-rearing effects on ma-
ternal behavior and infant stress reactivity in rhesus monkeys? Generally, it appears
that the mother-rearing, surrogate-peer rearing, and peer-rearing conditions utilized
at LCE do not produce aberrant patterns of maternal care in socially-housed adult

females, or enduring effects on stress reactivity in their offspring. Whether or not this
news is surprising, it is certainly welcome, especially to those with more than a prin-
cipled interest in nonhuman primate health and well-being. This conclusion is all the
more persuasive considering the purposely liberal statistical approach used to analyze
the data. That is, the planned comparisons all sought the least significant difference
between means; however, none of the ANOVAs actually yielded significant interac-
tion terms involving Mother’s Rearing. Moreover, the only ANOVAs with significant
main effects of Mother’s Rearing that would have warranted unplanned post-hoc com-
parisons were Mutual Ventral and D14 cortisol, and of those analyses the only differ-
ences to survive even Tukey type I error correction are the SPR mothers engaging in
more mutual ventral than MR at M1 and both other groups at M4, as well as infants
of MR mothers producing higher D14 cortisol than infants of SPR mothers.
Although our data indicate reproductively successful outcomes in differentially
reared monkey mothers and relatively normal development in their infants, it is impor-
tant to note that these data do not suggest that nursery-rearing is superior to mother-
rearing. Among other reasons, the use of nursery-reared monkeys continues to prove
valuable for the study of development as well as gene-environment interaction effects
on behavior and physiology (Barr, Newman, Becker, Parker, Champoux, & Lesch,
2003). However, nursery-rearing got its start and is still often employed as a model of
early-life stress through compromised attachment relationships and unguided early so-
cialization. Although the days of isolate rearing have long since passed, compared to
mother-rearing, even modern nursery-rearing has been shown to produce deficits in
central nervous system function and HPA axis regulation (Higley, Suomi, & Linnoila,
1992), as well as increasing adult risk of low social dominance, aggressive behavior,
and excessive alcohol consumption (Bastian et al., 2003; Higley, Hasert, Suomi, &
Linnoila, 1991; Newman et al., 2005). However, like Harlow’s motherless-mother
studies from so many years ago, what our study of rhesus monkey mothers demon-
strated is that despite the potential risks conferred by contemporary nursery-rearing in
other biobehavioral domains, a stable, species-appropriate social environment may fa-
cilitate competent reproductive and maternal function—arguably the most important
constellation of behaviors for any animal—with no apparent detrimental long-term
consequences for the infants, at least over their first six months of life.
Indeed, it is a rather complex process to determine if laboratory rearing conditions
affect later maternal behavioral interactions and if, in turn, maternal behavior in dif-
ferentially reared animals affects their infants’ biobehavioral responses to stress. Nev-
ertheless, in the case of mother-reared, surrogate-peer-reared, and peer-reared rhesus
monkey mothers, we can take comfort in the simple fact that normal maternal behav-
ior appears to be surprisingly resilient, and that ultimately, the kids are alright.
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Author Note
We are grateful to Courtney Shannon, Stephen Lindell, and our many other col-
leagues and friends for their tireless efforts in data collection and management, veteri-
nary and animal care, and facilities maintenance throughout the years.
This project was supported by intramural funds from the National Institute of
Child Health and Human Development and the National Institute on Alcohol Abuse
and Alcoholism/National Institutes of Health/Public Health Service/US Department of
Health and Human Services.
Correspondence concerning this article should be addressed to Pete Roma, Depart-
ment of Psychology, American University, 4400 Massachusetts Ave. NW, Washington,
DC 20016. Email: PeteRoma@gmail.com.
The Literacy of Interaction:
Are Infants and Young Children Receiving a
“Mental Diet” Conducive for Future Learning?
Pnina S. Klein
School of Education
Bar-Ilan University
Ramat-Gan, Israel
Abstract: There is a plethora of research on environmental effects on the development of

infants and young children, and a general consensus regarding several basic requirements
for quality of early education and care. However, there are still many questions that re-
main relatively unanswered, particularly in relation to parental teaching behavior, which
is one of the major objectives of adult-child interactions. Three main types of such ques-
tions are as follows:
1. What are the specific processes within adults’ teaching (mediation) behavior in in-
teractions with young children that may have an effect on their potential to learn
from new experiences?
2. How do these processes affect children’s flexibility of mind (readiness to learn)?
3. What are the differential expressions and potential effects of these components on
children with special needs and with populations of children and families in dif-
ferent cultures?
Possible answers to these questions are suggested in this paper from the theoretical
perspective of a developmental mediation approach, focusing on the quality of adult-child
interaction and on ways to understand and enhance it. Implications for early education
policy are discussed in light of current research.
Are Infants and Young Children Receiving a

“Mental Diet” Conducive for Future Learning?
One of the central challenges of education in the 21st century is to prepare children
to live in a rapidly changing world, requiring constant adjustment and flexibility of
mind. The latter may be defined as the capacity to benefit from new learning experi-
ences, or as readiness to learn. There is a general consensus, based on extensive re-
search documentation, that adult-child interactions are of central importance and that
quality care of young children should consist of a mental diet including warmth, nur-
turance, and stability (for example, see the review by Shonkoff & Phillips, 2000). This
123
124 PNINA S. KLEIN
generalization can be made despite marked heterogeneity of children, their families

and the education and care service they receive. In light of all the latter, it seems
highly important to focus on variables that represent the quality of that interaction in-
cluding variables of adults’ teaching behavior (mediation), which constitute a univer-
sal major component of adult-child interactions. Despite the consensus in child devel-
opment literature regarding the important role played by adult-child interactions,
research on adults’ teaching behavior in interactions with young children is still
scarce.
This paper focuses on adult-child interactions, particularly on adults’ teaching be-
havior in their interactions with very young children and on the potential effects of
these behaviors on children’s readiness to learn. There is a theory-based model and
research supporting the assumption of causal relationships between certain types of
behavior or characteristics of adult-child interaction that affect children’s social-
emotional and cognitive behavior and that create learning experiences that are poten-
tially contributive to children’s flexibility of mind (Feurstein, 1980; Vygotzky, 1978).
The role of these factors has been studied in various cultures and with different pop-
ulations of children and families with special needs (Klein, Wieder, & Greenspan,
1987, Klein, 1996; Klein & Alony, 1993; Klein, 2001b; Klein & Rye, 2004; Chis-
wanda, 1997). In these studies, mediational behaviors of parents (teachers or other
adults) were defined, and their frequency and manner or style of appearance were
identified. The identified mediational behaviors were found to be significantly related
to children’s learning processes and consequently to their cognitive and social-
emotional behavior (Feuerstein, 1979, 1980; Tzuriel, 1999; Klein, 1996; Klein, Feld-
man, & Zarur, 2003; Klein & Rye, 2004). This effect was explained as a consequence
of changes occurring in children’s need systems, including, for example, the need to
focus and perceive things clearly; the need to investigate things and to ask questions;
to make associations between things; to compare and contrast; to complete a task or
an action; to please others; to succeed at an objective; and to organize and to plan ac-
tivities. How does such a need system develop?
From Theory to Research and Practical Implications

There is a theoretical base (Feuerstein, 1979, 1980) and empirical data (Klein,
Wieder, & Greenspan, 1987; Klein, 1988, 1991; Tzuriel, 1999) suggesting that spe-
cific characteristics of adult interaction with children constitute mediational behavior
and may affect children’s predisposition to learn from new experiences. Mediated
learning, as distinct from direct learning through the senses, occurs when the environ-
ment is interpreted for the child by another person who understands the child’s needs,
interests, and capacities, and who takes an active role in making components of that
environment, as well as past and future experiences, compatible with the child. Medi-
ation affects the individual’s present learning and may improve his or her opportunity
to learn from future experiences.
The Literacy of Interaction 125
Elements of Mediation
Basic elements of what constitutes a teaching mediational interaction between a care-
giver and a young child have been identified (Feuerstein, 1979, 1980). The most salient
of these factors are empirically defined (Klein, Raziel, Brish, & Birenbaum, 1987; Klein,
Wieder, & Greenspan, 1987; Klein, 1988, 1991) and are presented in Table 1.
It was found that the factors of quality mediation predicted cognitive outcome
measures up to four years of age better than the children’s own cognitive test scores
in infancy, or other presage variables related to pregnancy, birth histories, and moth-
ers’ education (Klein, Wieder, et al. 1987). Similar findings were reported for a sam-
ple of very low birth weight infants (Klein, Raziel et al. 1987).
Intercorrelations between mothers’ mediational behaviors over time (when their
children were 6, 12, 24, and 36 months old), were moderate to high. The average in-
terjudge reliability for assessing these behaviors was considerably high in studies of
American families of low socioeconomic status (Klein, Wieder et al. 1987) and Israeli
mother-infant samples (Klein & Alony, 1993).
Similar studies were carried out in Ethiopia, Sri Lanka, Indonesia, USA, Sweden,
and Israel (Klein, 1996). A study designed to examine the sustained effects of modi-
fying the mother-infant mediational interaction on infants’ cognitive test performance
and behavior was carried out in Israel. This study will be referred to as the Israeli
follow-up study.
The research design of the Israeli follow-up study included random assignment to
the experimental and control groups; an observational assessment of maternal media-
tion; a baseline assessment of the infants’ developmental status, using Bayley’s Men-
tal Development Scales, prior to training mothers in mediational strategies; and a
follow-up evaluation of experimental versus control mothers and children one year
and three years after the termination of training.
The total study sample consisted of 68 families in a small, low income status urban
community in Israel, who were randomly assigned to an experimental and control
group. This community was singled out for intervention by the Ministry of Education
and the Office of Welfare due to the high proportion of children who had poor school-
readiness skills and a significant high school dropout rate.
Activities developed for the experimental group were based on the Mediational In-
tervention for Sensitizing Caregivers (MISC) process, which is described in detail
later in this article. These activities were designed to improve mothers’ mediation to
their children. The level of mediation was defined by the frequency of appearance, se-
quence and synchrony of maternal mediating behaviors, and their children’s respon-
siveness. Mothers were trained at home by paraprofessional “mediators” and super-
vised by professional developmental psychologists. Mothers were actually helped to
“read” their interactions with their children, to understand their own behavior and their
children’s responses, as well as the potential consequences of these interactions.
Intervention was terminated when mothers improved their mediation and could ver-
bally define the basic components of the parental behaviors targeted by the intervention.
126 PNINA S. KLEIN
Table 1. Definitions and Examples of Basic Criteria of Parental Mediation and Affected Needs
Examples of Social-Emotional
Mediation Processes the Process Intellectual Needs Needs
1. Focusing Making the environmental Need for precision in Need to focus on and
Any act or sequence of stimuli compatible to the perception (vs. scanning decode facial and body
acts of an adult that child’s needs, e.g., bring- exploration). expressions of emotion.
appear to be directed ing closer, covering Need for precision in Need to modify one’s
toward affecting a child’s distractions, repeating, expression. own behavior or the
perception or behavior. sequencing, grouping, environment in order to
These behaviors are helping the child focus, mediate to others (to
considered reciprocal see, hear and feel clearly. make the other person
when the infant or child see or understand).
in the intervention
responds, vocally,
verbally, or nonverbally.
2. Exciting Expressing excitement Need to search for meaningful new experiences

Behavior that expresses vocally, verbally or non- (i.e., listen, look, taste, things that remind one of past
verbal or nonverbal verbally over experiences, experiences).
excitement, appreciation, objects, people, etc.
Need to respond in a way that conveys meaning and
or affect in relation to Naming, identifying. excitement (sound, look and feel excited) and
objects, animals, con-
meaningful activities.
cepts, or values.
3. Expanding Explaining, elaborating, Need to go beyond what Need to think about

Behavior directed toward associating and raising meets the senses. Seek out one’s own feelings and
the expansion of a awareness to metacogni- further information through the feeling of others
child’s cognitive tive aspects of thinking. exploration Need cause and effect
awareness, beyond what Relating past present and Request information from sequences in social
is necessary to satisfy future experiences. other people and from interaction.
the immediate need that other sources.
triggered the interaction. Relating to physical, Need to associate
logical, or social rules and Need to seek between experiences, to
framework. generalizations. recall past information
and anticipate future
Need to link, to associate,
experiences.
to recall past information
and anticipate future
experiences.
4. Encouraging Praise in a way that is Need to seek more success Need to please others
Verbal or nonverbal meaningful to the child. experiences. and gain more mediated
behavior that expresses Clear isolation and identi- Need to summarize one’s feelings of competence.
satisfaction with a child’s fication of the reasons for own activities and deter- Need to identify what
behavior and that identi- success. mine what led to success. pleases different people.
fies a specific component
or components of the Well timed in relation to Need to provide others
child’s behavior which the experience. with mediated feelings
contribute to the experi- of competence.
ence of success.
5. Regulating Behavior Regulation with regard to Need to plan before acting, Need to control one’s
Behaviors that model, speed, precision, force, e.g., need to consider impulses in social
demonstrate, and/or ver- and preferred sequence of possible solutions prior to situations.
bally suggest to the child activities. responding. Learn acceptable ways
regulation of behavior in Clarifying goals, meeting of expressing one’s
relation to the specific subgoals. emotions (i.e., regulate
requirements of a task, or
to any other cognitive Need to pace one’s activities. the pace and intensity of
one’s social responses to
process required prior to Need to regulate the level anger and joy).
overt action. of energy invested in any
given task.
In the experimental group, these behaviors were represented by the criteria of mediation,
and in the control group, by basic aspects of a stimulating, responsive, non-punitive
environment.
Since mediation was found to affect children’s cognitive functioning (including
perception, elaboration, and expressive processes), it was expected that maternal me-
diation behaviors (e.g., focusing, showing affect, and expanding) would affect chil-
dren’s vocabulary and abstract reasoning and, in general, prepare children to perform
better in situations requiring “new learning,” such as tasks requiring immediate se-
quential memory. Thus, children’s cognitive performance was assessed using the fol-
lowing measures: Peabody Picture Vocabulary Test (PPVT), the auditory reception,
visual reception, visual association, auditory association, and auditory sequential
memory of the Illinois Tests of Psycholinguistic Abilities (ITPA), as well as the Beery
and Bucktanika test of visual motor integration. In addition, children’s behavior dur-
ing the play interactions with their mothers’ was video recorded and analyzed.
Comparison of the two groups on the separate components of each mediation fac-
tor, three years following the intervention, revealed that the mothers who participated
in the intervention, (i.e., learned to “read” their interactions with their children),
showed significantly more mediation behaviors (Klein & Alony, 1993).
Significant differences in favor of the children in this group were found on the
PPVT, auditory reception and auditory association measures. The average PPVT IQ for
the experimental group was 101 (SD = 15.5), and for the control group, 84 (SD = 14.1).
Of all factors of maternal mediation, mothers’ expanding and rewarding behaviors
were most frequently related to children’s cognitive performance. Within these two
types of behavior, maternal request for expansion of ideas (i.e., “Does it remind you
of anything?”, “What is it like?”) and mediation of competence with explanation
(rather than simply saying “Good,” “Fine,” etc.) were singled out as most significantly
related to the children’s cognitive performance at age four. These findings coincide
with those reported by Collins (1984), identifying the variable of “demandingness” as
one of the most essential determinants of the quality of “good” family environments.
Similarly, Heath (1983) suggests that demanding from children that they reconstruct
experiences verbally, (i.e., asking young children to tell about their experiences) may
enhance their thinking and language development. Children’s expressions of affect
were most significantly related to all criteria of maternal mediation, but mostly to ma-
ternal rewarding behaviors, maternal expansion of ideas, and maternal request for “af-
fect,” that is, attempts to arouse signs of excitement in relation to anything or anyone.
Focusing behavior in isolation from the other mediational behaviors (e.g., only
catching of attention) was not significantly related to any of the cognitive outcome
measures. A noteworthy relationship was found between the children’s performance
and the mothers’ nonverbal expression of feelings. Mothers’ expressions of feelings
were also found to be related to children’s spontaneous provision of rewards to others.
The mediational approach applied in the follow-up study was not designed to im-
prove children’s performance on specific cognitive tasks. Yet, three years following
the termination of the intervention, children in the experimental group outscored the
children in the control group with regard to language performance as measured by the
PPVT and two measures of verbal reasoning. These findings suggest that children
from poor families who participated in the intervention were brought well within the
128 PNINA S. KLEIN
normal range of verbal performance. Mothers in the intervention group expressed

higher aspirations for their children’s intellectual growth, as well as a more flexible
and balanced view of the factors they thought were important for their children’s
future development. Provision of external rewards was traditionally criticized in edu-
cational literature (e.g., LeVine, 1980; Lepper, 1981). In the Klein and Alony (1993)
follow-up study, verbal or gestural praise contributed favorably to children’s cognitive
and social-emotional development, but only when it was accompanied by explana-
tions relating “success” to its causes or associating it with other experiences. Young
children depend on adults for mediation of competence. Quality mediation requires
recognition of children’s individual needs, including those related to the frequency, in-
tensity, and type of reward they may require.
It has been well established in psycho-educational literature that children from
poor families generally score lower on a variety of cognitive measures related to in-
telligence and academic performance as compared to middle-class children. Mothers’
intelligence or years of schooling were repeatedly pointed out as powerful predictors
of children’s cognitive performance. The following finding from the mediational in-
tervention and follow-up study is of special interest in view of the preceding facts. The
correlation between mothers’ years of schooling and their mediation to their infants
and young children prior to the intervention was almost identical to that found in the
intervention and the comparison group (for the intervention groups, r = .43, and for
the control group, r = .45). Three years following the intervention, the correlation be-
tween mothers’ years of schooling and the mothers’ mediation went down (to .21) in
the intervention group, while remaining almost constant (r = .42) for the comparison
group. Furthermore, the correlation between mothers’ years of schooling and chil-
dren’s Bayley’s Mental Development Scales for both groups prior to the intervention
was .36. Following the intervention, the correlation between mothers’ years of school-
ing and children’s PPVT scores was .23 for the intervention group and .41 for the com-
parison group. These findings suggest that the quality of maternal mediation can be
modified. Once modified, the link between mothers’ schooling and their behavior in
interactions with their children can be modified as well, resulting in blocking of the
commonly found link between mothers’ education and children’s cognitive achieve-
ments. Poor mothers (and other caregivers and educators) can improve their mediation
and contribute to their children’s cognitive development as well as middle-class moth-
ers. The effectiveness of the mediational approach with populations of very poor chil-
dren was demonstrated in Sri Lanka (Fugelsang & Chandler, 1996), in Indonesia
(Hundeide, 1996) and recently, following a 12-year intervention project, in Ethiopia
(Klein, 2001a; Klein & Rye, 2004).
Typical Profiles of Mediation in Special Populations

The mediational approach was used with populations of children with special
needs, including children born at very low birth weight (Klein, Raziel et al., 1987),
children with Down Syndrome, and very young gifted children (Klein, 1996). A spe-
cific pattern of mediation was frequently noted for parents who believed in their abil-
ity to help their children overcome their developmental problems and who were highly
motivated to act toward achieving that goal. For example, parents of very low birth
weight (VLBW) children showed disproportionately high frequencies of focusing be-
haviors which were unmatched by high frequencies of other mediational behaviors,
i.e., showing affect, expanding, encouraging, and regulation of behavior. It was as
though those parents were highly motivated to interact with their children but were not
aware of the need to associate meaning to whatever was focused on. As a result, they
did not provide them with meaningful sequences of mediation. Instead, they focused
and refocused their children’s attention on objects or people in their environment, but
did not enable them to use the focused attention in order to obtain meaning, expand
experiences, and experience success. Even brief mediational interventions with popu-
lations of VLBW children and their parents led to significant improvement in parental
mediation and consequently to the enhancement of cognitive performance of the chil-
dren (Klein, Raziel et al. 1987).
In a study on the development of pre-verbal communication, 80 dyads of parents
and infants, including 40 infants with Down Syndrome and 40 infants who were de-
veloping normally, the infants were followed from the age of 7 months to 22 months
(Klein & Rosenthal, 2002). The developmental patterns of pre-verbal communication
of the babies were matched with the profiles of mediation provided by their mothers.
Children with Down Syndrome were found to be jeopardized twice, once due to the
syndrome causing a slower rate of development, and again due to poor mediation pro-
vided by the mothers. Major differences between interactions of mothers with typi-
cally developing infants and the interactions of mothers with Down Syndrome infants
emerged around the age of 14–16 months. At that age, significant gaps were found
in the development of Down Syndrome infants as compared to typically developing
infants. Mothers of Down Syndrome infants showed an excess of focusing behavior
and regulation of behavior with minimal affecting and expansion (e.g., expressing
meaning, explaining, and making associations).
Modifications of the mediational approach are introduced to meet the special
needs of young children with PDD (Pervasive Developmental Disorders). For exam-
ple, their parents are guided to mediate affect frequently and in an exaggerated man-
ner in order to open and close circles of communication with their children. In addi-
tion, they are helped to mediate affect by associating meaning with whatever the child
does, even if the child’s behavior seems unrelated to any intent or lacking in meaning.
These patterns of mediation are meant to create associations between actions and their
purpose and lead to the development of the spontaneous formation of such associa-
tions in the future (Greenspan & Wieder, 1996).
Parents of young gifted children appear to use a mediational style that is charac-
terized by higher frequencies of mediation in the form of questions rather than giving
of information. It appears that these parents repeatedly ask their children to verbally
reconstruct experiences they have had or to reply to questions about them. In other
words, parents of gifted children actively demand the “exercising” of their children’s
thinking (Moss, 1992).
Extreme poverty has been found to result in a general decrease in mediation, par-
ticularly in mediation of affect and expansion. Parents preoccupied with daily worries
130 PNINA S. KLEIN
about the mere survival of their family may not have enough mental energy to invest
in expressions of excitement related to objects or events in the environment or to as-
sociate those experiences with others in the child’s past or future. Thus, it is possible
that the cycle of poverty is perpetuated, since one of the types of mediation most con-
ducive to cognitive development as well as school achievement, is missing in parental
mediation to these young children.
Cross-Cultural Differences in Styles of Mediation:

Analytical and Holistic Styles of Mediation
Two general styles of mediation, a Western, analytic style and a traditional, holis-
tic style, were identified following studies of mediational experiences in six cultures
(Klein, 1996). The analytical style is frequently used by parents in Western cultures
and is guided primarily by the objective of teaching the infant about objects available
in his or her environment. The holistic approach is typically used in the so-called “tra-
ditional societies” in developing countries (Hundeide, 1996). Parents do not attempt
to fragment experiences in an analytical way for the child. The child learns through
participation in the life experiences of the family and acquires the meaning of things
holistically. There are very few experiences of expansion; most interactions with
adults are not decontexualized (i.e., not explored beyond the immediate context).
These children may be well equipped to adjust to life in their traditional native com-
munity, but they are not ready to cope with the Western style of education that requires
experiences of analytic mediation. Western children are equally unprepared to live in
traditional societies, but their parents are generally less interested in this sort of cross-
cultural learning.
Interpersonal Variability in Mediation

In order to assess the type of mental diet received by young children in their daily
interactions with the adults around them, it is necessary to assess the characteristics of
a child’s day, the people he or she interacts with, and the kinds of toys or objects used
in those interactions. Different people may provide different profiles of mediation. It
is also possible that the same adult may provide a different type of mediation to one
child as compared to another. Thus, it is of interest to assess a child’s mental diet by
summing up all the experiences he or she has with adults. Some of the causes for vari-
ability in a child’s mental diet have been found to be related to the adult’s perception
of the child and of his or her own educational objectives in relation to that child. In
addition, different toys, objects, games or activities typically invite various profiles of
mediation. For example, reading a book frequently includes higher frequencies of af-
fecting and expanding, whereas playing “rough and tumble” may include more regu-
lation of behavior.
Children’s interactions with other children may also contribute to a child’s mental
diet. For example, 5-year-olds were found to mediate to their 3-year-old siblings using
focusing, affecting, regulation of behavior, and encouragement. However, their medi-
ation typically lacked expansion and encouragement with explanation (Klein, Feld-
man et al. 2003). Both of these types of mediational behaviors were found as deter-
minants of children’s future learning. Thus, children who spend most of their time
interacting with their siblings or other children may lack these important components
of their mental diet.
Current research on the application of developmental mediation focuses on match-
ing specific developmental profiles of infants and young children with the profile of
mediation that may be best suited to their needs within the context of their family,
community, and culture. In a sense, this is an attempt to plan a mental diet appropri-
ate for the changing needs of infants and young children as they develop.
Summary
Infants and young children require adult mediation in order to develop the poten-
tial to benefit from new experiences. Various patterns of mediation have been found
to be related to characteristic behaviors of infants and young children, reflecting the
needs to seek clarity in perception, to search for meaning, to seek information beyond
what could be perceived directly through the senses, to link between experiences
(spontaneous associations), to experience success, especially in social contexts, and
others. It is possible to enhance parents’ or teachers’ mediation through intervention,
and consequently to affect the mental development of infants and young children. Spe-
cific patterns of mediation were identified cross-culturally and in populations of chil-
dren with special needs. Learning to “read” these patterns (i.e., learning to use the lit-
eracy of interaction) may be helpful in planning suitable mental diets through quality
educational programs for young children. “Literacy of interaction” refers to sensitiza-
tion and consciousness-raising regarding key issues in the adult-child (parent-child,
caregiver-child, or teacher-child) interaction. In practice this means trying to raise the
adult’s awareness regarding his or her own basic philosophy of childrearing, percep-
tions of the child; of himself or herself as parent or teacher; of the child’s emotional
and cognitive needs; and how all these affect the interaction with the child, especially
the mediational interactions, namely the attempts to teach the child. The representa-
tion of all these components is referred to as the literacy of interaction representing a
child’s mental diet.
Most of the decisions of educational policymakers focus on what is done, rather
than on how it is done in the teaching-learning interaction. The developmental appro-
priateness of educational programs for young children is frequently assessed in terms
of outcome measures, primarily including measures of achievement, skills and abili-
ties, and rarely involving a focus on how the process of adult-child interactions poten-
tially affect children’s readiness to learn in the future. This paper suggests that answers
to the “How” question may explain much of the variability in children’s readiness to
learn, through the effects on children’s need systems, motivation, and self-regulation.
The following is an example of an educational approach exemplifying the use of the
basic ideas discussed here.
132 PNINA S. KLEIN
The Developmental Mediation Approach

The MISC is presented here as a model educational approach, which is based on
attempts to analyze or read interactions and use them to enhance early education. The
acronym MISC stands for both the process and the objective of this approach. The ob-
jective of this approach is More involved, interested, insightful (Intelligent) and Sen-
sitive Children (MISC). Intelligence is referred to as the ability and need to learn
readily and easily from one’s experiences, also referred to as flexibility of mind. Sen-
sitivity is defined as the ability to understand one’s self and others’ emotions ex-
pressed in adult-child interactions and to respond in a way that promotes the quality
of the interaction, including positive affect, synchrony between partners, and optimal
duration of the interaction. The process through which this objective is achieved is
represented by the same acronym MISC—a Mediational Intervention for Sensitizing
Caregivers, including parents and teachers.
The MISC approach is based integrating three major frameworks, two of which,
the eco-cultural and the developmental approach, are frequently mentioned in current
early intervention approaches. The integration of the first two components with the
third, the mediational one, is unique and is proposed as a necessary combination for
effective early childhood education in general and for early intervention in particular.
The three components of the MISC are as follows:
1. The eco-cultural approach relates to the necessity to raise the awareness of the
adults interacting with young children of their own deep objectives of child-
rearing, their long-term educational goals, their perception of the ideal child,
ideal parent, etc., vis-à-vis their actions toward achieving immediate goals,
such as teaching specific content matter. This is particularly important when
teachers and children come from different cultural backgrounds.
2. Growth and development are viewed as a dynamic process in which both child
and adult are partners affecting each other and the environment. Based on this
framework, programs for infants and young children must take into consider-
ation young children’s basic emotional needs for stable affectionate relations
with one adult as the basis for any future learning.
3. A developmental mediation approach combines basic elements from the de-
velopmental approach and the mediational approach. Based on the theory of
cognitive modifiability (Feurstein, 1979, 1980) and Vygotzky (1978), several
basic characteristics of adults’ behavior that are necessary to create experi-
ences of mediated learning for young children were empirically defined and
identified. Empirical evidence (Klein & Alony, 1993; Klein, 1996; Tzuriel,
1999) suggests that these experiences may consequently promote the chances
for cognitive and emotional development of young children by affecting their
needs systems. These mediational processes (see Table 1) include the follow-
ing behaviors by adult caregivers:
• Focusing—attempts to get a child’s attention.
• Affecting—attempts to raise the child’s awareness of the affect or signifi-
cance associated with objects, people, and actions in the environment, i.e.,
expressing the meaning and significance of things, people, or processes.
• Encouraging—mediates feelings of competence to the child.
• Expanding—transcends verbally or nonverbally the concrete immedi-
ate context of the interaction (also known in the educational literature as
“distancing”).
• Regulating behavior—attempts to mediate planning behaviors, including
considerations that precede actions, as well as actually demonstrating to a
child how to do things.
Typical Features of the Developmental Mediation Approach

The objective of the developmental mediation approach is to promote a sound, fa-
cilitative adult-child relationship with a special focus on adults’ teaching behavior—
enhancing and improving the literacy of interaction representing a child’s mental diet.
One approach using the MISC is based on videotaping and providing video feedback of
adult-child interactions. Adults view themselves interacting with their children and are
helped to analyze their interactions in relation to their own views and perceptions of
their child, themselves, their educational objectives, and the child’s actual sensory pro-
file and developmental status (Klein, 1996). A profile of mediation represents the fre-
quencies and sequences of mediational behaviors in the observed interaction. Initially,
the most frequent or the best mediational behaviors are pointed out and discussed, fol-
lowed by the others. In addition, the synchrony of the interaction, and the adult’s sensi-
tivity and responsiveness to the child’s initiatives are highlighted. This process helps
parents, caregivers, and teachers sharpen their awareness regarding what they bring to
the interaction vis-à-vis what their child contributes to it, and how those contributions
interplay and modify the interaction. Following this process, parents, teachers, and care-
givers frequently become more motivated and interested in the interactions with their
children as they gain competence in their own behavior as caregivers. The latter is most
important for sustaining long-term effects of the mediational approach.
Poor Mediation and Difficulties in Learning?

In line with Feuerstein’s theory of cognitive modifiability (Feuerstein, 1980),
much of the variability in children’s capacity to benefit from new experiences
(namely, flexibility of mind) is linked to the type of mediational interactions they have
had with the adults who cared for them. These differences are apparent in the way
these children approach new experiences, in the way they integrate them with other
experiences, and in the way they express themselves. Many children lack the enthusi-
asm or need to explore their environment, to search for meaning, to think of connec-
tions between things, to seek newness. They are satisfied with a blurred, undifferenti-
ated picture of their environment. Their eyes and ears (although functioning normally)
are not tuned to detect fine differences between various things they perceive. They do
not have the need to form a link between cause and effect, between past, present, and
future experiences, and are less inclined to seek an adult’s assistance in order to solve
problems or obtain more interesting information or objects. It is clear that children
with undifferentiated, blurred perceptions, lack of enthusiasm, and absence of the
134 PNINA S. KLEIN
drive to explore and opportunities to do so, experience things in an isolated, frag-

mented manner, which limits their capacity to benefit from future experiences. Chil-
dren who have these limitations may be considered as lacking flexibility of mind or as
having difficulties in benefiting from new experiences. Most of these behaviors have
been identified by Feuerstein (1979, 1980) as reflecting deficient cognitive processes
related to poor mediational experiences.
Differences between the MISC and Other Early Interventions

The MISC was designed to overcome some of the difficulties that were inherent in
ongoing early intervention projects in various countries in Africa, Asia, Europe, and
in the United States (Klein, 1996). Although different programs were implemented in
different countries, the following problems were reported repeatedly in many of them:
1. Whereas many early education programs aim to promote the development of
cognitive skills or abilities, the prime objective of the mediational approach is
to affect the children’s need system, to create new, more differentiated needs
that could promote their future appetite and capacity for learning (see Table 1).
It is a misleading notion to assume that merely bringing people into contact
with new experiences helps them to develop a differentiated taste or need for
them. We can take children to the theater, to the library, or to a concert, but
does it affect their need to seek cultural experiences of this kind in the future?
An infant or young child experiencing pleasant feelings in the presence of an
adult wants to be with him or her even after basic needs have been fulfilled.
Hearing the adult, pointing to things, explaining them, associating, comparing,
contrasting, becomes desirable as well, and thus develops the need for more
such “educational” interactions. Fredrickson (2001) has suggested that posi-
tive feelings have an effect on cognitive dispositions and processes, and that as
the links between them persist, these processes become a permanent part of
one’s repertoire of behavior. It is through pleasurable human interaction and
mediation that an infant or young child learns to need and seek clear informa-
tion, beyond what is directly perceived by his or her senses and all the other
needs listed earlier, which are associated with better reception, organization,
and application of learned experiences.
2. Parents from various ethnic backgrounds, especially poor parents, were led by
education professionals to believe that there is one ideal model, a “better way”
of raising and educating young children, better than the traditional way they
brought with them from their old homes. The transition from the old to the
new frequently led to a feeling of alienation. Parents felt that what they had to
transmit to their children would not sufficiently promote later development.
They felt that they could only contribute the little they had been taught by their
child’s kindergarten teacher, nurse, or visiting specialist in the ongoing pro-
grams. This misperception limited all forms of cultural transmission and min-
imized the chance to capitalize on the best learning opportunities for the chil-
dren. The application of structured, content-oriented programs using specific
materials tended to create a dependency on these materials (e.g., toys, book-
lets, etc.) and limited transfer to other situations or other children within the
family, daycare, or educational setting.
3. There are differences between stimulating and mediating children. Stimula-
tion is a concept that most people, including professionals, parents, and care-
givers seem to view as a positive educational process. Yet, as is clarified here,
it may be a relatively useless or even a developmentally harmful process, far
from the original intent of those who are encouraging its use. In a modern
competitive society, parents are pressured to provide their children with every-
thing possible to insure that they are not left developmentally behind other
children. Many parents or caregivers are misled to believe that stimulating
young children, (i.e., merely catching their attention or focusing it on frag-
mented stimuli, without using this attention to convey meaning or relate expe-
riences), promotes their development. Such experiences may be perceived by
children as a bombardment of their senses and as inappropriate for them and
their specific needs at a particular moment. Such experiences may minimize
the child’s chances of developing the appetite and dispositions for learning.
As the MISC is focused on the quality of the adult-child interaction, and not on the
content of the material used in this interaction, it is not a program in the traditional
sense. It is more a method for sensitizing mothers (and other caregivers) to the posi-
tive aspects of their existing interaction and childrearing practices. As such, it can
never be in conflict with the mothers’ own traditional way of childrearing and stands
a better chance of sustaining long-term effects on parental behaviors.
Note: The research presented here was supported in part by WHO, UNICEF,
UNESCO, NORAD, and Red Barnna, supporting the implementation of the MISC in
Ethiopia, Sri Lanka, Indonesia, Norway, Sweden, the Unites States, and Israel. Prepa-
ration of this manuscript was supported by the Machado Chair for Research on Cog-
nitive Modifiability, Bar-Ilan University, Israel.
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Toward a Behavior of Reciprocity
Morton Ann Gernsbacher

University of Wisconsin-Madison
MAGernsb@wisc.edu
Abstract: It is frequently believed that autism is characterized by a lack of social or emo-

tional reciprocity. In this article, I question that assumption by demonstrating how many
professionals—researchers and clinicians—and likewise many parents, have neglected the
true meaning of reciprocity. Reciprocity is “a relation of mutual dependence or action or
influence,” or “a mode of exchange in which transactions take place between individuals
who are symmetrically placed.” Assumptions by clinicians and researchers suggest that
they have forgotten that reciprocity needs to be mutual and symmetrical—that reciprocity
is a two-way street. Research is reviewed to illustrate that when professionals, peers, and
parents are taught to act reciprocally, autistic children become more responsive. In one
randomized clinical trial of “reciprocity training” to parents, their autistic children’s lan-
guage developed rapidly and their social engagement increased markedly. Other demon-
strations of how parents and professionals can increase their behavior of reciprocity are
provided.

Worldnet Dictionary (thefreedictionary.com) defines reciprocity as “a relation of
mutual dependence or action or influence.” Hyperdictionary (hyperdictionary.com)
defines it as “a mode of exchange in which transactions take place between individu-
als who are symmetrically placed, that is, they are exchanging as equals, neither being
in a dominant position.” The connotation of reciprocal as actions given or done in re-
turn permeates many of our political and societal coinages; we use expressions such
as reciprocal aid, reciprocal trade, and reciprocal privileges (e.g., reciprocal member-
ship privileges at health clubs or reciprocal borrowing privileges at lending libraries).
Indeed, a primary association to the word reciprocity for the author is the agree-
ment between the University of Minnesota and the University of Wisconsin that
allows Wisconsin state residents to attend the University of Minnesota, paying only
in-state tuition, rather than the more expensive out-of-state tuition, and similarly Min-
nesota state residents can attend the University of Wisconsin, paying only in-state tu-
ition. This agreement between the Universities of Wisconsin and Minnesota epito-
mizes reciprocity: It is mutual, it is symmetrical, and the exchange occurs with neither
party being in a dominant position.
138
Toward a Behavior of Reciprocity 139
Now, consider reciprocity with regard to autism. The thesis of this article is that
many professionals—researchers and clinicians—and likewise many parents, have neg-
lected the reciprocal nature of reciprocity. They have forgotten that reciprocity needs to
be mutual and symmetrical—that reciprocity is a two-way street. Thus, the purpose of
this article is to move us toward a behavior of reciprocity, genuine reciprocity.
Reciprocity and Autism

It has become a truism that autism is characterized by a lack of social or emotional
reciprocity. So accepted is this assumption that, for example, in a recent research arti-
cle examining a hypothesized autism susceptibility gene, the opening line simply
claimed that “impaired reciprocal social interaction is a core feature of autism”
(Wassink et al., 2004, p. 968). No scientific citations were needed, no supporting data
were required; the statement was assumed to be fact. Interestingly, however, none of
the initial descriptions of autism mentioned reciprocity and its assumed lack. For ex-
ample, the seminal diagnostic criteria for autism published in 1980 in the DSM-III did
not mention one word about reciprocity (APA, 1980). The more recent 1994 published
DSM-IV criteria for autism do mention reciprocity (APA, 1994); more specifically, “a
lack of social or emotional reciprocity” is listed as one of the 16 possible characteris-
tics of autism. However, no examples are provided of how a lack of social or emo-
tional reciprocity would be manifested in behavior.
One would think that the very well known Social Reciprocity Scale (Constantino,
2002), which has been used in several studies of autism (Constantino & Todd, 2000;
Constantino & Todd, 2003; Constantino, Gruber, Davis, Hayes, Passanante, & Przy-
beck, 2004; Towbin, Pradella, Gorrindo, Pine, & Leibenleft, 2005), would provide ex-
amples. And indeed, a few of the 65 items on the Social Reciprocity Scale do approx-
imate a rough vernacular of what might constitute socially or emotionally reciprocal
cognitions, for example, “is unaware of what others are feeling or thinking,” and per-
haps “doesn’t recognize when others are taking advantage of him/her,” and “would
rather be alone.”1 However, even among the first several items on the Social Reciproc-
ity Scale there are items that do not fit a true meaning of reciprocity (or its lack), for
example, “expressions on his/her face don’t match what he/she is saying,” and “doesn’t
seem self-confident when talking.” Other items seem completely unrelated to social
reciprocity, for example, “is not well coordinated in physical activities,” or “doesn’t
have good personal hygiene.”
Other items on the Social Reciprocity Scale illustrate the thesis of this article:
Some professionals have forgotten the true meaning of reciprocity. Consider the item,
“is regarded by other children as odd or weird.” This item appears to measure other
1. I have relabeled these as “cognitions” because I find it baffling that they would be considered “behav-
iors,” given that they are thoughts (e.g., awareness of what other people are thinking or feeling) or perhaps
predilections (a preference to be alone). However, such items demonstrate a type of arrogance if the observer—
the parent or teacher, who completed the questionnaire about the target child—truly believes that he is aware of
what the other person (the target child) is thinking.
140 MORTON ANN GERNSBACHER
children’s lack of social or emotional reciprocity. Regarding another child as odd or

weird implicates the regarder—not the target child—as lacking in empathy or under-
standing. As a final example, consider the item on the Social Reciprocity Scale that
asks whether the child “gets teased a lot.” How in the world the occurrence of a child
being teased could be construed as a metric that he or she lacks social or emotional
reciprocity is baffling. However, as the researchers who constructed this scale have
demonstrated, this item is highly correlated with autism: Autistic children do get
teased a lot, so much so that being teased and bullied has been elevated to a pheno-
typic criterion (Kunihira, Senju, Dairoku, Wakabayashi, & Hasegawa, 2006). Why do
autistic children get teased so much? I submit this is because many non-autistic chil-
dren, in addition to professionals and sometimes parents, forget that reciprocity is a
two-way street.
Consider the following anecdote. On a lark one day a few years ago, I typed into
the search bar of eBay the word “autism.” I was surprised to see over 500 items listed
for auction that claimed to have some relation to autism. One item in particular caught
my attention. The auction was titled, “Autism: See the World through My Eyes,” and
the auction item was a button, such as one wears on a lapel. The button contained a
picture of a young girl named Sarah, looking out a window, and the message: “I wish
you could see the world through my eyes!” The auction description explained that
Sarah’s father created this button because the message captured how Sarah responded
to a homework assignment that asked what she would wish for if she had a magic
wand. Sarah wished that others could see the world through her eyes.
On the exact day that I bumped into that eBay auction, an article appeared in the
New York Times entitled, “Experiment Offers Look through Eyes of Autism” (O’Neil,
2002). The article stated that “using a high-tech eye-tracking device developed for the
military, researchers at Yale ran experiments that came closer than anything yet to of-
fering a look at the world as seen through the eyes of people with autism.” Could this
be Sarah’s most fervent wish coming true? No, sadly not. As the New York Times ar-
ticle stated, “In the experiment, described in the current issue of The American Jour-
nal of Psychiatry, the researchers compared the eye movements of a highly intelligent
autistic adult and a control subject of the same age, sex, and I.Q as they watched the
relentless emotional conflicts of “Who’s Afraid of Virginia Woolf?”
From this eye-tracking experiment, the researchers concluded that “the two sub-
jects were seeing the movie in starkly different ways. When Mr. Burton and Ms. Tay-
lor, playing an alcoholic professor and his shrewish wife, confronted each other face
to face, the gaze of the non-autistic adult swung intently between their eyes, while the
autistic subject looked back and forth, as well—but focused on the actors’ mouths.”
If the researchers could really see through the eyes of the autistic participant, they
might have seen that it was more comfortable for him to focus on the mouths rather
than the eyes (Gernsbacher & Frymiare, 2005), or that the mouths were even more
informative—particularly because the individual with autism had a history of lan-
guage impairment (Campbell & Dodd, 1980; Kuhl & Meltzoff, 1982; McGurk &
MacDonald, 1976). Indeed, we know that other individuals with a history of language
impairment who are not autistic focus on mouths for further information processing
during discourse. It is a very adaptive strategy. But this very adaptive strategy was
billed in the New York Times as “a profound social disability.”
In her book, How to Be a Para-Pro: A Comprehensive Teaching Manual for Para-
professionals, non-autistic Twachtman-Cullen (2000) takes the perspective of an
autistic child who requests the following of those around him or her: “Even though
there are many things about me that are unique, in the ways that really matter, I am
just like other children. I learn best from people I trust, and learn to trust when I sense
that people like me. Please try to see the world through my eyes. Please know that
even though it may not seem so, I really am trying to adapt to a world that my neuro-
logical challenges [sometimes] prevent me from understanding.”
Such neurological sensitivities were identified in a research article published in the
Journal of Applied Behavioral Analysis (Tang, Kennedy, Koppekin, & Caruso, 2002).
In this article, titled “Functional Analysis of Stereotypical Ear Covering in a Child
with Autism,” four researchers conducted 43 half-hour observations across four days
and submitted those extensive and intricate observations to numerous detailed behav-
ioral analyses to understand the origin of “stereotypical ear covering that was reported
by the child’s teachers to serve no identifiable function” (p. 95). The researchers con-
cluded that “the results of a descriptive analysis revealed a correlation between ear
covering and another child’s screaming. An analogue functional analysis showed that
ear covering was emitted only when the screaming was present” (p. 95). It is difficult
to imagine that a magic wand, high-tech expensive military eye-tracking equipment,
or a detailed applied behavioral analysis was needed to appreciate this child’s very
adaptive response to an assault against his auditory sensitivities. What was needed was
greater social and emotional reciprocity—social and emotional reciprocity by the
teachers and the researchers toward the autistic child.

How can parents, clinicians, teachers, and researchers move toward a greater be-
havior of reciprocity? In the words of the Count of Monte Cristo (Dumas, 1846/2000,
p. 592): “A secret voice seems to whisper to me that there must be something more
than chance in this unexpected reciprocity of friendship.” The behavior of social and
emotional reciprocity needs to be acquired with something more than chance; reci-
procity needs to be developed more purposefully by non-autistics and applied more
generously toward autistics. Twenty years of applied behavioral analysis (ABA) sup-
port this plea, although this body of ABA research has never been interpreted from a
truly reciprocal perspective.
For example, in 1985 researchers taught three typically developing kindergartners
some basic pro-social behaviors such as “offering to share with peers and to help
peers . . . [i]nviting peers to play and requesting permission to play with peers”
(Kohler & Fowler, 1985, p. 191). Two of the three typically developing children main-
tained and increased these pro-social behaviors; a third child did not. What happened
with the third child? Very simply, the “third child’s play invitations were not recipro-
cated by [her] peers; her invitations subsequently decreased in rate” (p. 187).
In 1986 researchers taught four typically developing preschoolers to either initiate
interaction with three autistic preschoolers or to respond to the interaction that the
three autistic preschoolers initiated, in other words, to be reciprocal (Odom & Strain,
1986). Which intervention had the more lasting influence on the autistic preschoolers’
social interaction? When the typically developing preschoolers were taught to respond
to the interaction that the autistic preschoolers initiated, the autistic preschoolers re-
sponded more frequently. In other words, when the typically developing preschoolers
behaved reciprocally, the autistic preschoolers responded more positively.
In 1988 researchers taught three autistic kindergartners to initiate pro-social physi-
cal interaction—giving high fives, patting a friend on the back—by incorporating the
actions into a song, such as “if you’re happy and you know it, give your neighbor a high
five” (McEvoy, Nordquist, Twardosz, Heckaman, Wehby, & Denny, 1988). The three
autistic kindergartners then interacted with six typically developing kindergartners, only
half of whom had also gone through the pro-social physical interaction training them-
selves. The typically developing kindergartners were considerably more likely to recip-
rocate the autistic kindergartners’ interactions if they too had gone through the training.
In 1992 researchers taught three typically developing preschoolers, called peer tu-
tors, to prompt for the verbal labels of preferred toys from three autistic children,
whom the researchers called target children (McGee, Almeida, Sulzer-Azaroff, &
Feldman, 1992). The peer tutors were told to “(a) wait for the target child to initiate a
request for (i.e., reach for) a toy, (b) ask the target child for the label of the toy (e.g.,
“Say duck”), (c) give the toy to the target child when he labels it, and (d) praise the
correct answer (‘That was great! You said duck’). None of the target autistic children
maintained their initiation with the typically developing peer tutors after the training
sessions were completed. Why not? I submit it was because the interactions were not
reciprocal. Recall that reciprocity is defined by “a relation of mutual dependence or
action or influence” and “a mode of exchange in which transactions take place be-
tween individuals who are symmetrically placed, that is, they are exchanging as
equals, neither being in a dominant position.” Peer tutors prompting autistic target
children for verbal labels is neither mutual nor symmetrical.
Given these ABA data, the following scenario related by a mother in the section
called “From the Front Line” of the near-classic ABA-for-autism manual, Behavioral
Intervention for Young Children with Autism: A Manual for Parents and Profession-
als (Maurice, Green, & Luce, 1996) makes infinite sense. The mother began by de-
scribing how she established a behavioral therapy program for her daughter.
The first order of business was to establish attending behaviors. This was ac-
complished by the therapist holding a food reinforcer at her eye level while
stating “Rebecca.” Rebecca wanted that reinforcer (a raisin or a Cheerio) so
she would look momentarily at the therapist who would immediately give her
the Cheerio and praise her verbally (Good looking, Rebecca!). Once Rebecca
began to attend, she was taught to follow simple gross motor imitations and
simple commands (stand up, clap hands, wave bye-bye). (p. 366)
By the time we hit the one year anniversary of our program 3 months ago,
Rebecca had developed a great deal of skills and language. . . . A sampling of
her current skills includes her ability to expressively identify all the letters of
the alphabet presented in random sequence. She knows her shapes and colors,
she can count up to 12 items, and she has an extensive vocabulary (several hun-
dred words). Additionally, she has become proficient in categorizing items
among nine different groupings. I was recently quizzing her in the car and
asked “What’s a zebra?” “It’s a animal.” “What’s a triangle?” “It’s a shape.”
“What’s a couch?” “It’s furniture.” “Who’s William?” “It’s a person.” “What is
a w?” “It’s a letter.” “What’s a helicopter?” “It’s something you ride in.”
“What’s a bathing suit?” “It’s clothes.” “What’s cake?” “It’s food.” (p. 369)
As the mother wrote, “I present these examples to illustrate that many of the things
that Rebecca knows are quite advanced for a child her age. I am convinced that Re-
becca is a highly intelligent child. Her teachers tell me this constantly. In a way, that
makes her deficits all the more maddening” (p. 369). What are these deficits that are
so maddening to her mother? As the mother laments,
If, for example, I enter the kitchen after my morning walk and [my two daugh-
ters] are sitting at the kitchen table eating breakfast, Rebecca might glance up
at me for a second and then look away. I have to walk up to her, get in her face,
and force the interaction (“Hi Rebecca.” “Hi Mama.” “How are you?” “Okay.”
“I love you.” “I love you, too.”). I have always found the contrast between my
two children to be the most obvious and the most painful at mealtimes. Holly
is such a talkative and observant child, and Rebecca will be sitting there like a
sphinx, unable to participate in the give and take.
We find ourselves continually trying to draw her into our conversations.
“Rebecca, what are you doing?” “I’m eating.” “What are you eating?” “Pasta.”
“Good. What’s pasta?” “It’s a food.” “Good! Is it delicious?” “Yes.” “Say, ‘It’s
delicious.’ ” “It’s delicious.” (p. 368)
Furthermore, as the mother describes, “One big problem that we have recently
been tackling concerns Rebecca’s compliance during her [behavioral therapy] ses-
sions. At times Rebecca becomes very silly … We had decided to completely ignore
Rebecca’s behavior during these incidents and to revert to a simple command pre-
sented over and over until Rebecca would get bored and comply. Unfortunately, this
tactic did not succeed in extinguishing the noncompliance (it was going on for more
than a month), so we are now resorting to putting Rebecca in time out, which we have
determined is an aversive for her” (pp. 369–370). Such an approach might be helpful
for teaching a child to see the world through your eyes, which is the promise of
Bridges for Children with Autism (bridgesABAtapes.com), an internet company that
sells ABA therapy training tapes, but recall that Sarah, the girl on the eBay button—
and perhaps Rebecca, also—wished that others could see the world through her eyes.
How can we do that?
Follow the Child’s Lead

According to one very prominent intervention style: “Follow your child’s lead and
play at whatever captures her interest” (Greenspan & Weider, 1998, p. 123–124). A
wealth of empirical evidence supports the benefit of following this crucial mantra in
both typical and atypical development. For example, Herman (2002) wrote the follow-
ing in her essay titled, “What Parents Do to Encourage Communication and Lan-
guage” regarding typical development:
The process of getting to know their new child involves parents noticing what
interests them and how they react. Parents watch to see what their baby looks
at and will often talk about whatever it is that appears to interest their child. In
this way, the parent follows the baby’s lead. For example, if the baby gazes to-
wards the light, the parent may comment “are you looking at the light?” In this
way, the parent imposes meaning on the baby’s actions, even though the baby’s
actions at this early stage are without any specific purpose. Eventually, this
teaches the baby that actions lead to responses. In addition, the fact that com-
munication is closely tied into whatever activity the baby is engaged in helps
the baby begin to make sense of the stream of words they hear.
Herman wrote that toward the end of the first year of life,
An important behaviour to emerge at this time is the development of joint at-
tention. This is a natural development from the parent following the baby’s
lead and talking about the child’s focus of attention, as described above. Babies
begin to be more aware of when they and their parents are focusing on the same
object or activity. By the age of 9–12 months, they are able to follow their par-
ent’s line of vision and make use of pointing gestures. This helps them to begin
to match the language they hear with the focus of attention. Indeed, where par-
ents follow the infant’s focus of attention when providing language, infants’
vocabulary acquisition has been shown to proceed at a faster pace.
But what about the child who is delayed in developing the ability to follow his par-
ent’s line of vision? What about the child who is delayed in developing the ability to
make use of pointing gestures, that is, to follow a parent’s manual point or to make his
own pointing gesture? Or even to make his own reaching gesture? Experience sug-
gests that this is when parents—and professionals—need to enact even more reciproc-
ity, need to share even more of the child’s world, need to follow even more of the
child’s lead, and need to become something of a detective to discern the ways that the
child is expressing joint attention and social and emotional reciprocity.
Consider the detective work effectively accomplished by Robert Hughes, a
Chicago writer, who chronicled his life with his autistic son Walker in a critically ac-
claimed book, Running with Walker. In an essay titled “Autism and Empathy,” pub-
lished in Chicago Parent magazine, Hughes (2004) wrote the following about 17 year-
old Walker:
He can’t converse, play a game, sit still, tie his shoes. He does every mainline
autistic behavior in the book: waves his hands and stares at reflected light,
shouts certain words and phrases over and over, rewinds his audiotapes until
they break. . . . But there is one quality he has in such abundance that it seems
almost to define him: empathy. Bouncing on his therapy ball, his throne in our
dining room, he knows his family’s hidden feelings no matter how well we
mask them.
Unfortunately, when he was much younger, his mother and I did not always
catch on to this depth of feeling in him. Since he never nodded “yes” and “no,”
much less enunciated those words in any consistent way, even some of his es-
sential character traits tended to stay under our radar. They were only revealed
in dramatic blips that slowly enabled us to see him in a new way.
One such moment came when he was four years old. I had just come home
from three days in the hospital undergoing tests for chest pain. The tests
showed that I had experienced one of those Middle-aged Dad Hypochondria
Alerts: My heart was fine; I was nuts. When I walked in our front door (as far
as Walker knew, back from the dead) he took my hand and pulled me over to
the couch. He got out a copy of Pinocchio, one of those Disney books a child
reads along with an audiotape, and turned the pages until he got to the place
where he wanted me to read to him.
It was the passage about Pinocchio saving his father from the whale. I
stopped in the middle of a sentence and stared at him, amazed. It was my odd,
silent four-year-old’s articulate way of telling his father of his love and con-
cern. Since then, [my wife] and I have read his strange behavior in the light of
the boy revealed that day: The one who feels far more deeply than he lets on,
who signals his thoughts and feelings in unconventional, but still very telling
ways.
It is those “unconventional, but still very telling ways” that parents, researchers,
clinicians, and members of society must seek to identify. As autistic advocate, Jim Sin-
clair, has written in an essay titled “Don’t Mourn for Us” (Sinclair, 1993):
The ways we relate are different. Push for the things your expectations tell you
are normal, and you’ll find frustration, disappointment, resentment, maybe
even rage and hatred. Approach respectfully, without preconceptions, and with
openness to learning new things, and you’ll find a world you could never have
imagined. Yes, that takes more work than relating to a non-autistic person. But
it can be done—unless non-autistic people are far more limited than we [autis-
tic people] are in their capacity to relate. We spend our entire lives doing it.
The Power of Imitation

In what ways can non-autistics show the behavior of reciprocity? We have known
for centuries that imitation is the sincerest form of flattery, and we have known for
decades that imitation improves social responsiveness in all children, including autis-
tic children (Dawson & Adams, 1984). I am not referring to autistics imitating non-
autistics, but rather non-autistics imitating autistics. When a stranger—such as an ex-
perimenter in a psychology laboratory—imitates an autistic child’s object-oriented
behavior, that is, the experimenter manipulates a duplicate object in the same way that
the child does, the child makes dramatically longer and more frequent eye contact with
the experimenter (Tiegerman & Primavera, 1984). When mothers imitate their autis-
tic children’s manipulation of toys, autistic children gaze longer and more frequently
at their mothers, the children engage in more exploratory and creative behavior with
the toys, and the children show considerably more positive affect (Dawson & Galpert,
1990). These effects are independent of the child’s developmental level.
In another laboratory experiment (Field, Field, Sanders, & Nadel, 2001), autistic
children displayed more socially reciprocal behaviors after repeated sessions in which
the experimenter imitated their behavior, in contrast to a control group of autistic chil-
dren with whom the experimenter played responsively but not imitatively. During a
second session in this experiment, autistic children who were imitated by the experi-
menter increased in looking, vocalizing, smiling and playing with the experimenter;
during a third session, autistic children who were imitated by the experimenter in-
creased in being close to the experimenter, sitting next to the experimenter, and touch-
ing the experimenter.
Can these reciprocal behaviors be packaged into a treatment program—a program
that trains parents and others to behave more reciprocally with their autistic children?
The answer is yes, and empirical evidence demonstrates the effectiveness of such pro-
grams. One study (Mahoney & Perales, 2003) used relationship focused intervention
to enhance the social emotional functioning of autistic children by implementing re-
sponsive teaching with the children’s parents. Some of the behaviors that the parents
were taught included the following: join the child’s perseverative play; read the child’s
behavior as an indicator of interest; follow the child’s lead; respond to the child’s be-
havioral state; match the child’s interactive pace; and expect the child to react accord-
ing to his or her temperament or behavioral style.
The participants were the mothers of 20 young children diagnosed as being on the
autism spectrum. The mothers received weekly one-hour intervention sessions for 8 to
14 months. Before and after the treatment, both the parents and the children were as-
sessed with a set of measures, but it is important to note that the treatment—the re-
sponsive teaching—was delivered only to the parents. Post-treatment, the mothers
were observed to have increased in their responsiveness and their affect, which was
the predicted outcome, and to have decreased in their achievement orientation and
their directiveness, which was also the predicted outcome (although the decreases in
achievement orientation and directiveness were not statistically significant). Post-
treatment, the children’s interactive behavior was observed to have increased an aver-
age of 50% in affect, persistence, interest, cooperation, initiation, and joint attention.
All improvements were statistically significant, and the largest gain was in joint atten-
tion, which improved 84%.
Post-treatment, the children’s socioemotional behavior was rated by their mothers
as being significantly less detached, more socially reactive, and better regulated,
according to the Temperament and Atypical Behavior Scale (Bagnato, Neisworth,
Salvia, & Hunt, 1999). In addition, as observed by the researchers using the Infant
Toddler Socioemotional Assessment, the children increased in their self-regulation and
social competence (Briggs-Gowan, Carter, Irwin, Wachtel, & Cicchetti, 2004; Carter,
Briggs-Gowan, Jones, & Little, 2003).
The gold standard in treatment outcome research is the randomized clinical trial
(i.e., an experiment in which there is both a treatment group and a control group, with
each participant being randomly assigned to one of the two groups). After decades of
claims such as “thirty years of research demonstrating the efficacy of applied behav-
ioral methods in reducing inappropriate behavior and in increasing communication,
learning, and appropriate social behavior” in autism (U.S. Surgeon General’s Office),
there exists only one randomized clinical trial assessing the efficacy of ABA interven-
tion for autism (Smith, Groen, & Wynn, 2000; see Gernsbacher, 2003, for a review).
Unfortunately, the one randomized clinical trial of ABA intervention for autism pro-
duced no significant improvements in social interaction or communication.2
Consider in contrast a randomized clinical trial evaluating the effectiveness of a
social communication intervention. Like the intervention delivered in Mahoney and
Perales (2003); however, this randomized clinical trial (Aldred, Green, & Adams,
2004) delivered intervention to only the parents of autistic children. The treatment
involved “educating parents and training them in adapted communication tailored to
their child’s individual competencies . . . promoting highly sensitive adult responses,
where actions made by the child are interpreted by the adult as having meaning and
being related to the child’s assumed intentions and desires, and replacing [the par-
ents’] controlling and intrusive responses with responses aimed at facilitating the
child’s active communication exchanges” (p. 1421–1422). Fourteen parents of autis-
tic children were randomly assigned to the treatment group, and the same number was
randomly assigned to the control group. The results of this randomized trial were quite
impressive.
Analysis of a 30-minute parent-child free play session by coders who were naïve
as to whether parents had been in the treatment or the control group identified several
statistically significant changes. First, parents in the treatment group increased 7.3% in
their synchronous communication, which comprises comments, statements, or ac-
knowledgements that maintain the child’s interaction; in contrast, parents in the con-
trol group decreased 7.6% in their synchronous communication. Second, parents in the
treatment group decreased 7.1% in their asynchronous communication, which com-
prised statements aimed at redirecting, controlling, or making demands on the child to
respond; in contrast, parents in the control group increased 7.6% in their asynchronous
communication. Third, parents in the treatment group increased 6.8% in their recipro-
cal communicative acts, which comprised verbal and non-verbal behaviors that share
communicative intent, while parents in the control group decreased 2.5%.
What effect did these parental changes have on their children? As measured by the
Autism Diagnostic Observation Schedule (Lord et al., 1989), children whose parents
received treatment were shown to increase significantly in their reciprocal social in-
teraction, their social engagement, their social rapport, their social responses, and their
spontaneous initiation of social interaction. The children also demonstrated dramatic
improvements in their language development, on the parentally reported MacArthur
Communication Development Inventory (Fenson et al., 1993). As shown in Figure 1,
children whose parents received treatment improved dramatically in their expressive
vocabulary, whereas children whose parents were in the control group did not. As
2. Although the original article reports significant effects on language development, there was an error in data
analysis, and an erratum was subsequently published (Smith, Groen, & Wynn, 2001).
Expressive Vocabulary
Vocabulary Size (on MCDI) 250
200
150 Treatment Group
100
50 Control Group
0
Pre-Treatment Post-Treatment
FIGURE 1. Data from Aldred et al. (2004)
Receptive Vocabulary
250
Vocabulary Size (on MCDI)
200
Treatment Group
150
100 Control Group
50
0
Pre-Treatment Post-Treatment
FIGURE 2. Data from Aldred et al. (2004)
shown in Figure 2, children whose parents were in the treatment group as well as the
control group improved in their receptive vocabulary.
Toward an Attitude of Reciprocity

Thus, parents can increase their reciprocity behavior. It is my hope that we can also
increase society’s reciprocal behavior and that greater reciprocity will permeate more
and more of our community’s attitude. Rather than reading a Newsweek “My Turn”
column (Lee, 2003), in which a mother bemoans a dreadful ride with her autistic son
on a hot, overcrowded, noisy trolley—an activity she had enjoyed when she was a
child but clearly her child did not, I’d like to see more media coverage like the Asso-
ciated Press story of Annie Lewis who camped out for 13 nights with her 12 year-old
autistic son Gregg so that Gregg, who is fascinated by Krispy Kreme donuts, could be
the first person to turn on the Krispy Kreme Hot light sign at the store’s grand open-
ing (Lucy, 2003). “It was a terrific experience, every minute,” Annie Lewis reported.
“I can now do a stand-up comedy act about this whole experience because it was
tremendously fun. I would do it again in a split second.”
Rather than reading on a state autism society list serve a mother’s description of
her child’s fourth birthday party that went like this:
Anna’s birthday started off fine, I had everything done and ready before the first
guest arrived at noon. The whole family was here by 1 so we ate, then Anna fell
asleep for her afternoon nap. Around 3ish I woke her up to open gifts. She got
all worked up, crying and yelling no, carrying on. It was mostly because I woke
her up, and she was feeling under the weather thanks to a wonderfully timed
cold. Anyhow, my husband Mark sat in her bedroom with her opening gifts
while the rest of my family sat there in the living room and dining room. She
finally warmed up and enjoyed a couple of the gifts. She then worked her way
to the dining room to play with a few new toys. I went and got the cake, put the
candles in, we sang, and Anna cried. That was an autistic moment; she NEVER
likes it when people sing the Birthday Song like that, even if it’s someone else’s
birthday. So I blew out the candles, we ate and soon after everyone went home.
After the cake issue I wondered why I even bother.
I’d like to read about more birthday parties such as the one Paul Collins (2004) re-
lated in his recently published book, Not Even Wrong: Adventures in Autism:
There’s one couple in Los Angeles with a son obsessed by all things relating to
trash and recycling. He has memorized the garbage collection routes, the
makes and types of disposal vehicles, and he talks of little else. So they
arranged with the local garbage men to have a seventh birthday party for him
out at the local landfill. The Los Angeles Times sent a reporter to cover it, bliss-
fully unaware that perhaps this boy was—well, even more different than he
seemed. “We don’t know where this interest in trash came from,” they quoted
the boy’s mother. “He’s been this way since he was 2.” But both parents say
they are fine with him spending his life working with trash, if that’s what
makes him happy.
Rather than reading the following opinion from a mother on www. epinions.com
(Wendywitch, 2004):
I hate that I have to drive her to therapy twice a week and go to IEP meetings.
I wanted tea parties, I got speech therapy. My dreams have become to make her
an independent adult, when they started out as having a daughter winning a
Nobel Prize or a Pulitzer. I envy parents who can take their children to Disney
World or to the movies.
I’d like to hear about more parents like Nancy Alar, who shared on the video,
Straight Talk about Autism with Parents and Kids: Childhood Issues (1998), some fea-
tures of her reciprocal relationship with her teenage son, Matthew Ward:
Last year he got interested in the gods of Egypt; who knows why. And we don’t
know where this came from, this absolute intense interest in hairless dogs. We
don’t know why hairless dogs. But, my husband and I are cat people. We now
have a hairless dog.
In each of these alternate scenarios, the parents’ behaviors embodied an attitude of
reciprocity. As Greenspan and Weider (1998) have warned, “This can be hard. It’s nat-
ural to want to take over . . . You need to remind yourself to fight this tendency. Your
child will take the most pleasure in activities he chooses himself” (p. 140). Without
embodying an attitude of reciprocity and working toward a behavior of reciprocity, it
is unlikely that enjoyment will be defined by reciprocity, that is, “experienced or felt
by both sides” (American Heritage Dictionary of the English Language, 2000).
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Book Review
Barbara J. King
Primates, Parenting, and Plasticity
Parenting for Primates

by Harriet J. Smith, Harvard University Press, 2005
One hot summer day, infant Rosie was trying to get herself from an outdoor area,
where she was baking in the full sunshine, to an indoor room with air-conditioning. To
do this, she needed to lift up a flap covering a small door, but the flap was too heavy
for her to manage. Rosie began to make sounds of distress. Hearing these, Rosie’s
Dad, Joe, roused himself from the shade of a peach tree, walked over, and lifted the
flap for his daughter. As Rosie went indoors, Joe headed back to his patch of shade.
Why open a review of a book on parenting by highlighting an event of such a rou-
tine nature? Joe and Rosie are not humans; they are cotton-top tamarins, small mon-
keys that come from South America. And when Rosie was born, in captivity four
months before the door-flap incident, things hadn’t gone smoothly at all. Rosie’s
mother, Chartier, and dad Joe, rejected her and her sibling Ira (tamarins give birth to
twins).
When he helped Rosie escape the summer heat, then, Joe acted like a good Dad
not because he’s a tamarin and that’s what all tamarins do, or because his genes had
programmed him for paternal care. He did so because he had gained experience at
good parenting, through Harriet Smith’s self-devised, in-home monkey parenting pro-
gram. Joe had been hand-reared by Smith in the early 1970s, and thus had grown up
without benefit of knowing how tamarins are supposed to raise their young. When he
matured enough to mate and father offspring, Joe, together with his mate Chartier,
forcefully rejected several sets of twins, monkeys that then had to be handraised also
by Smith.
Parenting for Primates is Smith’s account of how tamarin-raising led her to under-
stand that nonhuman primates learn to be good parents from experience, and can over-
come even a rocky start as Joe did. Her account of how she broke the cycle of poor
parenting makes absorbing reading. Because Smith is not only a monkey-observer but
also a clinical psychologist, her main point is to show that what is true for Joe,
Chartier, Rosie, and Ira, can be true for a human family as well.
In addition to thinking across species about parenting, Smith thinks cross-culturally:
“Training for parenthood is by apprenticeship for both boys and girls in most pre-
industrial societies. . . . This process of experience first, parenting second, is reversed
in contemporary Western culture: we marry and establish our households first, and
153
154 BARBARA J. KING
then get our childcare training on the job. Both mothers and fathers may be in the same
boat, if neither have babysat younger siblings or other young children, and both may
question their abilities as parents when parenting doesn’t come ‘naturally.’”
Fathers may be particularly disadvantaged by this lack of experience: “Fathers,
whose role with infants has long been considered optional, may have little desire at
first to become involved. They step aside while their wives become competent moth-
ers by trial and error, with a little advice from family or experts thrown in.” Yet re-
search shows clearly that “[w]hen fathers start taking care of their babies, the babies’
responsiveness increases” (pp. 104–105).
Smith conveys many valuable lessons about the healthy emotional development of
human children in a family setting. The crux of her message is this: “Adequate par-
enting increases our chances of ensuring our own ‘immortality’: when our offspring
grow up and reproduce, they pass on our genes to future generations. And yet, the fas-
cinating and complex ways in which primate parenting behavior varies with charac-
teristics of the environment, the social context, and individual experience shows us
that parenting behavior is not totally determined by our genes. The flexibility and mal-
leability of primate parenting behavior reveal that we have the ability not only to
change our behavior but to make conscious choices about the kinds of parents we wish
to be” (p. 11).
This last sentence is one I could have borrowed for my editorial in this inaugural
issue of the Journal of Developmental Processes. Smith’s perspective on parenting
emerged from an unusual career trajectory. First earning a PhD in comparative prima-
tology, Smith carried out research on cottontop tamarins in the laboratory. For the next
30 years, she kept a colony of these monkeys at her home. (Smith makes a point of
saying that “monkeys, like other wild creatures, should not be kept as pets,” so the
book is a bit steeped in a do what I say, not what I do framework.) From that base,
Smith went on to earn a post-graduate degree in clinical psychology, establishing a
practice with, of course, human clients.
This blended background is both a strength and weakness of the book. Many
primate-related books focus on chimpanzees, bonobos, or gorillas—the African great
apes. This makes good sense given that these apes are humans’ closest living relatives,
yet it is refreshing to find a popular counterpart to the work done by researchers such
as Jeffrey French, Charles Snowdon, and John Terborgh in the world of tamarin and
marmoset academic research. Twin-birthing, family-living mini-monkeys are the per-
fect exemplars for Smith’s point about primate plasticity.
It’s a strength as well that Smith continues on from a discussion of primate infancy
to encompass juvenility and adolescence. It’s not all about the cute phase. Smith freely
offers opinions on contentious matters. One example: “That human adolescents are fas-
cinated with sex is a normal, healthy reflection of their primate heritage,” followed by
advice for how parents may enable their teenagers to resist temptation (p. 204). An-
other: “A family with more than one capable adult sharing the responsibility for chil-
dren, regardless of gender, has a better chance of positive outcome” (p. 298); of course,
she means the parents’ gender—not the children’s—in a welcome advocacy for loving
families of all kinds.
Book Review 155
Indeed, Smith zeroes in on societal patterns that affect parenting. Citing statistics
about dual-career couples and working mothers, she notes that in some cases daycare
is not a preference but a necessity, and laments the resources available: “Almost half
a million childcare workers (mostly women) are paid less than workers in 99 percent
of occupations in the United States today. The low pay offered to young females who
work in daycare centers in the United States sends the message that there is almost no
job less important than childcare” (p. 131). This matters, of course, because stable and
long-term relationships between babies and caregivers matter: “A baby’s best chance
for receiving quality care is having a babysitter that knows him, likes him, and wants
to please him. . . Quality daycare given by nonkin babysitters does not have to be a
contradiction in terms” (p. 132).
Yet I can’t give the book a pure rave. Comparative primatology is a good thing, but
can be pushed too far, as when Smith jumps effortlessly from human to New World
monkey behavioral patterns: “At the extremes of human fatherhood are titi-like fathers
(albeit very few) who are their children’s primary caretakers, and squirrel monkey-like
fathers, who play no role in their children’s development after conception” (p. 87). A
flat conflation of fathering in a species that is well-adapted and clever with fathering in
a species that creates linguistic-cultural norms made me quite uneasy.
Further, readers may sense that the book is dated. Smith reports quite a number of
older studies, still valuable, but there’s a somewhat stale flavor to some of the analy-
sis. Primatologists have described far too much variation in social organization within
species for terms like “harem” (for gorillas) or “solitary” (orangutans) to be relevant
any longer. It is simply incorrect to assert that no nonhuman primate females undergo
menopause. And to say that “twenty years ago, most of the thinking about primate be-
havior was based on studies of rhesus monkeys and other macaques” (p. 95) is strange,
given that ape fever had gripped primatology by the mid-1980s and much was flow-
ing to us from long-term studies of chimpanzees, gorillas, and orangutans, not to men-
tion baboons and other non-macaque monkeys. Suffice to know that although Smith
thanks various primatologists for reading chunks of the manuscript, an overall keen,
and scientific, editing eye was still needed.
More significantly, Smith does not always give the book’s topics the depth of cov-
erage they deserve. Some of most exciting work in parenting is not just about top-down
socialization, but about fully contingent and co-created behavior understood through a
dynamic-systems perspective. The notion of the family as a system, with a change in
one part affecting all, so that mutual transformation is possible, informs works rang-
ing from Murray Bowen’s seminal Family Therapy in Clinical Practice to Fivaz-
Depeursinge and Corboz-Warnery’s The Primary Triangle to Stanley Greenspan and
Stuart Shanker’s The First Idea—and indeed articles in this first issue of JDP.
As the examples I have chosen indicate, Smith veers toward a systems understand-
ing, in which each partner affects the other within a family, and in which the larger so-
ciety affects the family. I appreciated, for instance, her discussion of the concept of
micro-environment (p. 352), the idea that each child’s developmental trajectory is
affected by a constellation of factors in his or her environment (including the genetic
environment). What I missed was an appreciation that this isn’t just one partner or one
156 BARBARA J. KING
level of society affecting another in a certain environment, but two partners negotiat-
ing and co-creating behavior and meaning, and family and society mutually construct-
ing each other.
Still, Smith’s message is very much needed in a gene-besotted society. KNOW
YOUR DNA, blares a headline on Scientific American’s front cover (January 2006).
The subtitle is: Inexpensive gene readers will soon unlock the secrets in your personal
double helix. Harriet Smith’s thesis is that the most fascinating secrets of primate par-
enting lie not in DNA but the complex world of social plasticity and nurturing. When
Joe, the tamarin Dad, got up from the shade on a hot day, his exemplified this point to
his daughter Rosie; through Smith, we all benefit from his message.
Journal of Developmental Processes
Submission Guidelines
Description
The goal of the Journal of Developmental Processes is to provide a vehicle for
research and clinical studies that advance knowledge of the complexity inherent in all
developmental processes. The JDP encourages exchange of ideas across fields including,
but not limited to, animal behavior, anthropology, biology, education, linguistics, neuro-
science, occupational and speech and language therapy, primatology, psychiatry, psychol-
ogy, public policy, sociology, and social work.
The Journal is interested in both experimental and descriptive studies, including
basic research, detailed case reports, ethnographic analysis, and theoretical explorations.
Particularly welcome are innovative conceptual frameworks and methods that capture the
complexity of developmental processes as well as assessment procedures and interven-
tions that enable children and families to overcome mental health, developmental, social,
and learning challenges.
Submissions
Send queries and submissions on clinical aspects and applications to Asso-
ciate Editor Ira Glovinsky at ira1834@sbcglobal.net; all other queries and submissions,
and books for potential review, should go to Editor Barbara J. King at bjking@wm.edu
or Department of Anthropology, College of William and Mary, Williamsburg, VA, USA,
23187-8795.
Please submit manuscripts electronically, preferably in Microsoft Word® format.
Length is negotiable with the editor, but generally should not exceed 50 manuscript pages,
including references. Submit your contact information, including phone, fax, and postal
mailing address. Also enclose a cover letter indicating that the article has not been pub-
lished, and is not under consideration elsewhere.
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References
References should be listed in alphabetical order. Each listed reference should be cited To purchase a copy of the Journal of Developmental Processes
in the text, and each text citation should be listed in the References. We follow the APA or to subscribe to future issues,
style, e.g.,
please visit www.icdl.com
Greenspan, S. I., & Shanker, S. G. (2004). The first idea: How symbols, language, and or call 301-656-2667 for information
intelligence evolved from our primate ancestors to modern humans. Cambridge,
MA: Da Capo.
Greenspan, S. I., & Shanker, S. G. (2005). Developmental Research. In E. S. Person,
A. M. Cooper, & G. O. Gabbard, American psychiatric publishing textbook of psy-
choanalysis (pp. 335–360). Washington, DC: American Psychiatric Publishing.
Greenspan, S. I., & Wieder, S. (1997). Developmental patterns and outcomes in infant and
children with disorders in relating and communicating: A chart review of 200
cases of children with autistic spectrum diagnosis. Journal of Developmental and
Learning Disorders, 1, 87–141.
Volume 1 Fall 2006
The
Journal

of
Developmental
Processes
Sponsored by the Interdisciplinary Council on

Developmental and Learning Disorders (ICDL),
the Council of Human Development, and the
Milton and Ethel Harris Research Initiative
www.icdl.com
www.councilhd.ca
www.mehri.ca
Vol. 1 Fall 2006
ISBN number: 0-9767758-4-0

JDPJournal Fall 2006

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Volume 1 Fall 2006

The Journal of Developmental Processes

Sponsored by the Interdisciplinary Council on

ISBN number: 0-9767758-4-0

Introductory Notes—Stanley I. Greenspan 1

A Welcome, and an Invitation, from the Editor—Barbara J. King 3

Dynamic Systems Research on Interindividual Communication:

Early Family Trauma and the Ontogeny of Glucocorticoid Stress

The Development of Spontaneous Gestures in Zoo-living Gorillas

The Kids Are Alright: Maternal Behavioral Interactions and Stress

The Literacy of Interaction: Are Infants and Young Children Receiving

Toward a Behavior of Reciprocity—Morton Ann Gernsbacher 138

Book Review: Parenting for Primates—Barbara J. King 153

Bethesda, Maryland Copyright © 2006

JDP Editorial Board

Barbara J. King, Editor

Capturing the continuous processes of change inherent in development, those stem-

The central mission of the Journal of Developmental Processes is to reflect, and to

The Paradox of Change and the Role of the Observer

of romantic partners, for example, sometimes kisses, sometimes hugs, sometimes

The Conceptualization of Change in Dynamic Systems Theory

Sequence vs. Process at the Microlevel (Level 1 Change)

Sequence vs. Process at the Macrolevel (Level 2 Change)

Sequence vs. Process in Developmental Change (Level 3 Change)

Dynamic Systems Methods for the Study of System Change

Microgenetic Research Designs

Qualitative Research and the Role of the Observer

makes an interpretation. If the original hypothesis needs to be altered, the researcher

Conclusions and Implications

Sample and methods: A longitudinal eighteen-year study (1988–2006) of child health in

Summary and conclusions: Grandparents appear to have significant mediating effects on

Introduction: Grandparenting as an Evolved Human Adaptation

The Paradox of Psychosocial Stress

HPA Stress Response to Social Events

FIGURE 1. Morning, mid-morning, and afternoon cortisol levels of Danny

Evolution of the Extended Family

Stress Hormone Profiles as an

muscle tissues, neuropeptide directed immune response, modulation by antiglucocor-

Social Worlds and the Ontogeny

Methods and Field Techniques

Cortisol Response to Naturally Occurring Social Challenges

FIGURE 2. On June 28, 1992, a serious marital conflict erupted in the

FIGURE 3. Household composition and average cortisol levels of children. Vertical

Ontogeny: The Early Trauma → HPA Dysfunction Hypothesis

Cortisol (standardized) 1.0

No EFT in utero 0–3 3–6

Age of first major trauma

FIGURE 5. Ten-hour cortisol profile of a 12-year-

Ameliorative Effects of Grandparental Care

Controls EFT children EFT children

Controls EFT children EFT children

Controls EFT children EFT children

Controls EFT children EFT children

Bowlby, J. (1969). Attachment. New York: Basic Books.

Abstract: We analyze the developmental sequence in which different types of representa-

Untaught Signs by Koko and Michael

Table 1. Referents of Koko’s Untaught Signs (First 10 Years)

Browse Eye makeup Frown

Unattention Bite Hair barrette

Plate 1. Some of Koko’s untaught signs

From Action to Object in the Creation of Gestures and Signs:

8. For more about gesture phrases, see Tanner 2004.