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Behavioral and Physiological Responses

to Child-Directed Speech as Predictors


of Communication Outcomes in Children
With Autism Spectrum Disorders

Linda R. Watson
Grace T. Baranek
Purpose: To determine the extent to which behavioral and physiological responses
Jane E. Roberts
during child-directed speech (CDS) correlate concurrently and predictively with
Fabian J. David
communication skills in young children with autism spectrum disorders (ASD).
Twyla Y. Perryman Method: Twenty-two boys with ASD (initial mean age: 35 months) participated in a
The University of North Carolina longitudinal study. At entry, behavioral (i.e., percentage looking) and physiological
at Chapel Hill (i.e., vagal activity) measures were collected during the presentation of CDS stimuli.
A battery of standardized communication measures was administered at entry and
readministered 12 months later.
Results: Percentage looking during CDS was strongly correlated with all entry and
follow-up communication scores; vagal activity during CDS was moderately to
strongly correlated with entry receptive language, follow-up expressive language,
and social-communicative adaptive skills. After controlling for entry communication
skills, vagal activity during CDS accounted for significant variance in follow-up
communication skills, but percentage looking during CDS did not.
Conclusions: Behavioral and physiological responses to CDS are significantly related
to concurrent and later communication skills of children with ASD. Furthermore,
higher vagal activity during CDS predicts better communication outcomes 12 months
later, after initial communication skills are accounted for. Further research is needed
to better understand the physiological mechanisms underlying variable responses
to CDS among children with ASD.
KEY WORDS: autism spectrum disorders, preschool children, attention, outcomes

A
s a group, children with autism spectrum disorders (ASD) are
at high risk for severe delays and lifelong impairments in broad
aspects of language competency (Lewis, Murdoch, & Woodyatt,
2007; Loucas et al., 2008; Mawhood, Howlin, & Rutter, 2000). Early inter-
vention to facilitate language development among young children with
ASD is recommended because of the strong associations between lan-
guage skills and later functional outcomes (Luyster, Qiu, Lopez, & Lord,
2007; Szatmari, Bryson, Boyle, Streiner, & Duku, 2003; Venter, Lord, &
Schopler, 1992). Recently, the links between prelinguistic communication
and later outcomes of children with ASD have garnered more attention.
An increased understanding of prelinguistic factors that predict pre-
school language development in children with ASD could lead to im-
proved communication assessment and early intervention strategies in
this population.

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One striking, replicated finding related to the pre- This behavioral response pattern to CDS is associ-
linguistic development of children with ASD documents ated with enhanced neural responses and more efficient
their low behavioral responsiveness to speech. Infants learning of some language features than occurs when
and toddlers with ASD are less responsive to a name call children are exposed to speech that does not have CDS
(Baranek, 1999; Lord, 1995; Osterling, Dawson, & Munson, features.
2002) and do not show the expected preferences for moth-
er’s voice and child-directed speech (CDS) over other stim-
uli (Klin, 1991; Kuhl, Coffey-Corina, Padden, & Dawson,
Impairment of Attention to CDS
2005; Paul, Chawarska, Fowler, Cicchetti, & Volkmar, in Children With ASD
2007). The implications of this limited responsiveness As noted, children with ASD do not attend to CDS
for later language and social-communicative outcomes to the extent that other young children do. Diminished
may be significant. Response to CDS can be measured attention to CDS among these children will reduce their
both behaviorally and physiologically, to capture differ- opportunities to benefit from its unique features. What
ent aspects of attention quality. The purpose of this arti- may explain decreased attention to CDS among children
cle is to examine concurrent and predictive associations with ASD? Some explanations may lie in the different
of behavioral and physiological responses during CDS components of attention that could be impaired when
with language and social-communication skills of chil- children with ASD are exposed to CDS. A primary com-
dren with ASD. To provide important background for ponent of attention is orienting, which is conceptualized
the study, we review the characteristics of CDS along as an involuntary, reactive phase of attention that oc-
with its relation to child language acquisition, the evi- curs immediately following the onset of a novel stimulus
dence for decreased attention to CDS among children (Posner & Petersen, 1990; Richards, 1987). In terms of
with ASD, vagal activity measures as physiological in- neurological processing, orienting has been associated
dexes of attention quality, and the vagal system in chil- with a more posterior brain system (Posner & Petersen,
dren with ASD. 1990). The tendency of children with ASD not to respond
reliably or promptly to a name call (and other forms of
CDS) likely reflects deficits in orienting. Obviously, ori-
CDS enting to stimuli is an important step in sensory process-
CDS is characterized by many differences when com- ing and attention, and the fact that children with ASD do
pared with adult-directed speech, including higher pitch, not orient quickly and reliably may result in less time
greater pitch range, shorter sentences, elongated vowels, spent attending to CDS over time. Even if a child with an
more repetition, less diversity in vocabulary, and more ASD initially orients to CDS, a limited maintenance of
references to the here and now (for a review, see Pine, attention likely would prevent that child from accruing
1994). CDS is posited to play several important roles in benefits from exposure to CDS.
child–caregiver interactions. First, the features pro- Beyond reactive orienting, the maintenance of atten-
mote the affective relationship between adults and young tion to particular stimuli is considered voluntary and has
children (Trevarthen & Aitken, 2001), as supported by been associated with a more anterior brain system that
findings that infants show more positive affect in re- regulates attention through cognitive control (Posner &
sponse to CDS than to adult-directed speech (Fernald, Petersen, 1990; Richards, 1987). In this investigation we
1993; Werker & McLeod, 1989). Second, CDS selectively examined individual variability among young children
engages the attention of typically developing children, with ASD in sustaining attention to CDS, with the as-
who prefer CDS to adult-directed speech as early as sumption that such sustained attention will underlie the
1 month of age (e.g., Cooper & Aslin, 1990) and continue learning necessary for effective social-communicative func-
these preferences into the toddler (Kuhl et al., 2005; tioning. This assumption is supported by the findings
Paul et al., 2007) and preschool years (Klin, 1991). In of two investigations involving young participants with
addition to enhanced attention, infants show enhanced ASD. In a study of preschoolers conducted by Kuhl et al.
neural responses to words spoken with intonations asso- (2005), a subgroup of children with ASD who preferred
ciated with CDS compared with the intonations used in CDS to a nonspeech analog showed better performance
adult-directed speech (Zangl & Mills, 2007). The third in a speech discrimination task than their counterparts
important role is that CDS appears to enhance children’s with ASD who preferred to listen to nonspeech stimuli.
language learning. For example, recent evidence dem- Another recent study of toddlers with ASD found sig-
onstrated that features of CDS assist infants in detecting nificant concurrent and predictive relations between at-
word boundaries (Thiessen, Hill, & Saffran, 2005) and in tention to CDS and receptive language abilities (Paul
learning language-specific phonetic categories (Werker et al., 2007). In the predictive analyses, however, Paul
et al., 2007). Thus, children seem to respond to CDS by et al. (2007) did not partial out the association between
preferentially attending to it in a context of positive affect. receptive language at age 2 and receptive language at

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age 3, leaving open the possibility that attention to CDS risk factors. In general, then, a higher resting RSA is as-
does not account for any unique variance in later lan- sociated with more positive developmental and social-
guage skills once initial language levels are taken into emotional outcomes.
account. Thus, the degree to which attention to CDS ac- Recent work has focused on the adaptive function of
counts for later language skills in children with ASD is vagal cardiac control in response to challenge. According to
not yet clear. Porges’s (1995b) polyvagal theory, sensitive adjustments
in vagal input to the heart, both up and down, provide
an individual with the physiological resources needed to
Physiological Bases of Attention engage appropriately with the environment in the face
Attention skills, like all behaviors, have underlying of changing demands. Polyvagal refers to the two differ-
physiological bases that can be measured and examined ent branches of the vagus, that is, (a) the myelinated and
for variability. For example, behavioral indications of phylogenetically more recent ventral vagal complex and
sustained attention, such as quieting and looking, are (b) the unmyelinated and phylogenetically older dorsal
associated with physiological changes, such as a slowing vagal complex. Porges (2007) argued that the ventral va-
of heart rate. Researchers have concluded that heart rate gal complex is linked to behavioral functions of social
changes during attention are mediated more by the para- communication, self-soothing, and calming. He further
sympathetic (i.e., rest–digest) than the sympathetic (i.e., argued that RSA largely reflects the influences of the
fight–flight) system (Richards & Casey, 1991). The in- ventral vagal complex on the heart and that the vagus is
fluences of the parasympathetic system on the heart part of a complex neurophysiological system involving
often are studied through measuring respiratory sinus bidirectional influences between the cortex and brain-
arrhythmia (RSA) as an index of vagal activity. In a stem operating in the service of social engagement. Social
resting state, heart rate varies depending on the phase affiliative responses to another person require sustained
of the respiratory cycle, with an increase in heart rate on attention, which is accompanied by decreased heart rate
inspiration and a decrease in heart rate on expiration. and greater vagal cardiac control. In contrast, in challeng-
The difference between the heart rate during inspiration ing, stressful, or threatening encounters vagal control of
versus expiration reflects the extent of influence of the the heart is diminished or withdrawn and sympathetic
vagus nerve in regulating the heartbeat. A larger differ- nervous system influences accelerate the heart rate as
ence (i.e., higher RSA) presumably reflects higher vagal the individual reacts with a fight–flight response. A
activity, and a smaller difference (i.e., lower RSA) pre- number of studies support Porges’s (1995b) theory in that
sumably reflects lower vagal activity. increased vagal regulation has been associated with bet-
Higher RSA under nonchallenging, calm conditions ter social skills and fewer behavior problems (Calkins
has been associated concurrently and prospectively with & Keane, 2004; Doussard-Roosevelt, Montgomery, &
a variety of child behavioral characteristics. For exam- Porges, 2003) and a greater capacity for focused attention
ple, in infancy a higher baseline RSA is associated with (Bornstein & Suess, 2000). Most studies of vagal regula-
more emotional reactivity, including more crying in re- tion have compared baseline RSA with conditions involv-
sponse to mildly frustrating events and positive affective ing negative stressors or cognitive challenges to determine
reactivity to social interactions; longitudinally, a higher the extent to which vagal influences on the heart are
baseline RSA in infancy predicts greater sociability dur- suppressed in response to challenges. When studies have
ing the toddler and preschool years (e.g., Fox, 1989; Porges, contrasted negative social stressors with positive so-
Doussard-Roosevelt, Portales, & Suess, 1994). Beauchaine cial interactions, however, results have indicated that
(2001) suggested that RSA in infancy reflects the infant’s RSA decreases in response to negative social stressors
capacity for engagement with the environment, with and increases in response to positive social interactions
high RSA associated with greater behavioral, attentional, (Bazhenova, Plonskaia, & Porges, 2001; Doussard-Roosevelt
and emotional responsiveness. Thus, high levels of in- et al., 2003). Therefore, levels of and change in RSA (both
fant responsiveness can be evidenced in more extreme increases and decreases) can index a child’s awareness of
negative and positive emotional reactions but lead to the environment; affective reactions to the environment;
better adaptation over time. Among preschoolers, higher and, potentially, responsiveness to CDS.
resting RSA is related to higher concurrent social com-
petence, better emotion regulation, and lower levels of
problem behavior (Blair & Peters, 2003; Calkins, 1997;
The Vagal System and ASD
Doussard-Roosevelt, McClenny, & Porges, 2001; Porges Existing work suggests that children with ASD have
et al., 1994). As Beauchaine, Neuhaus, Brenner, and reduced levels of resting RSA compared with control chil-
Gatzke-Kopp (2008) discussed, greater vagal influences on dren (Ming, Julu, Brimacombe, Connor, & Daniels, 2005),
the heart also appear to protect children from developing as well as diminished vagal adaptation to tasks with cog-
psychopathologies associated with varying environmental nitive demands (Althaus et al., 2004; Toichi & Kamio,

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2003). Participants in these studies have been school-aged and nondemanding. We posited that RSA during the
children and older adolescents; thus, the generalizabil- nonsocial condition would not reflect the child’s inclina-
ity of these findings to toddlers or preschoolers with tion to respond to CDS positively, whereas RSA during
ASD has not been determined. Sigman and colleagues CDS would index the extent to which a child attends to
(Sigman, Dissanayake, Corona, & Espinosa, 2003) found CDS with a positive affective response (cf. Beauchaine
that preschool children with autism did not differ from et al., 2008). We propose that this physiological measure
children with other developmental delays in their amount reflects a qualitative dimension of the child’s attention
of looking at videos of a baby crying versus a baby play- to CDS that will influence his or her tendency to learn
ing happily, and they did not differ in heart rate in re- efficiently from exposure to CDS.
sponse to the two videos; however, these investigators did
not measure RSA, which is considered to be a better index
Research Question 2: Are behavioral
of vagal cardiac control than is heart rate. No previous
research has examined the extent to which variability in
or physiological responses during CDS
RSA among young children with ASD may predict later or nonsocial stimuli predictive of
social-communicative outcomes. communication outcomes in young children
with ASD 1 year later, after controlling for
Purpose of This Study initial communication skills?
The overarching focus of this study was the associa- We formulated the following two hypotheses:
tion between behavioral and physiological responses to Hypothesis 2a. Looking during CDS stimuli (but not
CDS on the one hand, and concurrent and later commu- during nonsocial stimuli) will account for a significant
nication skills in young children with ASD on the other amount of variance in communication outcomes 1 year
hand. We chose to measure these responses under non- later, with a greater amount of looking during CDS pre-
demanding conditions, corresponding to descriptions of dicting better communication outcomes.
CDS as studied in other research; that is, the special Hypothesis 2b. RSA during CDS stimuli (but not dur-
features of CDS are assumed to arise in part from adults’ ing nonsocial stimuli) will account for a significant amount
efforts to establish positive affective relations with a young of variance in communication outcomes 1 year later, with
child. Furthermore, we included a contrasting nonsocial higher RSA during CDS predicting better communication
condition judged as likely to engage the children’s at- outcomes.
tention in order to test the specificity of behavioral and
Our rationale was the following: Although adults
physiological measures collected during CDS as predic-
decrease in the extent to which they use features of CDS
tors of language outcomes. Our research questions were
as children grow older and their language production and
as follows:
comprehension skills become more sophisticated (e.g.,
Snow, Perlman, & Nathan, 1987), we assumed that these
Research Question 1: What is the relationship
children, whose skills were initially at or below a 24-month
of behavioral and physiological responses language age equivalent (AE), were at a stage of lan-
during CDS or nonsocial stimuli guage acquisition at which the special features of CDS
to concurrent communication skills would continue to have a beneficial impact, if the chil-
in young children with ASD? dren attended to CDS. Thus, we hypothesized that the
quantity of attention to CDS (measured behaviorally by
We formulated the following two hypotheses:
means of looking) and quality of attention to CDS (mea-
Hypothesis 1a. Amount of looking during CDS stim- sured physiologically by means of RSA) would each have
uli (but not during nonsocial stimuli) will be positively a positive association with outcomes 1 year later, even
correlated with concurrent measures of communication after controlling for initial language abilities.
skills.
Hypothesis 1b. Vagal tone during CDS stimuli (but
not during nonsocial stimuli) will be positively correlated Method
with concurrent measures of communication skills.
Our rationales for the hypotheses were as follows.
Participants
First, a child who looks more during CDS stimuli has Twenty-two boys diagnosed with ASD participated
more opportunities to benefit from its features, and to as- in this longitudinal study (see Table 1). Inclusion criteria
sociate words with the objects or events they represent, included an existing diagnosis of autism by a licensed
and thus is likely to have better communication and lan- psychologist or physician, an expressive communica-
guage skills. Second, both the nonsocial and CDS con- tion AE of less than 24 months at entry, absence of a co-
ditions in this study were designed to be nonstressful occurring condition (neurological or genetic disorder,

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Table 1. Participant characteristics. total number of words understood was one component
of the receptive language aggregate score, and the total
Characteristic M SD Range number of words said was one component of the expres-
sive language aggregate score.
Chronological age (months) 35.0 4.28 28–42
PLS–4 language age (months) 11.68 6.43 3–22 The Preschool Language Scale, Fourth Edition
PLS–4 standard score 54.32 7.51 50–76 (PLS-4; Zimmerman, Steiner, & Pond, 2002), is a stan-
MSEL ELC 51.09 3.79 49–63 dardized observational assessment of a child’s receptive
VABS ABC 57.82 6.95 49–74 and expressive language from birth through 6 years,
11 months. It is composed of two subscales: (a) Auditory
Note. N = 22. PLS–4 = Preschool Language Scale—4th Edition; MSEL
Comprehension and (b) Expressive Communication.
ELC = Mullen Scales of Early Learning Early Learning Composite; VABS
ABC = Vineland Adaptive Behavior Scales Adaptive Behavior Composite. The Mullen Scales of Early Learning (MSEL; Mullen,
1995) is a standardized, individually administered assess-
ment that measures the developmental level of children
from birth to 68 months. The MSEL includes five domains:
e.g., Rett syndrome, tuberous sclerosis, or fragile X), and (a) Gross Motor, (b) Visual Reception, (c) Fine Motor,
vision and hearing acuity within normal or corrected (d) Receptive Language, and (e) Expressive Language.
normal ranges. Autism diagnoses were confirmed at study An Early Learning Composite standard score can be de-
entry with the Autism Diagnostic Observation Schedule rived that reflects an overall level of functioning across
(Lord, Rutter, DiLavore, & Risi, 1999) and the Autism domains, based on a mean of 100 and a standard devia-
Diagnostic Interview—Revised (Rutter, LeCouteur, & tion of 15; the lowest standard score provided is 49.
Lord, 2003). Twenty participants met the cutoff for au-
tism on both confirmatory measures; 2 additional sub- The Vineland Adaptive Behavior Scales (VABS;
jects met the cutoff for autism spectrum on the Autism Sparrow, Balla, & Cicchetti, 1984) is a standardized,
Diagnostic Observation Schedule. semistructured survey interview form designed to assess
personal and social skills needed for everyday living. The
The chronological age of the 22 participants (all
VABS can be used to assess functioning for a large age
boys) at entry ranged from 28 to 42 months. Nineteen of
span (infants to adults) in four major areas: (a) com-
the boys participated in the longitudinal follow-up assess-
munication, (b) daily living skills, (c) socialization, and
ment at ages 40 through 55 months; the remaining three
(d) motor skills. In addition to separate scores for the ma-
families were unavailable at follow-up because of health-
jor areas, the VABS yields an overall composite standard
related issues with the participant or other family mem-
score, the Adaptive Behavior Composite, which has a
bers. The mothers of 18 participants (82%) self-identified
mean of 100 and a standard deviation of 15. The lowest
as European American, non-Latino, and the mothers of
standard score provided is 20. We used scores from the
4 participants (18%) self-identified as African American.
Socialization and Communication scales to calculate an
In terms of highest level of education completed, 45%
aggregate measure of social-communicative adaptive skills.
of the mothers had a 4-year undergraduate or graduate
These two areas of adaptive behavior are conceptually
degree, 14% had an associate’s degree, and 41% had a
high school diploma or equivalent. most closely related to the core deficits in autism, and
empirically they were strongly correlated (r = .80) with
one another in this sample.
Measures
Responses to nonsocial and CDS stimuli. The non-
Communication skills. We used the four measures social and CDS stimulus conditions used in this inves-
listed next to derive aggregate scores of each participant’s tigation are described in Table 2. These conditions were
communication skills at entry and at follow-up in the fol- presented to each participant in the same order. The non-
lowing three categories: (a) receptive language, (b) expres- social condition, a video of music accompanied by move-
sive language, and (c) social-communicative adaptive skills. ment of inanimate toys as well as visual patterns, provided
(See the Procedure section for the derivation of aggregate a combination of visual and auditory stimuli and thus
scores.) was generally comparable in format to the CDS condi-
The MacArthur–Bates Communicative Development tions. The nonsocial condition was presented for 2 min,
Inventory, Words and Gestures form (CDI:WG; Fenson to provide sufficient time to collect RSA data while also
et al., 1993), is a standardized parent report tool for as- keeping the time relatively brief to maximize the num-
sessing an array of communicative skills in children from ber of children who would sit through the procedure. The
8 to 18 months of age, including receptive and expressive three CDS conditions were developed as a short battery
vocabulary. Because the participants in this study were of different 1-min samples of CDS with the aim of gener-
chronologically older than the normative sample for the ating more stable estimates of relative looking and RSA
CDI:WG, we used only raw scores for analyses. The during exposure to CDS than might be obtained from the

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Table 2. Experimental session of nonsocial stimuli and child-directed speech (CDS).

Stimulus Duration (min) Type Description of stimulus

Baby Bach video 2 Nonsocial Children’s music video with no social stimuli
Name call 1 Social Up to 5 name call trials while Baby Bach video
continued to playa
Video story 1 Social Video of a female actor reading out of a novel
storybook, as if reading to the child (book
facing outward, actor directly facing camera)
Puppet show 1 Social Live puppet show performed by female examiner
Nonsense toy 1 Social Video of a female actor playing with and describing
a novel toy using nonsense words

a
Data not analyzed for this study.

use of a single CDS sample. The behavioral measure of language), and then the assessment was scheduled. Par-
responses to the stimuli was the proportion of the time ents received a packet by mail that included consent forms,
the child sustained looking at the target stimuli. Brief rating scales, demographic and service information, and
glances at the stimuli were not included; instead, sus- sample electroencephalography electrodes to use to fa-
tained looking was coded only when the child looked for miliarize the child participant with this aspect of the
a duration of at least 2 consecutive seconds. We calcu- study procedures. Completed forms and questionnaires
lated two behavioral variables of responses to the stim- were collected when the family came to the research lab-
uli: (a) percentage of time spent in sustained looking oratory for the assessments. The project was approved
during the nonsocial condition and (b) percentage of time by the institutional review board at The University of
spent in sustained looking during CDS conditions. North Carolina at Chapel Hill.
The nonsocial and CDS conditions in this study were Entry assessments were typically conducted across
comparable to conditions used in other studies of young two sessions to maintain the attention and cooperation
children that have measured resting RSA during pas- of the child; all assessments were completed within a
sive exposure of children to a video or storybook read- 30-day window. Research staff administered the stan-
ing (e.g., Blair & Peters, 2003; Calkins, 1997; Perlman, dardized assessments involving direct interaction with
Camras, & Pelphrey, 2008). Physiological responses to the child in a child-friendly assessment room with child-
the stimuli were indexed by RSA during both the non- sized furniture. Interviews with parents were completed
social condition and the CDS conditions. RSA was com- either at the laboratory or over the telephone, depending
puted from continuous records of heart activity measured on the preference of the family.
in interbeat interval units (see Procedure section). Heart For the experimental session, two surface electrodes
activity was collected using the Mini-Logger 2000 (Mini were placed on the child’s chest and attached via leads to
Mitter Company, Inc.). a small Mini-Logger transmitter unit, which was then
placed in the child’s pocket or a waist pack. The interbeat
intervals of the child’s heart beat were detected by the
Procedure electrodes and transmitted to a Mini-Logger receiver
Participants were recruited from two sources asso- unit located within 3 ft of the child. A marker switch was
ciated with The University of North Carolina at Chapel connected to the receiver, and a research assistant acti-
Hill: (a) the Autism Research Registry, coordinated vated the marker switch to record the beginning and end
through the Neurodevelopmental Disorders Research of each condition during the session.
Center, and (b) the Sensory Experiences Project, funded The child was seated in a high chair positioned 3 ft
by the National Institute of Child Health and Human from the center panel of a puppet theater, which con-
Development. These referral sources distributed recruit- tained a window through which stimuli were presented.
ment flyers to the parents of potential participants and The side panels of the puppet theater were covered with
received responses from families who were willing to be black felt and decorated with a few pictures. The child’s
contacted about this study. Contact information for inter- parent sat in a chair next to the child. All stimulus con-
ested families was provided to the project staff. Project ditions (see Table 2) were presented within the window.
staff determined that children met preliminary eligibil- A small, unobtrusive video camera was mounted just
ity criteria by means of a telephone interview (e.g., clinical above the theater window in order to record the child’s
diagnosis of an ASD, no known genetic anomalies, limited behavioral responses, and it provided a clear image of

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the child’s face and eyes when he oriented toward the measures included in each aggregate score and determin-
theater window. All experimental sessions were completed ing the mean. To anchor all scores to the children’s ini-
between 9:00 a.m. and 12:00 p.m. to control for the effect tial performance levels, we used the means and standard
of circadian rhythm on heart activity. deviations on the measures at the entry assessment to
Longitudinal follow-up assessments were conducted calculate the z scores at both entry and follow-up. We refer
1 year after the entry assessments (M = 11.9 months, to these aggregate scores as entry scores and follow-up
range: 11–14 months) and consisted of repeated mea- scores in the remainder of this article. For 1 child, the
surement of language and social-communicative skills CDI:WG at entry was missing, and thus the aggregate
and documentation of speech-language intervention dur- score for this child was based on his mean z score for the
ing the time since the entry assessment. Parents received two available measures.
$25, and the children received a small toy or book for their
contributions both for the entry assessments and the
follow-up assessments. Results
We coded videos of the experimental session using
Descriptive Analyses
Observer 3.0 software (Software for Behavioral Research,
1996) to measure the child’s sustained looking at the stim- Communication skills. Descriptive information on
ulus window. The coding of videotapes for sustained look- the multiple measures of communication used for the
ing began once coders reached training reliability standards aggregate variables of receptive language, expressive
of at least 80% agreement. Reliability coding was com- language, and social-communicative adaptive skills is
pleted on five randomly selected sessions (23%), with a mean presented in Table 3. Participants had mean AE scores
interrater agreement of 90% and a mean kappa of .79. around 12 months on standardized tests across the dif-
We synchronized heart activity with the experimen- ferent language and social-communicative measures at
tal sessions by aligning the markers inserted via the entry, with considerable variability around that mean.
marker switch into the heart activity data with the video- By follow-up, the participants as a group had mean AE
taped data. We edited heart activity data using MxEdit scores around 20 months across measures, with an in-
software (Delta Biometrics of Bethesda, MD; patented crease in the range of scores reflecting that some chil-
by Porges, 1985). We calculated RSA using MxEdit in dren showed limited to no progress in their scores from
a manner consistent with the procedures developed by entry to follow-up, whereas other children showed consid-
Porges (1985). We quantified RSA during each sequen- erable progress (see change score data in Table 3).
tial 30-s epoch and computed averages for each condi- Behavioral and physiological response to nonsocial
tion. We used the mean across the three CDS conditions and to CDS stimuli. Children engaged in sustained look-
in the data analyses as a measure of RSA during CDS. ing 76.3% of the time during presentation of the non-
We dropped heart activity data for 4 of the 22 partici- social stimuli (SD = 20.0) and 53.3% of the time during
pants from the entry assessment because of technical CDS (SD = 28.1). During the presentation of nonsocial
difficulties in collecting the data (n = 2) or excessive ar- stimuli, the mean RSA was 4.76 (SD = 1.09), and dur-
tifacts (n = 2). Out of the 19 children seen at the longi- ing presentation of CDS stimuli the mean RSA was
tudinal follow-up, 15 had heart activity data from the entry 4.33 (SD = 1.04). An explanation of the RSA index can
assessment and were included in longitudinal analyses. be found in Porges (1995a).

Data Analysis Primary Analyses


We calculated three aggregate communication scores Research Question 1: What is the relationship of be-
from measures taken at both entry and follow-up assess- havioral and physiological responses during CDS or non-
ments, including (a) receptive language, which comprised social stimuli to concurrent communication skills in young
MSEL Receptive Language AE, PLS-4 Auditory Com- children with ASD? Zero-order correlations between the
prehension AE, and CDI:WG total words understood; behavioral and physiological measures of responses dur-
(b) expressive language, which comprised MSEL Expres- ing CDS or nonsocial stimuli and the children’s entry
sive Language AE, PLS-4 Expressive Communication AE, communication skills are given in Table 4. These data
and CDI:WG total words said; and (c) social-communicative indicate that sustained looking during CDS was signif-
adaptive skills, which comprised VABS Socialization AE icantly associated with entry (concurrent) receptive lan-
and VABS Communication AE. In general, we derived ag- guage, expressive language, and social-communicative
gregate communication scores by calculating the z scores adaptive skills, with large effect sizes for the magnitude
for individual measures (e.g., PLS-4 Auditory Comprehen- of these correlations. Also, sustained looking during non-
sion AE, MSEL Receptive Language AE, CDI:WG to- social stimuli was significantly correlated with entry re-
tal words understood), then adding the z scores for the ceptive language and expressive language, but not with

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Table 3. Entry and follow-up language and social-communication developmental assessment results.

Entry Follow-up Change scores

Measure M SD Range M SD Range M SD Range

PLS–4 AC 10.9 7.8 1–23 20.3 11.9 5–42 9.0 6.8 –3–24
PLS–4 EC 13.1 6.1 5–27 20.6 10.3 8–43 7.4 7.0 –2–24
MSEL RL 12.7 8.3 1–27 21.2 12.4 4–57 8.4 6.8 –1–30
MSEL EL 12.0 6.9 2–26 19.4 13.9 5–60 7.4 11.2 –6–46
CDI WU 162.3 120.8 2–352 228.2 127.9 8–394 65.9 67.6 –27–244
CDI WS 69.4 102.7 0–340 136.7 153.1 0–384 67.3 93.2 –4–337
VABS Comm 12.1 6.3 3–23 17.7 9.4 4–34 4.6 5.3 –3–18
VABS Social 12.0 3.9 4–18 18.3 9.2 6–42 6.3 7.7 –4–24

Note. PLS-4 AC = Preschool Language Scale—4th Edition, Auditory Comprehension age equivalent; PLS-4 EC = PLS-4 Expressive
Communication age equivalent; MSEL RL = Mullen Scales of Early Learning Receptive Language age equivalent; MSEL EL = MSEL
Expressive Language age equivalent; CDI WU = MacArthur Communicative Development Inventories total words understood;
CDI WS = CDI total words said; VABS Comm = Vineland Adaptive Behavior Scales Communication age equivalent; VABS Social =
VABS Socialization age equivalent.

entry social-communicative adaptive skills. We compared RSA during CDS was associated with entry recep-
the magnitude of the correlation of sustained looking tive language, but not with entry expressive language or
during CDS with entry receptive language, r (22) = .86, social-communicative adaptive skills. RSA during non-
with the magnitude of the correlation of sustained social stimuli was not associated with any concurrent
looking during nonsocial stimuli with entry receptive lan- language or social-communication measures.
guage, r(22) = .45, using the Simple Statistical Interactive Research Question 2: Are behavioral or physiological
Analysis (http://www.quantitativeskills.com/sisa/index. responses during CDS or nonsocial stimuli predictive of
htm) procedure for comparing dependent correlations communication outcomes in young children with ASD?
and confirmed that the former correlation is signifi- We first examined the zero-order correlations between
cantly greater than the latter, t(19) = 2.9, p = .005. We the measures of response to CDS and nonsocial stimuli at
observed the same pattern for the other two measures (i.e., entry and communication measures at follow-up (see
entry expressive language and entry social-communicative Table 4). In terms of sustained looking, the percentage of
adaptive skills), in the relative magnitude of correla- looking during CDS at entry was significantly associated
tions, although the differences were not significant. with follow-up scores on receptive language, expressive

Table 4. Correlations between entry measures of response to nonsocial and CDS stimuli and language and social
communication skills at entry and follow-up.

Variable Statistic RL-1 EL-1 SC-1 RL-2 EL-2 SC-2

% Looking–nonsocial r .452 .544 .276 .380 .396 .320


p .017 .004 .107 .054 .047 .091
N 22 22 22 19 19 19
% Looking–CDS r .859 .756 .613 .787 .715 .585
p .000 .000 .001 .000 .000 .004
N 22 22 22 19 19 19
RSA–nonsocial r .203 .272 –.077 .058 .186 .188
p .210 .138 .381 .419 .253 .251
N 18 18 18 15 15 15
RSA–CDS r .427 .274 .139 .395 .496 .632
p .039 .136 .291 .073 .030 .006
N 18 18 18 15 15 15

Note. All tests are one-tailed. RL-1 = receptive language aggregate score at study entry; EL-1 = expressive language aggregate
score at study entry; SC-1 = social-communicative adaptive skills aggregate score at study entry; RL-2 = receptive language
aggregate score at follow-up; EL-2 = expressive language aggregate score at follow-up; SC-2 = social-communicative adaptive
skills aggregate score at follow-up.

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language, and social-communication adaptive skills. The Table 5. Summary of hierarchical regression analyses for sustained
association between percentage of looking during non- looking during CDS as a predictor of communication scores at
social stimuli at entry and the follow-up scores was follow-up.
significant only for expressive language, although cor-
relations approached significance for receptive language Variable B SE B b R2
and social-communication adaptive skills. Predicting RL-2
Turning to the physiological data, RSA during CDS Step 1: RL-1 1.16 0.14 .89*** .79
was significantly correlated with follow-up expressive Step 2
language and social-communication adaptive skills, and RL-1 1.11 0.30 .86**
it approached significance for receptive language. In con- Sustained looking–CDS 0.19 1.10 .04 .79
trast, RSA during nonsocial stimuli was not significantly Predicting EL-2
correlated with any follow-up scores. It is interesting that Step 1: EL-1 1.46 0.27 .80*** .64
the strength of the association between RSA during CDS Step 2
at entry and follow-up expressive language scores in- EL-1 1.08 0.38 .59*
creased over the concurrent level of association between Sustained looking–CDS 1.76 1.32 .28 .67
these measures at entry (from .27 to .49), as did the Predicting SC-2
strength of the association between RSA during CDS Step 1: SC-1 1.43 0.31 .74*** .55
at entry and follow-up social-communication adaptive Step 2
skills (from .14 to .63). SC-1 1.28 0.46 .66*
Sustained looking–CDS 0.76 1.65 .11 .56
Pearson product–moment correlations are reported
in Table 4. Because of the relatively small sample size, Note. N = 19.
we also calculated nonparametric Spearman correlations,
*p < .05. **p < .01. ***p < .001.
with similar orders of magnitude in the correlations in
most cases. The one notable exception was that the cor-
relation between RSA during CDS and expressive lan-
guage at follow-up dropped to a negligible level (rs = .06) Discussion
and was not significant.
As hypothesized, sustained looking during CDS was
Next, we conducted multiple linear regression anal- significantly related to concurrent measures of receptive
yses to determine the association between initial mea- language, expressive language, and social-communicative
sures of response to CDS and follow-up communication adaptive skills. These findings are consistent with the
scores, after controlling for the corresponding entry
communication scores. Given the relatively small sam-
Table 6. Summary of hierarchical regression analyses for vagal tone
ple available for these analyses, we examined Cook’s
during CDS as a predictor of communication scores at follow-up.
distance scores for each analysis. All Cook’s distance
scores were less than 1.0, suggesting that no individual
Variable B SE B b R2
participant unduly influenced the results of the multiple
regression analyses (Chatterjee, Hadi, & Price, 2000). Predicting RL-2
The results of the multiple regression analyses us- Step 1: RL-1 1.30 0.14 .94*** .87
ing sustained looking during CDS as a predictor of follow-up Step 2
RL-1 1.27 0.15 .91***
communication scores are shown in Table 5. Although
Vagal tone–CDS 0.11 0.17 .07 .88
sustained looking during CDS had a strong zero-order
correlation with each of the follow-up scores (as shown in Predicting EL-2
Table 4), it failed to account for significant additional Step 1: EL-1 1.42 0.31 .79*** .62
variance in any of the three follow-up scores after con- Step 2
EL-1 1.31 0.26 .73***
trolling for the corresponding entry score.
Vagal tone–CDS 0.73 0.29 .37* .75
With a second set of regression analyses we exam-
Predicting SC-2
ined the extent to which RSA during CDS predicted com-
Step 1: SC-1 1.35 0.31 .77** .59
munication scores at follow-up. As seen in Table 6, RSA
Step 2
during CDS did not account for significant additional SC-1 1.12 0.25 .64**
variance in receptive language at follow-up after con- Vagal tone–CDS 0.92 0.30 .45** .77
trolling for entry receptive language, but it did account
for significant additional variance in follow-up expressive Note. N = 15.
language as well as in follow-up social-communication *p < .05. **p < .01. ***p < .001.
adaptive skills.

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results of Kuhl et al. (2005) and Paul et al. (2007), who to measures of social behaviors (e.g., Blair & Peters, 2003;
also found significant levels of association between at- Calkins, 1997; Heilman, Bal, Bazhenova, & Porges, 2007;
tention to CDS and concurrent measures of language Porges et al., 1994), there were marked differences in the
performance. Contrary to our hypothesis, sustained look- sample, experimental protocol, and outcome measures
ing during nonsocial stimuli was also significantly related used in this study compared with previous research. Thus,
to concurrent measures of receptive language and expres- our findings do not directly challenge those of the prior
sive language, suggesting that some general attention fac- research on the concurrent association between RSA
tors may influence the development of language among and developmental measures, but they add to the avail-
young children with ASD, or the performance of these able information.
children on standardized measures of language, or both. This study makes unique contributions to the litera-
Nevertheless, the correlation between sustained look- ture in its findings related to the predictive associations
ing during CDS and receptive language was significantly of RSA with later communication skills in children with
stronger than the correlation between sustained looking ASD. Linear regression analyses that controlled for en-
during nonsocial stimuli and receptive language, with try communication scores indicated that RSA during
similar, although nonsignificant, trends for expressive CDS predicted follow-up expressive language and social
language and social-communicative adaptive skills. Thus, communication adaptive skills. Although not definitive,
in addition to general attention factors, the specific abil- the pattern of results suggests that the physiological
ity to sustain attention during CDS appears either to aid regulation of attention to CDS influences the ongoing de-
language development or to be aided by concurrent lan- velopment of communication skills, rather than com-
guage skills, or both. munication skills having a deterministic influence on
Longitudinally, the pattern of results for sustained physiological responses during CDS. Furthermore, the
looking was parallel to the concurrent correlations, with association of RSA during CDS, but not during nonsocial
moderate to strong zero-order correlations between look- stimuli, with later communication outcomes suggests that
ing during CDS and the outcome measures and moder- children with ASD make variable physiological adjust-
ately low zero-order correlations between looking during ments during the CDS conditions that are important in
nonsocial stimuli and the outcome measures. The mod- their processing of language and other communication
erate to strong associations of looking during CDS with stimuli. If, as proposed by the polyvagal theory, the RSA
follow-up language and social-communication aggregate of these children with ASD reflects influences of the
scores also are consistent with the results reported by neocortex on a complex social engagement system that in-
Paul et al. (2007), who found that the length of attention cludes the vagus, then children who respond with higher
to CDS of 2-year-olds with ASD was positively correlated RSA during CDS are possibly those who are experiencing
with receptive language 1 year later. Our regression anal- stronger social affiliation and, relatedly, a more opti-
yses demonstrated, however, that sustained looking during mal physiological response for processing and learning
CDS at an earlier time point did not predict communica- from CDS.
tion outcomes 1 year later after partialing out the child’s We are uncertain about how to explain the lack of a
entry communication performance. Thus, the direction predictive association between RSA during CDS at entry
of effects in this instance is unclear. Children who had de- and follow-up receptive language, especially in light of
veloped higher levels of language or social-communicative the concurrent association between these measures at
skills at the time of entry into this study may have been entry. One possible explanation is that there is variabil-
able to sustain more attention to CDS at that point be- ity in the way RSA influences communication in young
cause they understood more of what was being said. children with ASD over time; specifically, RSA may have
Alternatively, perhaps these children had been more mo- a more direct impact on receptive language early in a
tivated to attend to CDS during the infancy period and child’s language development, but over time this asso-
therefore had developed stronger language and social- ciation may be mediated by other influences, such as
communicative skills by 2 to 3 years of age, when they parental interaction style, as suggested in a recent study
entered the study. A third, and perhaps most likely, of children with varying birth conditions conducted by
possibility is that both factors operated in a tightly Feldman and Eidelman (2009).
integrated, reciprocal fashion and influenced the chil-
dren’s initial and subsequent learning and attention
skills. Limitations
With regard to our physiological variable, RSA dur- This study is limited in several respects. First, the
ing CDS was associated only with entry receptive lan- sample size is small for the regression analyses used.
guage and not with entry expressive language or entry Because of the limited power, we conducted a series of
social-communication adaptive skills. Although previ- regression analyses with two variables each, rather than
ous research has found that RSA is concurrently related testing all variables of interest in a single model. We

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also attempted to address the sample size limitation by of behavioral and physiological measures of attention to
examining the possible influence of outliers on the re- CDS in predicting communication outcomes.
gression analyses. The low Spearman rho correlation Given the emergent nature of this study, drawing
between RSA during CDS and follow-up expressive clinical implications is a highly speculative endeavor.
language, contrasted with a moderately strong and sig- One possibility is that measures of RSA in young chil-
nificant Pearson product–moment correlation, empha- dren with ASD during exposure to CDS or during social
sizes the importance of replicating these results with a interactions may predict variable response to treatment.
larger sample. We chose not to adjust the alpha levels for Hypothetically, if children with higher RSA in social con-
multiple tests of significance, preferring in this initial texts have stronger social affiliation with other people,
study to accept the risk of Type I errors over Type II then a relationship-based intervention approach (Odom,
errors. Thus, the likelihood of false positive findings is Boyd, Hall, & Hume, 2010) may be more effective for
increased, and replication of our results in future stud- those children, whereas for children with relatively low
ies is an important goal. The small sample size also in- RSA during social contexts an applied behavior approach
creases the possibility of false negative findings due to a that initially reinforces new communication skills with
lack of power to detect significant relations, and replica- nonsocial reinforcers may be more effective. Another pos-
tion with a larger sample might provide some additional sibility is that children with ASD might benefit from
clarification in this regard as well. interventions to stimulate the vagus. For instance, re-
A second challenge to unambiguous interpretation searchers have reported improvements in baseline RSA
of our results is the nature of the stimuli presented (see for high-risk infants who receive infant massage (Diego,
Table 2). One goal of this investigation was to expose the Field, & Hernandez-Reif, 2005) and have suggested that
children to nonsocial and social stimuli with high eco- vagal nerve stimulation might improve behavioral adap-
logical validity. Thus, our nonsocial and social stimuli tation for children with ASD (Escalona, Field, Singer-
were complex, multimodal stimuli involving both visual Strunck, Cullen, & Hartshorn, 2001). It is possible that
and auditory components; furthermore, one of the CDS early interventions for children with ASD that result in
stimulus conditions was presented live by a research as- greater improvements in parasympathetic regulation
sistant, whereas all other conditions were presented by would be associated with the strongest long-term social-
means of videotape. As a result, our stimuli do not repre- communication outcomes, independent of immediate im-
sent carefully controlled analogs of speech versus non- provements in communication skills resulting from the
speech stimuli or CDS versus adult-directed speech stimuli. intervention.
It is possible that some of our findings may be attrib- In a review of the literature on vagal activity and
utable to uncontrolled factors, such as a greater degree infant development, Field and Diego (2008) pointed out
of visual movement in the nonspeech stimuli, or the ef- that in multivariate studies RSA has been found to be
fects of including a live condition among our CDS stimuli one of multiple variables that mediate development. They
but not in the nonsocial stimuli. also noted that the correlational designs of most studies
A third limitation of this study is that our partici- that have examined vagal activity in child development
pants were quite impaired relative to age expectations have not allowed conclusions that vagal activity plays a
and in the lower range of functioning even among young causal role. With attention to the important points Field
children with ASD. As a result, the present findings may and Diego raised, future research can build on the meth-
not generalize to young children with ASD who are func- ods and novel findings of this study to achieve a better
tioning at higher language and cognitive levels. understanding of the complex developmental processes
that affect language and communication outcomes in
children with ASD.
Summary and Future Directions
To our knowledge, this study is the first investiga-
tion to combine behavioral and physiological measures Acknowledgments
of response to CDS among children with ASD and the
first longitudinal investigation of concurrent and pre- We gratefully acknowledge the support of National
Alliance for Autism Research /Autism Speaks Grant 681 and
dictive relations between RSA and later language and
National Institute of Child Health and Human Development
social-communicative outcomes in this population. There-
Grant R01-HD42168. We thank the families who participated
fore, replicating the results with a larger sample of young in this study. We also thank Irene Chan, Renee Clark, Sheila
children with ASD is a future goal of our research pro- Lang, Kerry Callahan Mandulak, Megan McLester, Beth
gram. In addition, a larger sample would permit testing Schultz, and Doanne L. Ward-Williams, who assisted with
of more complex regression models, such as evaluating recruitment, data collection, and coding; and Elizabeth R.
in a single model the relative and unique contributions Crais, who provided a valuable critique of a draft of this article.

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