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Cardiovascular Arousal in

Individuals With Autism

Matthew S. Goodwin, June Groden, Wayne F. Velicer,


Lewis P. Lipsitt, M. Grace Baron, Stefan G. Hofmann,
and Gerald Groden

Despite the hypothesized link between arousal and behavior in tic of underarousal can interfere with this population’s ability
persons with autism, there is a lack of idiographic research that to attend to, process, and interact with the environment and
directly assesses arousal responses to novel stimuli or social sit- can result in the failure to learn normative behaviors and skills
uations in this population. The current study used heart rate as from other people (Lord & McGee, 2001; Prizant, Wetherby,
a measure of sympathetic activity to compare arousal responses Rubin, & Laurent, 2003; Siegel, 2003).
to the presentation of potentially stressful situations in five per-
Despite the hypothesized link between arousal and behav-
sons with autism and five age- and sex-matched typically devel-
ior in persons with autism, there is a lack of idiographic re-
oping individuals. Findings revealed that the group with autism
showed significant responses to stressors only 22% of the time search that directly assesses this population’s arousal responses
compared to the typically developing group, which showed sig- to novel stimuli or social situations. In an effort to systemati-
nificant responses 60% of the time. Interpretation of these re- cally evaluate arousal responses in persons with autism, the pre-
sults and methodological considerations for future research on sent article reviews research on stress, stress-related anxiety,
arousal in persons with autism are discussed. and physiological arousal and experimentally compares arousal
responses to identified environmental stressors in five ind-
ividuals with autism and five age- and sex-matched typically
developing children.

A
ccording to the Diagnostic and Statistical Manual of
Mental Disorders–Fourth Edition (DSM-IV; American
Psychiatric Association, 1994), autism is character-
ized by qualitative impairments in socialization, communica-
Stress, Anxiety, and Autism
tion, and circumscribed interests, including stereotypical
behavior patterns and behavioral rigidity to changes in rou- A stressor is any stimulus or circumstance that compromises an
tines. Although these symptomatic features are well estab- individual’s physical or psychological well-being (Lazarus &
lished, it is unclear whether their origin lies simply in the Folkman, 1984) and that requires an individual to make an ad-
absence of appropriate social skills and behavioral flexibility or justment (Selye, 1956). The consequences of stressors within
arises from a qualitative difference in physiological arousal as- an individual are collectively called the stress response. The stress
sociated with these abilities. response typically relates to three periods of interaction be-
There is currently little research addressing the role of tween the stressor and the individual’s response: (a) before the
physiological arousal in autism despite earlier suggestions that stressful event occurs, (b) during the stressor, and (c) after the
neurophysiological factors implicated in the disorder can cause stressor, when the individual may experience some of the resid-
or contribute to significant problems in modulating arousal to ual effects of the event.
social and sensory stimuli that are novel or unpredictable
(Dawson, 1991; Dawson & Lewy, 1989; Kinsbourne, 1987; Stress and Autism
Ornitz, 1989; Ornitz & Ritvo, 1968), resulting in behavioral
and physiological response patterns of either overarousal (Hutt, Literature suggests that many of the behaviors associated with
Hutt, Lee, & Ounsted, 1964) or underarousal (DesLauriers autism are related to stress, as stressful events frequently
& Carlson, 1969). According to these arousal modulation precipitate the maladaptive behavior problems seen in this
theories of autism, both anxious and agitated responses char- population, such as aggression, self-injury, tantrums, and de-
acteristic of overarousal and passivity and lethargy characteris- struction of property (Groden, Cautela, Prince, & Berryman,

FOCUS ON AUTISM AND OTHER DEVELOPMENTAL DISABILITIES


VOLUME 21, NUMBER 2, SUMMER 2006
PAGES 100–123
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1994; Prior & Ozonoff, 1998). Stereotypic behaviors includ- Physiological Arousal and Autism
ing echolalia, twirling, rocking, flicking, and hand flapping are
also found to increase when this population is exposed to The reviewed research suggests that stressful events are asso-
events commonly defined as stressors in the typical population ciated with behavioral challenges and anxiety in persons with
(Howlin, 1998; Hutt & Hutt, 1968). autism. However, given this population’s difficulties identify-
Characteristics of persons with autism, including commu- ing and describing their feelings through self-report (Hill,
nication (e.g., Lord & Paul, 1997) and socialization deficits Berthoz, & Frith, 2004), traditional assessments of stress that
(e.g., Mundy & Stella, 2000), sensory problems (e.g., Bar- utilize verbal communication (e.g., interviews, paper/pencil
anek, 2002), and deficits in executive function (e.g., Rogers tests) have limited use in persons with autism. Contemporary
& Bennetto, 2000), may also make this population exceed- researchers have attempted to overcome these unreliable self-
ingly vulnerable to stressors and limit their ability to cope reports and measure stress in this population by focusing on
(Groden, Cautela, Prince, & Berryman, 1994). Ineffective physiological reactivity during rest and performance on a task.
coping to stressors can lead to anxiety, and research suggests
that anxiety is more prevalent in persons with autism, Asper- Physiological Stress Responses
ger syndrome (AS), and Pervasive Developmental Disorder–
Not Otherwise Specified (PDD-NOS) than in individuals who Widespread changes in the cardiovascular system, the immune
are typically developing, behaviorally disordered, or learning system, the endocrine glands, and brain regions involved in
impaired. For example, Muris and colleagues (1998) inter- emotion and memory are activated when an organism is
viewed parents of 44 children with either autism or PDD-NOS aroused by a stressor (Sapolsky, 1998). These physiological ac-
using the Anxiety Disorders section of the Diagnostic and Sta- tions are controlled primarily by the autonomic nervous sys-
tistical Manual of Mental Disorders–Third Edition-Revised tem (ANS) and enable an organism to respond adaptively to a
(DSM-III-R; American Psychiatric Association, 1987) and found stressor by preparing the body to fight or flee. The peripheral
that 84.1% met criteria for an anxiety disorder. In a similar part of the nervous system, the ANS controls smooth muscle,
study, Kim et al. (2000) conducted standardized interviews cardiac muscle, and glands and includes both sympathetic and
with parents of 59 children with either autism or AS and found parasympathetic branches. The sympathetic branch is domi-
a greater rate of anxiety in this group compared to a norma- nant in emergency conditions and initiates widespread and
tive sample of 1,751 typical children from the community. profound body changes, including acceleration in heart rate,
Green et al. (2000) compared the psychological comorbidity dilation of the bronchioles, discharge of adrenaline into the
of 29 individuals with AS to age-matched adolescents with bloodstream, inhibition of digestion, and elevation in blood
a conduct disorder and found significantly higher levels of pressure. The parasympathetic branch contains chiefly cholin-
anxiety in the AS group. Findings from this study also revealed ergic fibers that tend to induce secretion, increase the tone and
that 35% of the children with AS met the International contractility of smooth muscles, and slow heart rate. In gen-
Statistical Classification of Diseases and Related Health eral, the sympathetic division is a catabolic system associated
Problems–Tenth Revision (ICD-10; World Health Organiza- with emergencies; the parasympathetic, an anabolic system
tion, 1992) criteria for generalized anxiety disorder and 10% associated with vegetative processes. The sympathetic and
met criteria for a specific phobia. In another study, Gillot et al. parasympathetic divisions of the ANS work in antagonistic
(2001) found that 15 children with high-functioning autism ways to maintain homeostasis: a dynamic equilibrium in which
scored higher on measures of anxiety than both age-matched continuous changes occur, yet relatively uniform conditions
children with specific learning impairments and typically de- prevail (Fox, 1996).
veloping children. Lastly, Bellini (2004) examined anxiety in Autonomic defensive responding is thought to be an indi-
41 adolescents with either high-functioning autism, AS, or cator of arousal characterized in part by accelerations in the
PDD-NOS and found that 49% of the sample met criteria for sympathetic nervous system, including heart rate (HR), respi-
social anxiety. ration, and pupillary dilation, that fail to habituate to envi-
Evidence also suggests that children with developmental ronmental stimuli of high intensity (Lacey, 1967). As such, it
disabilities, including those with autism, are more fearful than is thought to be an adaptive strategy that enables an organism
typically developing children (Evans, Canavera, Kleinpeter, to avoid or escape the potential dangers of threatening stimuli
Maccubbin, & Taga, 2005; Knapp, Barrett, Groden, & Gro- (Stern, Ray, & Quigley, 2001). Autonomic defensiveness to
den, 1992; Matson & Love, 1990). Some of the most com- environmental stimulation has been observed previously in per-
mon fears identified for children with autism in these studies sons with autism. Cohen and Johnson (1977) measured car-
were associated with noises, presence of other people, and the diovascular reactivity during a variety of attention-demanding
dark. Individuals with autism have also been shown to exhibit tasks in 10 individuals with autism and age-matched typical
panic-like levels of discomfort in response to environmental controls. Their tasks were designed to elicit either outward di-
changes (Steingard, Zimnitzky, DeMaso, Bauman, & Bucci, rection of attention (and intake of sensory input) or inward di-
1997). rection of attention (and relative rejection of external sensory
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input). Results indicated that the group with autism had a ten- individuals with autism. Groden et al. (2005) telemetrically
dency to reject external sensory input and elicit higher mean recorded HR in 10 individuals ranging in age from 13 to 37
blood flow and lower peripheral vascular resistance. In a years (M = 24 years) who were positively identified with either
follow-up study, Kootz and Cohen (1981) measured HR, autism or PDD-NOS. Cardiovascular responses were recorded
mean blood flow, and peripheral blood flow in 14 individuals at baseline and then while the participants engaged in four po-
with autism and 16 typical boys while resting, during social in- tentially stressful situations adapted from the Stress Survey
teraction, and while engaged in a reaction-time task. Findings Schedule for Persons with Autism and Developmental Disabili-
revealed that the individuals with autism had elevated HR re- ties (SSS; Groden et al., 2001). The SSS is a psychometrically
sponses during the entire session and failed to show cardio- sound survey instrument for rating the severity of perceived
vascular changes with sensory intake. Finally, Kootz, Marinelli, stress reactions to commonly identified stressors in the lives of
and Cohen (1982) studied 16 individuals with autism by mea- persons with autism and developmental disabilities. It contains
suring blood pressure and HR during a reaction-time task, 49 items/situations that relate to eight dimensions of stress,
social interaction, and at rest. In this observation, higher func- including changes and threats, anticipation/uncertainty, un-
tioning individuals with autism displayed a normal pattern of pleasant events, pleasant events, sensory/personal contact,
cardiovascular responses to sensory intake, whereas lower food-related activity, social/environment interactions, and
functioning individuals showed increased cardiovascular reac- ritual-related stress. The potentially stressful situations adapted
tivity and rejection of external sensory stimuli. from the SSS used in the study included losing at a game, eat-
Additional investigations have found that individuals with ing a preferred food, having a change in staff, and having un-
autism, compared to persons who are typically developing, structured time. Using interrupted time series analysis, the
generally respond with increased sympathetic tone at baseline data for each participant were examined to see if mean HR re-
(Ming, Julu, Brimacombe, Connor, & Daniels, 2005) and sponses were significantly different during each stressor phase
when exposed to environmental stimulation (Angus, 1970; compared with mean HR during baseline. Results illustrated
Lake, Ziegler, & Murphy, 1977; Palkovitz & Wiesenfeld, good compliance with the HR monitor and arousal to all four
1980; Zahn, Rumsey, & van Kammen, 1987). Other studies, stressors in some of the participants.
however, have found little to no differences between groups In an effort to provide a wider sample of potential stres-
during experimental demands for socialization, attention, or sors that can elicit significant arousal responses in this popula-
habituation (Althaus, Mulder, Mulder, Aarnoudse, & Min- tion, Goodwin et al. (2004) repeated the experimental design
deraa, 1999; Graveling & Brooke, 1978; Hutt, Forrest, & and analysis plan from Groden et al. (2005) in five individ-
Richer, 1975; MacCulloch & Williams, 1971; Sigman, Dis- uals with autism ranging in age from 12 to 20 years (M = 15
sanayake, Corona, & Espinosa, 2003; Stevens & Gruzelier, years). Cardiovascular reactions were assessed while the par-
1984; Toichi & Kamio, 2003; van Engeland, 1984). Only one ticipants engaged in three previously untested stressors from
study has found lower than normal arousal levels in persons the SSS, including exposure to a loud noise, engagement in a
with autism responding to social demands (DesLauriers & difficult task, and attending to a remote control robot (an un-
Carlson, 1969). predictable stimulus). This study also used a more sophisti-
Although these findings suggest some arousal differences cated, wireless HR monitor (LifeShirt, Vivometrics, Inc.) that
in persons with autism, it is difficult to interpret this body of records concomitant motor movements. Results illustrated
research due to methodological problems. For instance, most that participants tolerated the new ambulatory monitor and
of these studies were conducted prior to the publication of the showed some significant arousal responses to all three added
DSM-III-R criteria for autism, calling into question the valid- stressors.
ity of participant diagnoses. The physiological equipment used The present investigation sought to further replicate the
in the majority of these investigations was antiquated, likely measurement protocol from Groden et al. (2005) and Good-
contributing to participant discomfort, movement artifact, win et al. (2004) and control for some remaining method-
and equipment failures that resulted in a loss of data. Few of ological problems associated with previous ANS assessments
these studies incorporated a large sample of novel situations or of arousal in persons with autism. Controlling for background
stimuli to elicit significant arousal responses, and many failed factors that can affect cardiovascular responses, including co-
to include a baseline measure from which to compare physio- morbid psychological disorders, use of pharmaceuticals, and
logical reactivity. Finally, few studies reported on or controlled general cardiovascular functioning, the current study expe-
for background factors that can affect arousal responses, in- rimentally compared arousal responses to identified envi-
cluding comorbid psychological disorders, the participant’s ronmental stressors in five individuals with autism and five
use of pharmaceuticals, and general cardiovascular function- age- and sex-matched typically developing children. A series
ing. of 10 single-subject time series designs was used. The single-
To control for some of the methodological problems as- subject designs consisted of 14 phases where resting tasks al-
sociated with previous ANS studies of arousal in persons with ternated with potentially stressful tasks. Sessions began with a
autism, we conducted two feasibility studies for telemetrically baseline phase. After the baseline phase the participants en-
assessing cardiovascular arousal to environmental stressors in gaged in six potentially stressful situations. The potentially
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stressful situations alternated with rest phases. In addition, a ranged from 31.5 to 43.5 (M = 39), placing the sample in the
physical exertion phase was used to ensure that participants moderately to severely autistic range. Four of the five partici-
could demonstrate an increase in HR significantly greater than pants with autism used spoken language as their primary
baseline. Given the reviewed literature on stress, stress-related method of communication, and one participant used sign lan-
anxiety, and ANS arousal findings in persons with autism, it guage. The second group was composed of five typically
was hypothesized that the group with autism would have sig- developing, chronological age- and sex-matched individuals.
nificantly greater cardiovascular reactivity, as compared to Typically developing participants were children of staff mem-
baseline, to a greater number of environmental stressors than bers at the Groden Center recruited from advertisements
the group of typically developing peers. posted at the center. None of the participants in either group
were prescribed any psychiatric medications and none had
documented comorbid disorders (e.g., attention-deficit/
Method hyperactivity disorder, obsessive-compulsive disorder, seizure
disorder) at the time of the study. Typically developing partic-
Participants ipants and participants with autism were also assessed for high
blood pressure using diastolic and systolic measures and found
Two groups of children with parental consent participated in
to be normotensive (< 90 mmHg diastolic blood pressure).
this study. The first group consisted of five males with autism,
Characteristics of the 10 participants are presented in Table 1.
none of whom were included in the feasibility studies de-
scribed earlier. They ranged in age from 8 to 18 years (M =
13.8, SD = 4.24) and were recruited from the Groden Cen- Setting
ter, a day program serving behavioral and academic needs of
children with developmental disabilities. Diagnoses were made Participants were seated in a comfortable chair in a sound-
by a licensed psychologist familiar with autism using DSM-IV attenuated room with low-level incandescent lighting. A one-
guidelines, the Childhood Autism Rating Scale (CARS; way mirror provided discrete viewing capabilities from an
Schopler, Reichler, & Renner, 1986), and previous psychiatric adjacent observation room. A familiar person accompanied the
reports. Participant cognitive abilities as assessed either by participants to increase comfort with the setting and experi-
standardized intelligence measures (e.g., Stanford-Binet Intel- mental phases.
ligence Scale–Fourth Edition [Thorndike, Hagen, & Sattler,
1986]; Leiter International Performance Scale–Revised [Roid
Instruments
& Miller, 1997]) or scales of cognitive development (e.g.,
Bayley Scales of Infant Development–Second Edition [Bayley, Cardiovascular responses were recorded using the LifeShirt
1993]) ranged from 24 to 38 (M = 31) and 5 months to 24 (Vivometrics, Inc.), a noninvasive telemetric recording device
months, respectively. A familiar staff person also completed a that continuously (i.e., beat-to-beat) stores electrocardiograph
CARS for each participant with autism. Scores on the CARS (ECG) data on a portable battery-powered electronic recorder

TABLE 1
Participant Characteristics
Age Primary method Diastolic Systolic Cognitive CARS
Participant (years) Sex Diagnosis of communication pressure pressure development/IQ Total score

Autism
M.L. 8 Male Autism Verbal 58 102 32b 36
J.L. 10 Male Autism Verbal 64 110 5 mo.a 43.5
S.E. 16 Male Autism Verbal 84 136 38b 31.5
M.C. 17 Male Autism Verbal 70 128 18–24 mo.a 39
A.F. 18 Male Autism Sign language 66 124 24c 42.5
Typically developing
B.A. 8 Male —- —- 68 96
C.N. 10 Male —- —- 62 106
D.P. 16 Male —- —- 74 106
D.V. 17 Male —- —- 66 98
S.M. 18 Male —- —- 72 118

Note. CARS = Childhood Autism Rating Scale (Schopler, Reichler, & Renner, 1986).
a
Bayley Scales of Infant Development-Second Edition (Bayley, 1993). bStanford-Binet Intelligence Scale-Fourth Edition (Thorndike, Hagen, & Sattler, 1986). c Leiter
International Performance Scale-Revised (Roid & Miller, 1997).
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worn on the body (for description see Wilhelm, Roth, & Sack- ticipants with autism had visits to the laboratory included on
ner, 2003). The LifeShirt also collected motor movements and their weekly classroom schedules. Finally, all participants chose
changes in posture positions using a dual-axis accelerometer from a reward menu (food, game, or activity) at the end of
positioned on the anterior surface of the rib cage. Movement their preobservation visits to increase future participation.
data were obtained for the present study to control for HR re-
sponses attributable to physical demands. All of the informa- Design. The observational design for each participant
tion stored in the electronic recorder was downloaded to a PC consisted of 14 phases (see Table 2). Each session began with
computer as an ASCII file and exported to Excel in prepara- a 5-minute baseline phase (sitting quietly with a familiar per-
tion for statistical analyses. son). After the baseline phase the participants engaged in six
potentially stressful situations (see Stress Phases). These po-
tentially stressful situations alternated with 2-minute rest phases
Procedure
(sitting quietly with a familiar person). A physical exertion task
Preobservation Procedure. To increase comfort and (riding a stationary bicycle for 2 minutes) was included to en-
compliance with the stress assessment, each participant was in- sure that participants could demonstrate an increase in HR sig-
troduced to the laboratory setting and heart monitor prior to nificantly greater than baseline. The order of presentation of
the experimental session. For the participants with autism, lab- the stress phases was intentionally not counterbalanced to per-
oratory visits occurred once a day for a week prior to being mit direct comparisons both between and within the typically
observed. For the typically developing participants, a mini- developing and autism groups.
mum of 30 minutes prior to the assessment period was pro-
vided to try on the HR monitor, ask questions about the Stress Phases. A wide sample of potential stressors was
device, and sit in the laboratory. Both groups of participants selected to enable adequate opportunities for the participants
were given a rationale for measuring HR appropriate to their to elicit a cardiovascular stress response. The following stress
developmental level (e.g., “We are interested in seeing how phases and accompanying stress dimensions identified in the
fast your heart beats when you are doing activities”). To ac- SSS (Groden et al., 2001) were included in the study because
commodate for difficulties with changes in daily routines, par- they (a) included events that naturally occur in the environ-

TABLE 2
Observational Design and Stress Task Descriptions
Phase Task Task length Task description Stress survey domain

1 Baseline 5 min With a familiar person, seated in a comfortable chair


2 Loud noise 2 min With a familiar person, seated in a comfortable chair while a Sensory/personal contact
vacuum cleaner runs outside the room
3 Rest 2 min With a familiar person, seated in a comfortable chair
4 Remote robot 2 min With a familiar person, seated in a comfortable chair while Anticipation/uncertainty
a remote control robot navigates around the room
5 Rest 2 min With a familiar person, seated in a comfortable chair
6 Unstructured time 2 min Sitting in the room alone, given no other instructions than Anticipation/uncertainty
“We will be back in 2 minutes”
7 Rest 2 min With a familiar person, seated in a comfortable chair
8 Eating preferred food 2 min With a familiar person, given preferred food to eat Pleasant event
9 Rest 2 min With a familiar person, seated in a comfortable chair
10 Difficult task 2 min With a familiar person, seated in a comfortable chair and Changes/threats
asked to mimic how the familiar person folds a towel
11 Rest 2 min With a familiar person, seated in a comfortable chair
12 Change in staff 2 min Familiar person leaves and person unfamiliar to the Unpleasant event
participant sits in the room
13 Rest 2 min With a familiar person, seated in a comfortable chair
14 Physical exertion 2 min With a familiar person, riding a stationary bicycle
Transition Time between tasks
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ment; (b) could be replicated in an experimental setting; ploy traditional tests of statistical significance using the general
(c) consist of physical, social, and cognitive stimuli that over- linear model.
lap considerably with the problems of socialization, commu- Three waves of analyses were conducted for each partici-
nication, and behavioral rigidity characteristic of persons with pant using SAS Proc ARIMA (SAS Institute, 1988). The first
autism; and (d) were shown to elicit increased heart activity wave involved a graphical display of the data. The second wave
in the two feasibility studies (Goodwin et al., 2004; Groden involved a model identification procedure to determine the
et al., 2005). The stress phases included were as follows: best-fitting ARIMA (p, d, q) model. For all 10 participants,
the general transformation approach of Velicer and McDonald
1. Loud noise (sensory/personal contact): with a familiar (1991) was used. This approach is the equivalent to assuming
person, seated in a comfortable chair while a vacuum a higher order (5+) autoregressive model and has been shown
cleaner runs outside the room. to perform accurately in previous simulation studies (Harrop
2. Remote robot (anticipation/uncertainty): with a familiar & Velicer, 1985, 1990; Velicer & Colby, 2005). The third
person, seated in a comfortable chair while a remote- analysis wave employed a within-subject, interrupted TSA to
control robot navigates around the room. determine whether mean HR during each potential stressor
3. Unstructured time (anticipation /uncertainty): sitting in phase was significantly different from mean HR during base-
the room alone, given no other instructions than “We line. The data points used to calculate baseline were the last 3
will be back in 2 minutes.” minutes of the first 5 minutes of observation for each partici-
4. Eating a preferred food (pleasant event): with a familiar pant. The first 2 minutes of the baseline phase were excluded
person, seated in a comfortable chair and given preferred a priori from the analysis for each participant to allow habitu-
food to eat. ation to the telemetric apparatus and laboratory setting.
5. Difficult task (changes/threats): with a familiar person,
seated in a comfortable chair and asked to fold a towel
the same way the familiar person folds it. The familiar Results
person is instructed prior to the session to fold the towel
at a pace difficult for the participant to imitate. When the Movement Data
participant folds the towel incorrectly, the familiar person
says, “Try it this way.” Table 3 lists the mean motor movement results for the partic-
6. Change in staff (unpleasant event): seated in a comfort- ipants with autism and the typically developing group. The
able chair, familiar person leaves the room and a person motion component ranges from 0 for no movement to 50 for
unfamiliar to the participant sits in the room. running very fast. With the exception of the physical exertion
7. Transition: an artifact of the study design consisting of task, where motor movements were expected to increase, there
time between stressors and rest phases when the partici- was very little movement detected across phases for either
pant waited for the investigator to set up and begin the group. In addition, for each participant motor movement was
subsequent phase. included in the time series analysis as a time-varying covariate
to account for any explained variance in the HR data. The find-
ings suggest that the subsequent reported HR results are vir-
Analysis tually free from detected movement artifacts.
The data analyses consisted of 10 separate univariate time se-
ries analyses (Crosbie, 1993; Glass, Willson, & Gottman,
Heart Rate Data
1975; Velicer & Colby, 1997; Velicer & Fava, 2003) per-
formed on each participant for the dependent variable HR. Within Individual Differences: Autism Group. M.L.
Time series analysis (TSA) requires repeated measurement at (see Appendix A) showed statistically significant HR increases
equally spaced intervals over a large number of observations from baseline (M = 106, SD = 7) to eating a preferred food
and as such is a powerful longitudinal method for modeling (M = 112, SD = 8), t(629) = 2.65, p < .01; difficult task
change over time. In TSA, sample size reflects the number of (M = 110, SD = 10), t(629) = 2.14 p < .05; and physical ex-
observations over time rather than the number of subjects. ertion (M = 122, SD = 11), t(629) = 6.58, p < .0001. J.L. (see
The telemetric HR monitor provided beat-to-beat HR values Appendix B) showed statistically significant HR increases from
generating approximately 3,500 data points per participant. baseline (M = 84, SD = 7) to remote robot (M = 92, SD = 19),
TSA was used to analyze these data given that repeated mea- t(540) = 2.40, p < .05; unstructured time (M = 95, SD = 1),
surements over time on a single subject creates serial depen- t(540) = 2.11, p < .05; and physical exertion (M = 93, SD =
dency that violates the statistical assumption that errors in the 15), t(540) = 2.32, p < .05. S.E. (see Appendix C) only
data are independent across observations. TSA can calculate showed statistically significant HR changes from baseline
an autocorrelation between adjacent observations and thus (M = 113, SD = 3) to physical exertion (M = 125, SD = 10),
transform serially dependent data to be independent. Once the t(700) = 2.22, p < .05. M.C. (see Appendix D) only showed
data has been transformed to be independent, TSA can em- statistically significant HR changes from baseline (M = 87,
FOCUS ON AUTISM AND OTHER DEVELOPMENTAL DISABILITIES
106

TABLE 3
Mean Movement Results for Autism and Typically Developing Participants

Baseline
Loud Remote Unstructured Eating Difficult Change Physical
Participant M SD noise robot time food task in staff Transition exertion

Autism
M.L. 0.41 0.41 0.33 0.34 0.38 0.34 0.77 0.90 0.72 1.45
J.L. 0.19 0.19 0.13 0.41 0.28 0.42 0.86 0.55 0.53 1.44
S.E. 0.31 0.12 0.19 0.14 0.21 0.27 0.72 0.25 0.35 1.09
M.C. 0.23 0.29 0.61 1.48 2.14 0.50 0.59 0.65 0.64 1.49
A.F. 0.46 0.41 0.25 0.33 0.40 0.38 0.56 0.35 0.74 1.13
Group 0.32 0.30 0.54 0.68 0.38 0.70 0.54 0.60 1.32
Typically developing
B.A. 0.55 1.09 0.27 0.12 0.46 0.27 1.24 0.22 0.63 2.22
C.N. 0.21 0.14 0.34 0.48 0.39 0.38 0.71 0.41 0.80 2.60
D.P. 0.26 0.09 0.23 0.22 0.21 0.18 0.89 0.22 0.20 0.94
D.V. 0.28 0.10 0.05 0.03 0.18 0.23 0.84 0.04 0.23 1.17
S.M. 0.31 0.12 0.19 0.14 0.21 0.27 0.72 0.25 0.35 1.09
Group 0.32 0.22 0.20 0.29 0.27 0.88 0.23 0.44 1.60

Note. Motion component ranges from 0 for no movement to 50 for running very fast.

SD = 5) to physical exertion (M = 110, SD = 10), t(563) = showed statistically significant HR changes from baseline (M =
10.37, p < .0001. A.F. (see Appendix E) showed statistically 74, SD = 6) to eating a preferred food (M = 90, SD = 5),
significant HR changes from baseline (M = 90, SD = 8) to eat- t(484) = 5.32, p < .0001; difficult task (M = 89, SD = 5),
ing a preferred food (M = 103, SD = 11), t(601) = 5.63, p < t(484) = 3.62, p < .0001; transition (M = 81, SD = 8), t(484) =
.0001; difficult task (M = 106, SD = 13), t(601) = 6.17, p < 3.66, p < .0001; and physical exertion (M = 94, SD = 7),
.0001; change in staff (M = 97, SD = 13), t(601) = 3.22, t(484) = 6.87, p < .0001. S.M. (see Appendix J) showed sta-
p < .001; transition (M = 101, SD = 12), t(601) = 5.18, p < tistically significant HR changes from baseline (M = 50, SD =
.0001; and physical exertion (M = 108, SD = 12), t(601) = 5) to unstructured time (M = 58, SD = 8), t(497) = 3.12, p <
7.35, p < .0001. .01; eating a preferred food (M = 67, SD = 7), t(497) = 3.68,
p < .001; difficult task (M = 64, SD = 8), t(497) = 3.20, p <
Within Individual Differences: Typically Developing .01; change in staff (M = 56, SD = 7), t(497) = 2.06, p < .05;
Group. B.A. (see Appendix F) showed statistically significant transition (M = 62, SD = 13), t(497) = 3.63, p < .001; and
HR changes from baseline (M = 98, SD = 10) to remote robot physical exertion (M = 78, SD = 11), t(497) = 6.25, p < .0001.
(M = 110, SD = 9), t(673) = 2.81, p < .01; unstructured time
(M = 119, SD = 7), t(673) = 4.13, p < .0001; eating a pre- Within-Group Differences: Autism Group. Two of the
ferred food (M = 116, SD = 3), t(673) = 4.44, p < .0001; dif- participants (S.E., M.C.) showed no significant HR changes
ficult task (M = 114, SD = 5), t(673) = 3.18, p < .01; change to any of the potentially stressful situations. Two other partic-
in staff (M = 105, SD = 5), t(673) = 4.62, p < .0001; transi- ipants (M.L., J.L.) showed significant HR changes to only two
tion (M = 112, SD = 13), t(673) = 4.88, p < .0001; and phys- of the stressors. The remaining participant (A.F.) showed sig-
ical exertion (M = 141, SD = 9), t(673) = 5.28, p < .0001. nificant HR changes to four of the stressors. In all participants,
C.N. (see Appendix G) showed statistically significant HR the physical exertion phase elicited significant mean HR re-
changes from baseline (M = 89, SD = 6) to transition (M = 93, sponses greater than baseline.
SD = 9), t(571) = 2.18, p < .05, and physical exertion (M =
105, SD = 18), t(571) = 5.37, p < .0001. D.P. (see Appendix Within-Group Differences: Typically Developing Group.
H) showed statistically significant HR changes from baseline One participant (C.N.) showed significant HR changes to only
(M = 57, SD = 5) to unstructured time (M = 60, SD = 6), one stressor. One participant (D.V.) showed significant HR
t(478) = 1.99, p < .05; eating a preferred food (M = 68, changes to three stressors. One participant (S.M.) showed
SD = 5), t(478) = 4.57, p < .0001; difficult task (M = 70, significant HR changes to five of the stressors. Two par-
SD = 7), t(478) = 5.42, p < .0001; change in staff (M = ticipants (B.A., D.P.) showed significant HR changes to six of
62, SD = 7), t(478) = 2.64, p < .001; transition (M = 65, the stressors. Again, in all participants, the physical exertion
SD = 8), t(478) = 4.44, p < .0001; and physical exertion (M = phase elicited significant mean HR responses greater than
73, SD = 9), t(478) = 5.52, p < .0001. D.V. (see Appendix I) baseline.
VOLUME 21, NUMBER 2, SUMMER 2006
107

Between-Group Differences. Figures 1 and 2 illustrate mean HR for difficult task in the autism group ranged from
for each phase the mean HR results for each participant with 87 bpm to 115 bpm with an overall group mean of 101 bpm
autism and each typically developing participant, respectively. (SD = 13). The mean HR for difficult task in the typically de-
The mean HR for baseline in the autism group ranged from veloping group ranged from 64 bpm to 114 bpm with an over-
84 bpm to 113 bpm with an overall group mean of 96 bpm all group mean of 85 bpm (SD = 19). The mean HR for
(SD = 12). The mean HR for baseline in the typically devel- change in staff in the autism group ranged from 85 bpm to
oping group ranged from 50 bpm to 98 bpm with an overall 102 bpm with an overall group mean of 97 bpm (SD = 11).
group mean of 74 bpm (SD = 20). The mean HR for loud The mean HR for change in staff in the typically developing
noise in the autism group ranged from 87 bpm to 113 bpm group ranged from 56 bpm to 105 bpm with an overall group
with an overall group mean of 97 bpm (SD = 11). The mean mean of 78 bpm (SD = 20). The mean HR for transition in
HR for loud noise in the typically developing group ranged the autism group ranged from 87 bpm to 115 bpm with an
from 52 bpm to 94 bpm with an overall group mean of 75 overall group mean of 100 bpm (SD = 12). The mean HR for
bpm (SD = 18). The mean HR for remote robot in the autism transition in the typically developing group ranged from 62
group ranged from 86 bpm to 112 bpm with an overall group bpm to 112 bpm with an overall group mean of 83 bpm (SD
mean of 96 bpm (SD = 11). The mean HR for remote robot = 21). The mean HR for physical exertion in the autism group
in the typically developing group ranged from 49 bpm to 110 ranged from 92 bpm to 125 bpm with an overall group mean
bpm with an overall group mean of 75 bpm (SD = 26). The of 112 bpm (SD = 14). The mean HR for physical exertion in
mean HR for unstructured time in the autism group ranged the typically developing group ranged from 73 bpm to 141
from 90 bpm to 113 bpm with an overall group mean of 100 bpm with an overall group mean of 98 bpm (SD = 27).
bpm (SD = 10). The mean HR for unstructured time in the
typically developing group ranged from 58 bpm to 119 bpm
with an overall group mean of 80 bpm (SD = 25). The mean Discussion
HR for eating a preferred food in the autism group ranged
from 85 bpm to 113 bpm with an overall group mean of 100 The present study compared the cardiac responses of five rel-
bpm (SD = 13). The mean HR for eating a preferred food in atively low-functioning persons with autism to five age- and
the typically developing group ranged from 67 bpm to 116 sex-matched typically developing individuals under repeated
bpm with an overall group mean of 87 bpm (SD = 20). The conditions of environmental stressors. Based on arousal mod-

M.L.
J.L.
S.E.
M.C.
A.F.

Baseline Loud noise Remote Unstructured Eating Difficult task Change in Transition Physical
robot time preferred staff exertion
foods
PHASE

FIGURE 1. Mean heart rate level by phase for autism group.


FOCUS ON AUTISM AND OTHER DEVELOPMENTAL DISABILITIES
108

B.A.
C.N.
D.P.
D.V.
S.M.

Baseline Loud noise Remote Unstructured Eating Difficult task Change in Transition Physical
robot time preferred staff exertion
foods

FIGURE 2. Mean heart rate level by phase for typical group.

ulation theories of autism (Dawson, 1991; Dawson & Lewy, showed approximately half the amount of variance in HR re-
1989; Kinsbourne, 1987; Ornitz, 1989; Ornitz & Ritvo, sponsivity compared to the typically developing group. These
1968), reports of stressful events being associated with behav- data appear to replicate the previous findings of Cohen and
ioral challenges (Groden et al., 1994; Howlin, 1998; Hutt & colleagues (Cohen & Johnson, 1977; Kootz & Cohen, 1981;
Hutt, 1968; Prior & Ozonoff, 1998), and documented co- Kootz, Marinelli, & Cohen, 1982) and suggest that persons
morbid anxiety disorders in persons with autism (Bellini, with autism who have high basal HR are unable to elicit
2004; Gillot et al., 2001; Green et al., 2000; Kim et al., 2000; significantly greater increases in cardiovascular reactivity to en-
Muris et al., 1998), it was hypothesized that the group with vironmental stimulation. The diminished cardiovascular reac-
autism would show significant cardiovascular responses to a tivity to environmental stressors suggests that the group with
greater number of stressors than the typically developing con- autism was either overly aroused by the testing situation on the
trol group. However, the findings revealed just the opposite: whole (which included the same characteristics and staff that
Out of the 35 opportunities for each group to show a signifi- may be stressful on a daily basis) or in a general state of auto-
cant mean HR response to a stressor (i.e., seven potentially nomic defensiveness.
stressful phases × five participants), the group with autism If the hypothesis is tenable that some individuals with
showed significant responses only 22% of the time (8 out of autism are in a general state of high autonomic arousal, then
35), compared to the typically developing group, which it is of interest to identify the underlying mechanisms con-
showed significant responses 60% of the time (21 out of 35). tributing to such responsivity. Although no one theory has
At first glance, these results suggest that the group of in- gained overwhelming support, several putative mechanisms
dividuals with autism is less aroused by environmental stres- have been suggested. Ornitz (1989) speculated that dysfunc-
sors than the typically developing control group. However, the tions in the neuronal networks in the brainstem, including the
diminished cardiovascular reactivity to potential stressors in diencephalon, can cause disordered sensory processing that re-
the group with autism may be related to their high basal HR sult in problems of arousal modulation. Hutt and Hutt (1970)
and reduced variance in responsivity (see Figure 3). On aver- hypothesized dysfunctions in sympathetic inhibitory control
age, the participants with autism showed mean HR responses mediated by the limbic system. Others have postulated dys-
approximately 20 bpm higher during baseline and nearly every functions in the central control of HR modulation (Graveling
potentially stressful situation. The group with autism also & Brooke, 1978; Hutt, Forrest, & Richer, 1975; MacCulloch
VOLUME 21, NUMBER 2, SUMMER 2006
109

Autism
Typical

Baseline Loud noise Remote Unstructured Eating Difficult task Change in Transition Physical
robot time preferred staff exertion
foods

FIGURE 3. Average mean heart rate level by phase for autism and typical groups.

& Williams, 1971), including the vagus nerve (Althaus, Mul- ing situation, and biologically based individual differences, in-
der, Mulder, Aarnoudse, & Minderaa, 1999). More recently, cluding severity of the disorder.
the amygdala, which plays a central role in moderating fear and In light of these cautions, there are methodological
anxiety (Davis & Whalen, 2001), is thought to be abnormal strengths and weaknesses associated with the present study’s
in autism (Baron-Cohen et al., 2000; Schultz, Romanski, & findings. First, several steps were taken to control for arousal
Tsatsanis, 2000; Sweeten, Posey, Shekhar, & McDougle, induced by the testing environment: (a) The preobservation
2002), contributing to improper arousal regulation in this protocol enabled the participants with autism to sample the
population (Amaral, Bauman, & Mills Schumann, 2003). laboratory setting and heart monitor repeatedly prior to the
Although biological preconditions leading to and behav- observation; (b) a relatively noninvasive, wireless HR monitor
ioral observations indicative of overarousal are implicated in that can be worn underneath a garment was used; (c) ob-
autism, one must still reconcile the fact that physiological over- servations were undertaken in a minimally stimulating (e.g.,
arousal does not always replicate in this population. Some ten- incandescent lighting, pattern-free walls and carpet), sound-
tative reasons for this discrepancy have been offered by Zahn proof laboratory; and (d) a familiar person accompanied the
(1986) in an early review of ANS arousal findings in autism: participants throughout the observational sessions. Second,
(a) that most individuals with autism have chronically high lev- several steps were taken to control for arousal artifacts unre-
els of autonomic activity, but that a subgroup within the dis- lated to the independent variables: (a) With the exception of
order may respond at normal levels; (b) that persons with riding the stationary bicycle, participants were seated in a com-
autism may exhibit heightened ANS activity only some of the fortable chair for the duration of the observation to minimize
time; and (c) that physiological studies requiring interaction HR increases associated with physical activity; (b) the HR
with people or that create confusion about what the partici- monitor recorded postural changes and motor movements and
pant is being asked to do can cause study participants to ex- inclusion of this data as a covariate in the statistical analyses
hibit high arousal. Clearly, all of these potential conditions can controlled for HR increases due to recorded physical activity;
vary depending on the experimental research design used, the and (c) participants in this study had normal blood pressure
procedure for gaining compliance, and the sample studied. measurements and were free of medications, ruling out the
Dawson and Lewy (1989) have also suggested that levels of possibility that their arousal responses were affected by abnor-
stimulation can vary across individuals with autism as a func- mal cardiovascular systems or pharmacological agents. Finally,
tion of developmental level, degree of familiarity with the test- a wide sample of potential stressors was used to provide mul-
FOCUS ON AUTISM AND OTHER DEVELOPMENTAL DISABILITIES
110

tiple opportunities for participants to elicit a stress response. pants or environmental stressors, or simply to the act of being
Sampling just one potentially stressful situation may or may observed in a simulated environment.
not have elicited significant physiological reactions across all The individual differences found within the autism and
participants, enabling potentially erroneous conclusions about typically developing groups also demonstrate the advantages
arousal responses in this sample. and complexity inherent in interpreting single-subject data.
While these experimental controls attempt to minimize ex- Nomothetic approaches that classify large, random groups of
traneous variables that can affect measurement of arousal re- people based on an average response statistic to find inter-
sponses in persons with autism, there are a few potential individual variation prevail in psychology. However, this ap-
confounds and limitations associated with the current study proach often yields superficial understanding of any one
that merit future research. For example, there were instances person because limited data are typically collected. In contrast,
across both the autism and control groups where significant idiographic methods (see Molenaar, 2004) that gather single-
cardiovascular reactivity occurred during rest phases. A review subject data, such as those used in the present study, investi-
of the data suggests that these responses might be related to gate a small sample of individuals in detail and focus on a
(a) a carry-over effect from a previous stress condition, (b) cu- person’s uniqueness. Quantitative analysis of idiographic data
mulative arousal mediated by a participant’s relevant cog- highlights intraindividual variation over time to gain a thor-
nitions or emotions, or (c) participant reactivity to being ough and more subtle understanding of a few people to lead
observed in an artificial setting. to more general understanding of others. In this framework,
In the present study, a carry-over effect seems evident in systematic replication (Barlow & Hersen, 1984) becomes the
the autism group for M.L., who showed significant HR re- basis for generalizability. Because the current study only in-
sponses during rest only after a significant response to a pre- cluded five individuals with autism, it is questionable whether
ceding stressor. While representing a potential threat to the the observed HR results and accompanying interpretation of
internal validity of the experimental stressors, this carry-over the data would generalize to a large sample. Therefore, larger
effect suggests that arousal associated with a stressor can ex- sample sizes are needed in future studies to assure more accu-
tend over time even when the stressful stimuli or situation is rate representation of response types in a notoriously hetero-
removed. This phenomenon, if replicated in future studies, geneous population. Continuing research might also recruit
may be of clinical interest as it demonstrates that some indi- participants who have a greater range of functioning abilities
viduals with autism cannot self-regulate their arousal response and might employ standardized, adaptive behavioral measures
to a stressor in a timely manner. that better identify individual differences by differentiating be-
Cumulative stress responses evidenced by increased car- tween high- and low-functioning individuals with autism, a
diovascular reactivity in every previous and subsequent condi- variable that Kootz and colleagues (1982) and Dawson and
tion, typically toward the end of the observation, occurred for Lewy (1989) suggest can mediate arousal responses.
A.F. in the autism group and B.A., D.P., D.V., and S.M. in the Future studies might also make attempts to record and
control group. This pattern of responding may be related to correlate overt behavioral responding with underlying physio-
unobservable thoughts or feelings (e.g., memory of a previous logical functioning to determine if there is synchrony or dy-
stimulating occasion, boredom, anticipation) that are them- synchrony across levels of measurement. Despite the general
selves arousal producing. Although only speculative, this finding of high HR in the participants with autism, anecdotal
hypothesis has some face validity given that this pattern of re- observation of overt behavior in this study indicated only
sponding occurred primarily in the more cognitively able, typ- minor signs of arousal. This is a potentially interesting hap-
ically developing group. It is also possible that these arousal pening that deserves more systematic study given that com-
responses are not related to the environmental stressors per se, munication deficits characteristic of this population require
but to the simple act of being monitored in a laboratory set- educators to make inferences about internal states from overt
ting. For instance, three participants with autism (M.L., S.E., behavioral responses. It may well be that some individuals with
A.F.) and one typically developing individual (B.A.) had basal autism look relatively calm overtly, but are experiencing sig-
HR, prior to any presentation of an experimental stressor, nificant physiological arousal covertly.
equal to or greater than 90 bpm. A nurse on staff at the Gro- Finally, while HR is a robust measure of general physio-
den Center reviewed the medical records of all the participants logical arousal, it is influenced by both sympathetic and
to verify that no one had documented problems with cardio- parasympathetic nervous system activities. Heart rate variabil-
vascular functioning before entry into the study. Therefore, it ity, on the other hand, allows more fine-grained analyses of
is unclear whether these basal rates are accurate estimates of stress on cardiovascular arousal, including the assessment of
resting HR or whether they are artificially high in response to vasovagal tone. Physiological research supports the notion that
being observed in an artificial setting. Future studies that de- HR patterns are predominantly mediated via the vagus nerve
ploy wireless HR monitors in the natural environment might (Levy, 1984). Measures of vagal reactivity to sensory, visceral,
gather data from individuals with autism and indicate whether or cognitive challenges indicate the adaptive functioning of the
the high basal HR and stress response patterns observed in the nervous system. Therefore, measures of cardiac vagal tone can
current study are attributable to characteristics of the partici- provide an important window into the central control of au-
VOLUME 21, NUMBER 2, SUMMER 2006
111

tonomic processes and by inference the central processes nec- ioral Practice. His current interests include the psychophysiology and
essary for organized behavior. Future studies that employ such treatment of emotion and anxiety disorders. Gerald Groden, PhD, is
data may determine if restricted autonomic flexibility (Porges, the cofounder of the Groden Center and is currently on appointment at
1985) contributes to the cardiovascular overarousal found in Brown University and the University of Rhode Island. Address: Mat-
thew S. Goodwin, The Groden Center, Inc., 86 Mt. Hope Ave., Provi-
this study.
dence, RI 02906; e-mail: msgoodwin@earthlink.net
In sum, this study further explores the role that stress,
stress-related anxiety, and physiological arousal play in the be-
havior of individuals with autism. Continuing research that fo- NOTES
cuses on these constructs and addresses the methodological
considerations raised when using HR as a direct measure of 1. Small amounts of food were used so that the entire portion of food
stress will be required to determine if qualitative differences in could be consumed in the time provided.
2. In the analyses, HR data was reduced to 5-second averages to facil-
arousal prevent this population from attending to, processing,
itate graphical representation and statistical testing.
and interacting with their environment and learning norma-
tive behaviors and skills from other people. However, if repli-
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APPENDIX A
Mean Heart Rate Level by Phase for M.L.
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APPENDIX B
Mean Heart Rate Level by Phase for J.L.
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APPENDIX C
Mean Heart Rate Level by Phase for S.E.
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APPENDIX D
Mean Heart Rate Level by Phase for M.C.
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APPENDIX E
Mean Heart Rate Level by Phase for A.F.
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APPENDIX F
Mean Heart Rate Level by Phase for B.A.
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APPENDIX G
Mean Heart Rate Level by Phase for C.N.
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APPENDIX H
Mean Heart Rate Level by Phase for D.P.
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APPENDIX I
Mean Heart Rate Level by Phase for D.V.
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APPENDIX J
Mean Heart Rate Level by Phase for S.M.

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