Animals may act as social buffers: Skin conductance arousal in children with autism spectrum disorder in a social context: Animals and Autism
Abstract
Children with autism spectrum disorder (ASD) experience high rates of social stress and anxious arousal. Preliminary evidence suggests that companion animals can act as buffers against the adverse effects of social stress in adults. We measured continuous physiological arousal in children with ASD and typically developing (TD) children in a social context during four conditions: (a) a baseline of reading silently, (b) a scripted classroom activity involving reading aloud, (c) free play with peers and toys, and (d) free play with peers and animals (guinea pigs). Our results confirmed heightened arousal among children with ASD compared to TD children in all conditions, except when the animals were present. Children with ASD showed a 43% decrease in skin conductance responses during free play with peers in the presence of animals, compared to toys. Thus, animals may act as social buffers for children with ASD, conferring unique anxiolytic effects. © 2015 Wiley Periodicals, Inc. Dev Psychobiol.
© 2015 Wiley Periodicals, Inc.
2 Figures
Animals May Act as Social
Buffers: Skin Conductance
Arousal in Children With
Autism Spectrum Disorder in a
Social Context
ABSTRACT: Children with autism spectrum disorder (ASD) experience high
rates of social stress and anxious arousal. Preliminary evidence suggests that
companion animals can act as buffers against the adverse effects of social stress in
adults. We measured continuous physiological arousal in children with ASD and
typically developing (TD) children in a social context during four conditions: (a) a
baseline of reading silently, (b) a scripted classroom activity involving reading
aloud, (c) free play with peers and toys, and (d) free play with peers and animals
(guinea pigs). Our results confirmed heightened arousal among children with ASD
compared to TD children in all conditions, except when the animals were present.
Children with ASD showed a 43% decrease in skin conductance responses during
free play with peers in the presence of animals, compared to toys. Thus, animals
may act as social buffers for children with ASD, conferring unique anxiolytic
effects. ß2015 Wiley Periodicals, Inc. Dev Psychobiol
Keywords: animal-assisted intervention; arousal; autism spectrum disorder;
children; classroom; electrodermal activity; guinea pigs; human-
animal interaction; skin conductance; social anxiety; social buffer;
typical development
INTRODUCTION
Children with autism spectrum disorder (ASD) experi-
ence significantly more social anxiety than their
typically developing (TD) peers (e.g., Kuusikko et al.,
2008). The developmental pathway to social anxiety for
children with ASD is posited to involve a cyclical
relationship between heightened physiological arousal,
social withdrawal, social skills deficits, and negative
peer interactions. Heightened arousal during social
situations may lead to social withdrawal, which limits
opportunities to develop effective social skills, and may
make children with ASD more sensitive to negative
peer interactions such as those characterized by preju-
dice or rejection (Bellini, 2006). Indeed, children with
ASD experience substantially higher rates of peer
victimization and bullying than their TD classmates
(e.g., Little, 2001). Heightened arousal in social
contexts may also prevent children with ASD from
acquiring social skills and benefiting from targeted
interventions (e.g., Goodwin et al., 2006). One strategy
to reduce arousal in social situations may be to include
a companion animal.
Companion animals can act as buffers against the
adverse effects of social exclusion and social anxiety.
Manuscript Received: 2 September 2014
Manuscript Accepted: 5 March 2015
Correspondence to: Marguerite E. O’Haire
E-mail: mohaire@purdue.edu
Contract grant sponsor: WALTHAM
1
Centre for Pet Nutrition
Contract grant sponsor: Eunice Kennedy Shriver National
Institute of Child Health and Development
Contract grant number: R03HD070683
Contract grant sponsor: The Thomas Meloy Foundation
Contract grant sponsor: The American Australian Association
Contract grant sponsor: The Australia Awards Endeavour
Program
Article first published online in Wiley Online Library
(wileyonlinelibrary.com).
DOI 10.1002/dev.21310 ß2015 Wiley Periodicals, Inc.
Developmental Psychobiology
Marguerite E. O’Haire
1
Samantha J. McKenzie
2
Alan M. Beck
1
Virginia Slaughter
3
1
Center for the Human Animal Bond,
Department of Comparative Pathobiology
College of Veterinary Medicine
Purdue University
West Lafayette, IN, 47907 USA
2
School of Population Health
The University of Queensland
Herston, QLD, 4006 Australia
3
School of Psychology
The University of Queensland
Brisbane, QLD, 4072 Australia
Adults experiencing social exclusion report greater
wellbeing if an animal is present (Aydin et al., 2012).
When shown pictures of identical scenes both with and
without an animal present, adults rate social scenes
with animals as less tense, and the people in them as
more friendly and less threatening (Lockwood, 1983).
The mere presence of an animal appears to change
people’s perception of social contexts, making them
appear less stressful and more positive.
Although a long line of evidence espouses the
benefits of human social support, it appears that in
some instances, the presence of an animal may be
superior to humans in reducing arousal. For example,
when performing a stressful cognitive task, adults show
lower cardiovascular reactivity in the presence of an
animal, compared to a friend, spouse, or being alone
(Allen, Blascovich, & Mendes, 2002). In laboratory
studies designed to induce social stress among strang-
ers, undergraduate students show lower salivary cortisol
and heart rate when an animal is present, compared to
a friend, or being alone (Polheber & Matchock, 2013).
Initial evidence suggests similar findings among chil-
dren. A group of 47 male 7- to 11-year-old children
with insecure attachment participated in the Trier
Social Stress Test, which involves preparing and giving
a short speech to unfamiliar adults. After the task,
children showed the quickest recovery in salivary
cortisol when an animal was present, compared to a
friendly human or toy animal (Beetz, Julius, Turner, &
Kotrschal, 2012). These findings may be due to the
perceived non-judgmental nature of animals. Whereas
human counterparts inherently pass social judgment,
animals are often perceived as sources of unconditional,
positive support. For example, animals do not engage
in the emotionally hurtful behavioral manifestations of
judgment such as teasing, bullying, or insulting people.
Taken together, a growing body of evidence suggests
that the presence of an animal may ameliorate the
adverse physiological effects of social anxiety.
Despite the pervasiveness of social stress and
exclusion among children with ASD, only one study to
date has examined the physiological effect of animals
for children with ASD. In this study, mean cortisol
awakening response was evaluated as a daily indicator
of stress in 42 children aged 3–14 years. Results
revealed significantly lower cortisol awakening
response during four weeks with a service dog in the
home, compared to two weeks prior to the dogs’ arrival
and two weeks after the dogs’ removal (Viau et al.,
2010). These findings suggest that the presence of an
animal can reduce physiological stress in children with
ASD in the home environment; however, the results are
limited and indirect. They do not evaluate whether the
findings are unique for children with ASD compared to
TD children, nor whether the findings are unique to
animals compared to other novel stimuli that could be
introduced into the home.
The current study is the first to directly examine
continuous physiological arousal in children with ASD
and their TD peers in a social context in the presence
of animals compared to other novel stimuli. Arousal
was assessed via skin conductance, which is one of the
most robust and well-studied physiological signals
(Dawson, Schell, & Filion, 2000). It increases in
response to social stress among both children with
ASD and their TD peers (Levine et al., 2012). It has
also been effectively used to distinguish the physiolog-
ical response profiles of children with ASD and their
TD peers with respect to some social stimuli, such as
direct gaze. Compared to faces with averted gaze or
closed eyes, the level of increased arousal to direct
gaze was positively associated with social impairment
in children with ASD, but not their TD peers (Kaarti-
nen et al., 2012). We measured skin conductance for
these reasons and because it is a relatively low-
invasive method compared to taking saliva samples.
The current study is part of a larger project
examining the relationship between human–animal
interactions and the developmental pathways to social
anxiety in ASD. A total of 192 age 5- to 12-year-
old children participated in the study, including 64
children with ASD and 128 classroom-matched TD
children. Guinea pigs were selected as the study animal
due to their small size, to be closely comparable to a
control condition of toys, as well as their suitability to
research in the school classroom environment (Ameri-
can Society for the Prevention of Cruelty to Animals,
2008). Data were collected to reflect each element of
the developmental pathways model for social anxiety in
ASD, including social skills deficits, social withdrawal,
negative peer interactions, and physiological arousal.
Findings revealed that children with ASD showed
global improvements in parent- and teacher-
reported social skills after eight weeks with animals in
the school classroom, compared to a waitlist control
period (O’Haire, McKenzie, McCune, & Slaughter,
2014).
For a subsample of 99 participants (33 with ASD),
naive behavioral observation and skin conductance data
were collected. Children participated in groups of three,
including one child with ASD and two classroom-
matched TD peers. Four conditions were presented,
each designed to mirror the social context of a tradi-
tional classroom setting, where school-age children
spend the majority of their time. Conditions included:
(a) a baseline of reading silently, (b) a scripted
classroom activity involving reading aloud, (c) free
play in the presence of toys, and (d) free play in the
2O’Haire et al. Developmental Psychobiology
presence of animals. Results of the behavioral data
showed that children with ASD exhibited less social
withdrawal and fewer negative peer interactions when
the animals were involved, compared to the toys
(O’Haire, McKenzie, Beck, & Slaughter, 2013). Taken
together, these initial findings suggest that the presence
of an animal ameliorates three of the four components
of the developmental pathways model to social anxiety
in ASD (i.e., social skills, social withdrawal, and
negative peer interactions). It is therefore essential to
evaluate the final component, physiological arousal, as
a potential mechanism for observed behavioral
changes.
Here, we explore the results of the skin conductance
data for both children with ASD and their TD peers.
We predicted that children with ASD would show
higher physiological arousal in all conditions, com-
pared to their TD peers, consistent with elevated rates
of heightened social arousal in children with ASD. Our
main hypothesis was that children with ASD would
show reduced physiological arousal in the presence of
the animals, compared to the other three conditions.
We expected that children with ASD would show
greater decreases in arousal than their TD peers, for
whom an informal social setting would not trigger
heightened arousal.
METHODS
Ethics Statement
All human-related and informed consent protocols were
approved by The University of Queensland’s Human Ethics
Committee and all animal-related protocols were approved by
The University of Queensland’s Animal Ethics Committee.
Approval to approach school principals was granted by the
Queensland Department of Education, Training, and Employ-
ment for state schools and Brisbane Catholic Education for
private schools. Upon written consent from the principal,
teachers, and parents (including next of kin or guardians)
were approached for written consent on behalf of child
participants, who also gave verbal assent.
Participants
Inclusion Criteria. Each participant group consisted of one
target participant with ASD and two TD peers. Inclusion
criteria for participants with ASD included: (a) age between 5
and 13 years; (b) enrolment in a grade K-7 mainstream
classroom, (c) a parent- and teacher-reported diagnosis of
ASD (details below) and (d) no prior parent-reported history
of animal abuse. Given the limited amount of time available
for testing within the school classroom, lengthy diagnostic
instruments such as the Autism Diagnostic Observation
Schedule (ADOS) were replaced with validated parent- and
teacher-report screening instruments. Inclusion criteria for
data analysis were based on two ASD screening instruments,
and included: (a) a score 11 on the Social Communication
Questionnaire (SCQ), which is the optimal cut-off value for
clinical use to indicate the presence of ASD (Norris &
Lecavalier, 2010) and (b) a percentile rank 25 on the Social
Skills Rating System (SSRS) Social Skills domain parent- or
teacher-version to indicate low social skills characteristic of
ASD (Macintosh & Dissanayake, 2006). Alternatively, in the
absence of SCQ data (n¼3) or an SCQ score <11 (n¼3),
the inclusion criterion was set to a more stringent percentile
rank of 5 on SSRS Social Skills. Inclusion criteria for TD
peers included: (a) age between 5 and 13 years, (b) enroll-
ment in a classroom with a target participant with ASD, (c)
no parent- and teacher-reported diagnosis of ASD, and (d) no
prior parent-reported history of animal abuse.
Sample Characteristics. Thirty-eight groups of three chil-
dren (114 children total) participated in the study. Each group
consisted of one target participant with ASD and two TD
peers. Following data collection, five groups were excluded
from data analysis for the following reasons: (a) the child
with ASD changed schools prior to completing data collec-
tion, (b) one of the TD children decided that they did not
want to participate, and (c) three participants with ASD did
not meet the screening criteria for ASD. The final sample
included 33 groups comprised of 99 children from 15
classrooms in four schools throughout the greater Brisbane
area in Australia.
Target participants with ASD included 33 children aged
5.2–12.1 years with a diagnosis of ASD, including Autism
Spectrum Disorder (n¼7), Autistic Disorder (n¼7), Asperg-
er’s Disorder (n¼14), and Pervasive Developmental Disorder
Not Otherwise Specified (n¼5). Diagnoses were made by
independent pediatricians (n¼30), clinical psychiatrists
(n¼2), and clinical psychologists (n¼1). On the SCQ, 18
participants qualified for ASD and 9 qualified for autism. The
remaining six target participants (three scoring <11 and three
missing SCQ data) all scored a percentile rank 5 on SSRS
Social Skills. The sample of TD participants included 66
children aged 5.1–12.7 years with no prior diagnosis of ASD.
No TD children met the criteria for ASD or autism on the
SCQ (all scores 10). Mean participant demographic and
ASD screening data are reported in Table 1.
Procedure
All participants met individually with the researcher (MEO)
prior to the experimental procedure. The initial meeting was
intended to familiarize participants with the researcher and
the study, and to prevent potential novelty effects of a new
person. Children were thus accustomed to the experimenter,
but not to the study materials, prior to the experiment.
Children participated in experimental sessions in groups of
three, including one child with ASD and two randomly
selected TD children from the same classroom. Sessions took
place during school hours in a quiet space outside of the
child’s regular classroom. Four experimental conditions were
administered with each group by the researcher in the same
Developmental Psychobiology Animals and Autism 3
order with the same three participants. Physiological data
were collected continuously throughout all conditions for
both children with ASD and TD children.
Baseline (Reading Silently). A baseline period of reading
silently allowed for participants to adjust to the experimental
setting and to collect physiological data during a quiet
activity among peers. The stimulus material for reading
silently was a child-selected book from their classroom
library. Participants were instructed to engage in reading
silently or browsing for five minutes.
Scripted Activity (Reading Aloud). For participants in
first grade (year one) and beyond, the stressor activity was
reading aloud in front of peers and the experimenter. The
stimulus materials for reading aloud were selected from the
Dynamic Indicators of Basic Literacy Skills (DIBELS) Oral
Reading Fluency, which offers approximately 20 standardized
passages per grade level with high test-retest and alternate-
form reliability (Good, Gruba, & Kaminski, 2002). The
DIBELS Oral Reading Fluency procedure requires each child
to read aloud for one minute. For each group, the selected
passages and reading order were pre-determined through a
computerized randomization procedure. The entire procedure
took approximately 5 min for a group of three children.
For younger children without reading skills (<25% of
sample) the stressor task consisted of an experimenter-
directed coloring task in which children were instructed to
use pre-determined colors in a regimented order to complete
a drawing within a specified time frame.
Toys. The toy condition consisted of 10 min of free play
with peers and toys. The toys included a standardized set of
items, which the children had not previously seen. A variety
of toys was selected for both genders and a range of ages.
Examples include cars, dolls, colored clay, and spinning tops
for use in a plastic battle arena. For a complete listing of the
toys, see O’Haire et al., 2013.
Animals. The animal condition consisted of 10 min of free
play with peers and animals. The animals included two
guinea pigs, which the children had not previously seen.
Guinea pigs were selected as the study animal due to their
small size, to be most comparable to toys. They were
obtained at a young age to enable early socialization to
human handling. Each same-sex pair of guinea pigs was
housed in a large, two-level cage with soft, dry bedding, a
hiding house refuge, and constant access to a fresh supply of
food and water. To ensure that outcomes were not due to an
individual guinea pig, a different pair of guinea pigs was
randomly allocated to each classroom. Children were
instructed prior to the session on how to properly hold guinea
pigs.
Measures
Autism Screening. Two standardized instruments were
administered for ASD screening purposes. The Social Com-
munication Questionnaire (SCQ), formerly known as the
Autism Screening Questionnaire, is the most researched and
well validated parent-report screening tool for ASD (Norris &
Lecavalier, 2010; Rutter, Bailey, & Lord, 2003). It demon-
strates good reliability and validity, and shows strong discrim-
ination between ASD and non-ASD cases, irrespective of
child IQ or parental education (Chandler et al., 2007). The
Social Skills Rating System (SSRS) is a commonly used
parent- and teacher-report tool to assess social functioning. It
demonstrates adequate internal consistency and test-
retest reliability (Gresham & Elliott, 1990). Given diagnostic
deficits in social skills associated with ASD, the SSRS has
been demonstrated as an effective tool to differentiate
individuals with ASD from TD individuals (Norris &
Lecavalier, 2010).
Social Anxiety. The Social Worries Questionnaire (SWQ)
is a 10-item (parent version) and 8-item (teacher version)
survey instrument designed to assess social anxiety in
children (Spence, 1995). It can reliably screen for social
anxiety disorder (Bailey, Chavira, Stein, & Stein, 2006), and
has been used to demonstrate higher social anxiety among
children with ASD compared to TD children (Gillott, Furniss,
& Walter, 2001). On the SWQ, informants are prompted to
rate how often a child avoids or worries about certain social
situations. To provide greater variability of responses, we
expanded the original 0–2 scale to a 0–3 scale (0 ¼never
Table 1. Demographics and Screening Measures for Children With Autism Spectrum Disorder (ASD) and Typically
Developing (TD) Children
Demographics ASD Screening Measures
SCQ Lifetime SSRS Social Skills SSRS Problem Behaviors SSRS Academic
Sex (male) Pet owners
Age (years),
M (SD)
Parent,
M (SD)
Teacher,
M (SD)
Parent,
M (SD)
Teacher,
M (SD)
Parent,
M (SD)
Teacher,
M (SD)
ASD 72.7 % 81.8 % 9.4 (2.3) 18.9 (6.6) 24.4 (24.9) 6.9 (12.2) 75.6 (23.0) 86.1 (19.8) 26.0 (27.8)
TD 42.4 % 72.9 % 9.0 (2.3) 3.7 (2.7) 72.9 (28.7) 53.3 (28.0) 38.1 (27.6) 45.5 (26.9) 50.9 (25.3)
p.004 .214 .465 <.001 <.001 <.001 <.001 <.001 <.001
SCQ, Social Communication Questionnaire; SSRS, Social Skills Rating System; p, comparison between ASD and TD.
4O’Haire et al. Developmental Psychobiology
true, 1 ¼rarely true, 2 ¼sometimes/partially true, 3 ¼usually/
typically true). Higher total scores represent greater social
anxiety. The current study yielded excellent internal reliability
(a¼.93), which is consistent with previous research reporting
a¼.82 (Sofronoff, Attwood, & Hinton, 2005).
Character Description. Parents and teachers were asked to
rate how much they agreed with three character descriptions
about participants. Statements included a social rating (i.e.,
“He/she is social”), confidence rating (i.e., “He/she is
confident”), and calm rating (i.e., “He/she is calm”).
Responses were rated on a 7-point Likert scale (0 ¼strongly
disagree, 1 ¼disagree, 2 ¼somewhat disagree, 3 ¼neither
agree nor disagree, 4 ¼somewhat agree, 5 ¼agree, 6 ¼
strongly agree). Responses were re-coded from 3 to 3 for
ease of interpretation.
Emotional Valence. At the end of the study, children were
asked to report how they felt during each condition on a 1-5
Likert scale with faces (1 ¼,2¼,3¼,4¼,
5¼). Questions began with, “How do you feel when you
are…” and conditions included “reading quietly,” “reading
aloud,” “with the toys,” and “with the guinea pigs.”
Skin Conductance. Physiological arousal was assessed via
electrodermal, eccrine sweat gland activity, which indicates
sympathetic nervous system arousal. Skin conductance data
were collected using wireless, wristband sensors designed for
continuous assessment in naturalistic settings (Q Sensor,
Affectiva Inc., Waltham, MA). Skin conductance recordings
from the central wrist are highly correlated with more
traditional, laboratory-based measurements on the fingertips,
mean r¼.574 (van Dooren, de Vries, & Janssen, 2012).
To reduce motion artifacts and electrical noise, raw skin
conductance data were smoothed using a 5-second Hanning
window and then filtered using a zero-phase first order
Butterworth filter with a normalized cut-off frequency of
0.05 Hz (Bach, Friston, & Dolan, 2013). Next, continuous
decomposition analysis was used to extract skin conductance
components based on standard deconvolution (Benedek &
Kaernbach, 2010). Extracted components included non-
specific skin conductance responses (SCRs) and skin con-
ductance level (SCL). Each represents a unique indicator of
autonomic arousal. Skin conductance responses (SCRs) are
indicative of phasic activity; they show the “phases” or abrupt
increases in skin conductance. Skin conductance level (SCL)
is indicative of tonic activity; it shows the overall “tone” of
the slow-changing, background skin conductance level. In
both cases, higher levels represent greater physiological
arousal.
The sensor sampling rate was set to 8 Hz and skin
conductance measurements are provided in microSiemens
(mS). The minimum amplitude threshold for SCRs was set to
0.01 mS (Boucsein et al., 2012). SCRs are reported as the
number of significant (above threshold) non-specific skin
conductance responses per minute. SCL is reported as the
square-root-transformed mean of the decomposed tonic skin
conductance component.
Skin Temperature. Skin temperature (˚C) was assessed via
the wristband electrode, which approximates the temperature
underneath the sensor.
Motor Movement. A tri-axial accelerometer (g) within the
wristband device was used to estimate movement during
experimental sessions. Tri-axial accelerometers assess motion
in the anteroposterior (x-axis), mediolateral (y-axis), and
vertical (z-axis) planes. Motor movement was calculated as
the sum of the absolute values of motion change in each
direction.
Data Analysis
Prior to examining the primary hypotheses, we checked for
differences between ASD and TD participants on the two
ASD screening measures (SCQ raw scores and SSRS
percentile ranks) in order to provide additional validation of
parent- and teacher-reported ASD diagnoses. We also checked
for differences on potentially confounding demographic
variables (age, gender, and pet ownership status) as well as
social anxiety measures (SWQ raw scores and parent and
teacher ratings). Independent samples ttests were conducted
for continuous variables and x
2
tests were used for categorical
variables. We examined participants’ self-reported emotional
valence using a repeated measures analysis of variance
(ANOVA) with the between-subjects variable of diagnosis
(ASD, TD) and the within-subjects variable of condition
(reading silently, reading aloud, toys, and animals).
To account for the nested study design (i.e., multiple
conditions nested within individuals nested within classrooms
with different guinea pigs), we used specialized hierarchical
analyses (Raudenbush & Bryk, 2002). Hierarchical linear
modeling (HLM) was used for the continuous variable of
SCL and hierarchical generalized linear modeling (HGLM)
was used for the count data variable of number of SCRs per
minute. We conducted a series of three-level models, where
the levels reflected repeated measurements (Level 1), individ-
ual effects (Level 2), and classroom or guinea pig effects
(Level 3). Random effects in the model were identified as
intercepts at the repeated measures effect of condition (to
account for correlations between repeated observations of the
same participant across conditions) as well as intercepts at the
individual-level (to account for variance across individuals)
and classroom-level (to account for correlation between
individuals in the same classroom with the same guinea pigs).
We addressed our primary hypotheses, that in the animal
condition, children with ASD would show reduced physio-
logical arousal relative to the other conditions and relative to
their TD peers, by including the fixed effects of experimental
condition (reading silently, reading aloud, toys, and animals),
diagnosis (ASD, TD), and the interaction between diagnosis
and condition. To control for potential covariates and their
interaction with condition, we included the additional fixed
factors of age, pet ownership, parent- and teacher-
reported social anxiety (SWQ scores), skin temperature,
motor movement, and the interaction between each of these
factors and experimental condition. Continuous variables
were grand-mean centered prior to mixed model analyses.
Developmental Psychobiology Animals and Autism 5
Skin conductance data were processed using Ledalab
Version 3.4.3 (see Benedek & Kaernbach, 2010) in MATLAB
Version 7.13 (MathWorks, Natick, MA). Tests of statistical
significance were conducted using SPSS Version 21 (IBM,
Armonk, NY). All tests were two-tailed with a significance
level of a<.05. Post-hoc analyses were conducted using the
Bonferroni correction (Tabachnick & Fidell, 2012). HLM
results are reported as unstandardized betas with 95%
confidence intervals to indicate differences in SCR and SCL
across conditions and diagnosis. Effect sizes were calculated
using the corrected formula for Cohen’s din hierarchical
linear models, which divides the estimated mean difference
by the pooled raw standard deviation (Feingold, 2009). Values
greater than 0.20, 0.50, and 0.80 were interpreted as small,
medium, and large, respectively (Cohen, 1988).
RESULTS
Social Anxiety
Results showed significant differences in social anxiety
between participants with ASD and their TD peers
(Table 2). Participants with ASD scored significantly
higher on the SWQ on both the parent-version, t
(94) ¼9.49, p<.001, and the teacher-version, t
(97) ¼4.34, p<.001, indicating greater anxiety and
worry about social situations. Participants with ASD
also scored significantly lower on character descriptions
as social (parent: t(94) ¼6.26, p<.001, teacher: t
(97) ¼7.57, p<.001), confident (parent: t(94) ¼4.81,
p<.001, teacher: t(97) ¼4.69, p<.001), and calm
(parent: t(94) ¼3.99, p<.001, teacher: t(96) ¼5.59,
p<.001); thus, both parents and teachers perceived
children with ASD to have greater social anxiety and to
be less social, confident, and calm than their TD peers.
Emotional Valence
Children’s self-reported emotional valence during each
condition was explored with a 2 (diagnosis: ASD, TD)
4 (condition: reading silently, reading aloud, toys,
and animals) repeated-measures ANOVA. Means and
standard deviations are reported in Table 3. Results
showed a main effect for condition, F(3, 291) ¼39.52,
p<.001, but no main effect for diagnosis, F(1,
97) ¼2.38, p¼.126. The interaction between diagnosis
and condition was non-significant, F(3, 291) ¼0.68,
p¼.566; thus, there were no differences in self-
reported emotional valence between children with ASD
and TD children in any condition. Bonferroni-
adjusted post-hoc testing for condition revealed that
children felt the best when with the animals, with large
effects compared to toys (p<.001, d¼0.91), reading
silently (p<.001, d¼1.30), and reading aloud
(p<.001, d¼1.50). They also felt better when playing
with toys, with small to medium effects compared to
reading silently (p¼.045, d¼0.36), and reading aloud
(p<.001, d¼0.65). Taken together, children who
participated in the study reported feeling the best when
with the animals, followed by toys, reading silently,
and reading aloud (Fig. 1).
Skin Conductance
Random Effects. The three-level hierarchical models
we conducted accounted for within-participant variance
across repeated assessments (Level 1), between-
participant variance across individuals (Level 2), and
between-classroom variance (Level 3). Results showed
that the random effect of classroom with different
guinea pigs was not significant for either model (SCR:
p¼.087, SCL: p¼.073; Table 3). Thus, there was no
significant variability in outcomes across classrooms or
guinea pigs. However, results were significant for the
random effects of between-participant variance and
within-participant variance in both models (all
p’s <.001). These findings indicate that the use of
hierarchical models was appropriate to account for
heterogeneity across individual participants and
repeated measurements across conditions (Table 4).
Main Effect of Condition. Across all participants, the
presence of animals was related to decreased skin
conductance. When children were with animals, the
mean number of SCRs per minute was lower than
when they were with toys (p<.001, d¼0.28), reading
aloud (p<.001, d¼0.22), and reading silently
Table 2. Social Anxiety Means (and Standard Deviations) by Diagnosis
SWQ Social Worries Social Rating Confidence Rating Calm Rating
Teacher Parent Teacher Parent Teacher Parent Teacher Parent
ASD 12.7 (6.2) 18.8 (5.8) 0.4 (1.7) 0.2 (1.7) 0.1 (1.9) 0.2 (1.9) 0.5 (1.7) 0.2 (2.0)
TD 6.7 (6.6) 7.8 (5.1) 2.2 (0.8) 1.7 (1.2) 1.6 (1.3) 1.3 (1.2) 2.1 (1.1) 1.3 (1.5)
p<.001 <.001 <.001 <.001 <.001 <.001 <.001 <.001
SWQ, Social Worries Questionnaire; ASD, autism spectrum disorder; TD, typically developing; p, comparison between ASD and TD.
6O’Haire et al. Developmental Psychobiology
(p<.001, d¼0.21). Children showed fewer abrupt
increases in sympathetic activity during the animal
condition, compared to all other conditions. This
pattern of results was less pronounced in SCL, for
which the animal condition was significantly lower
than the toy condition only (p¼.049, d¼0.34). The
main effect of condition revealed that all children had a
lower general state of arousal in the presence of
animals compared to toys.
Main Effect by Diagnosis. For children with ASD,
Bonferroni-adjusted post-hoc analyses revealed the
same pattern of results with medium to large effects
(Fig. 2). On average, children with ASD showed 43%
fewer skin conductance responses (SCR) per minute in
the presence of animals, compared to toys in a social
context. SCRs were significantly lower during animal
presence compared to toys (p¼.007, d¼0.96), reading
aloud (p¼.015, d¼0.58), and reading silently
(p¼.017, d¼0.58), and SCL was significantly lower
during animal presence compared to toys (p¼.025,
d¼0.51), but not reading aloud (p¼.271) or reading
silently (p¼.155). Among TD children, Bonferroni-
adjusted post-hoc analyses showed no significant differ-
ences across conditions for SCRs (all p’s >.237) and
an inverse pattern of results for SCL with small effects.
With respect to general arousal, TD children showed
greater SCL in the presence of animals, compared to
all other conditions, including toys (p¼.022, d¼0.31),
reading aloud (p¼.031, d¼0.30), and reading silently
(p¼.031, d¼0.31). Thus, the presence of animals
reduced general arousal (SCL) and the number of
arousal peaks (SCRs) for children with ASD, but
increased general arousal (SCL) among TD children.
Interaction Between Diagnosis and Condition. Chil-
dren with ASD showed greater physiological arousal
than their TD peers in all conditions where the animal
was not present, including toys (SCR: p<.001, d¼-
0.26; SCL: p<.001, d¼-0.89), reading aloud (SCR:
p¼.005, d¼0.21; SCL: p¼.008, d¼0.67), and
reading silently, (SCR: p<.001, d¼0.26; SCL:
p¼.003, d¼0.75). However, this pattern reversed
when the animal was present. Children with ASD
showed lower arousal than their TD peers in the
presence of animals (SCR: p¼.007, d¼0.19; SCL:
p¼.049, d¼0.46). The interaction between diagnosis
and condition demonstrated that the presence of
animals reduced both the general level of arousal
(SCL) and the number of arousal peaks (SCRs) in
children with ASD compared to their TD peers.
DISCUSSION
This study presents the first evaluation of physiological
arousal in the presence of animals for children with
ASD, compared to their TD peers. The results con-
firmed that children with ASD showed significantly
higher skin conductance, indicative of physiological
arousal, than TD children across the baseline, reading
aloud and free play with toys conditions. This was
consistent with parent- and teacher-reports indicating
greater ongoing social anxiety in children with ASD
compared to their TD peers. The results also supported
our primary hypothesis that children with ASD would
show reduced physiological arousal during peer inter-
action when animals were present, compared to toys,
Table 3. Emotional Valence Means (and Standard
Deviations) by Experimental Condition and Diagnosis
Reading Silently Reading Aloud Toys Animals
ASD 3.8 (1.2) 3.5 (1.3) 4.2 (1.0) 4.9 (0.3)
TD 4.1 (0.8) 3.7 (1.1) 4.4 (0.9) 4.9 (0.3)
ASD, autism spectrum disorder; TD, typically developing.
FIGURE 1 Child-reported emotional valence by experi-
mental condition. Higher values indicate a more positive
emotional valence. Horizontal significance bars show differ-
ences between conditions, using the Bonferroni-adjusted p-
values of *p<.05 and *** p<.001. There were no significant
differences between children with autism spectrum disorder
(ASD) and typically developing (TD) children for any
condition. Error bars represent standard error of the mean.
Developmental Psychobiology Animals and Autism 7
and compared to reading aloud and reading silently in a
social context. Effect sizes were in the medium to large
range for children with ASD. These outcomes were
independent of differences across classrooms, guinea
pigs, individuals, repeated assessments, age, pet owner-
ship, parent- and teacher-reported social anxiety, skin
temperature, and general motion. The findings suggest
that the presence of an animal confers a unique
anxiolytic effect for children with ASD.
Previous studies with this population and other
children with ASD have demonstrated that the presence
of an animal is related to increased social skills (e.g.,
Carlisle, 2014; O’Haire et al., 2014), less social with-
drawal, and fewer negative social interactions (e.g.,
Berry, Borgi, Francia, Alleva, & Cirulli, 2012; Gabriels
et al., 2012; O’Haire et al., 2013). These outcomes
represent three components of the proposed develop-
mental pathway to social anxiety in ASD. The present
study evaluated the final component of the model–
physiological arousal. Results showed reduced arousal
related to animal presence in a social context. Reduc-
tions in heightened arousal may provide a feasible
mechanism for observed increases in social behavior in
children with ASD. With lower arousal levels, children
with ASD may feel more at ease and amenable to
positive peer interaction.
Reduced arousal during animal presence in social
settings may be due to the perceived non-
judgmental nature of animals, which are often reported
as comforting and supportive sources for children
(McNicholas & Collis, 2001). Children with ASD may
be in particular need of additional support given that
they may be bullied and isolated from their TD peers
(e.g., Rowley et al., 2012). The positive nature of the
animals’ presence in the current study is evidenced by
children’s self-reported emotional valence. Both chil-
dren with ASD and TD children reported feeling the
best when they were with the animals, with large effect
sizes compared to toys, reading aloud, and reading
silently. Interestingly, the elation experienced by both
groups of children differentially influenced their phys-
iological response. Children with ASD showed reduced
Table 4. Skin Conductance Outcomes by Experimental Condition and Diagnosis
Effect (Reference Category)
Skin Conductance Responses (SCR) Skin Conductance Level (SCL)
b(SE) t95% CI db(SE) t95% CI d
Fixed Effects
Condition (Animal)
Total Sample
Reading Silently 1.10 (0.29) 3.89*** 0.55, 1.66 0.21 0.19 (0.14) 1.38 0.08, 0.47 0.23
Reading Aloud 1.12 (0.28) 3.96*** 0.57, 1.67 0.22 0.16 (0.14) 1.14 0.12, 0.44 0.20
Toys 1.45 (0.28) 5.09*** 0.89, 2.00 0.28 0.28 (0.14) 1.98* 0.00, 0.56 0.34
ASD only
a
Reading Silently 2.95 (1.23) 2.40* 0.22, 5.67 0.58 0.28 (0.14) 1.95 0.00, 0.56 0.36
Reading Aloud 2.97 (1.23) 2.42* 0.22, 5.71 0.58 0.24 (0.14) 1.69 0.04, 0.53 0.32
Toys 4.97 (1.85) 2.68* 0.53, 9.40 0.96 0.39 (0.15) 2.65* 0.10, 0.67 0.51
TD only
a
Reading Silently 1.25 (0.71) 1.76 2.96, 0.46 0.24 0.26 (0.09) 2.87* 0.45, -0.08 0.31
Reading Aloud 0.05 (0.78) 0.06 1.49, 1.59 0.01 0.25 (0.09) 2.75* 0.43, -0.07 0.30
Toys 0.22 (0.78) 0.29 1.53, 1.97 0.04 0.26 (0.09) 2.92* 0.44, -0.09 0.31
Condition x Diagnosis (ASD)
Reading Silently 1.39 (0.37) 3.74*** 2.12, -0.66 0.26 0.55 (0.18) 2.95** 0.91, -0.18 0.75
Reading Aloud 1.04 (0.37) 2.80** 1.76, -0.31 0.21 0.49 (0.19) 2.66** 0.86, -0.13 0.67
Toys 1.36 (0.36) 3.75*** 2.07, -0.65 0.26 0.65 (0.18) 3.53*** 1.01, -0.29 0.89
Animals 0.97 (0.36) 2.71** 0.27, 1.67 0.19 0.39 (0.20) 1.99* 0.00, 0.77 0.46
b(SE) Wald Z 95% CI b(SE) Wald Z 95% CI
Random Effects
Classroom 0.28 (0.17) 1.71 0.09, 0.89 0.11 (0.06) 1.79 0.04, 0.33
Individual 0.60 (0.13) 4.55*** 0.39, 0.93 0.21 (0.04) 5.21*** 0.15, 0.31
Repeated Measures 0.63 (0.07) 9.59*** 0.51, 0.77 0.18 (0.02) 11.55*** 0.15, 0.21
Both models controlled for age, pet ownership, parent- and teacher-reported social anxiety, skin temperature, and motor movement.
SCR, skin conductance responses per minute; SCL, skin conductance level in mS; b, unstandardized coefficient; SE, standard error; CI,
confidence interval; d ¼Cohen’s d; ASD, autism spectrum disorder; TD, typically developing.
a
Bonferroni-adjusted post-hoc analyses; * p<.05; ** p<.01; *** p<.001.
8O’Haire et al. Developmental Psychobiology
arousal in the animals’ presence, while TD children
showed increased arousal in the animals’ presence.
Differential physiological responding to positive emo-
tions has also been demonstrated in previous research.
For example, one study evaluated participants with
high and low social speech anxiety. All participants in
the study reported feeling most positive when viewing
an image of a person with a joyful expression.
However, positive feelings manifested differentially in
physiological outcomes across groups. Individuals with
high social anxiety showed decreased SCL in response
to the positive stimuli while individuals with low social
anxiety showed increased SCL in response to the
positive stimuli (Vrana & Gross, 2004).
These differences mirror findings in the current
study. Children with ASD had high social anxiety,
and the presence of a positive stimulus (animals)
resulted in lower SCL. In contrast, TD children had
low social anxiety, and the presence of a positive
stimulus resulted in higher SCL. For children with
ASD, the stressful nature of social interaction may
have been ameliorated by animal presence, resulting
in relatively lower skin conductance. For TD children,
the neutral setting may have been enhanced by the
excitement of a novel animal, resulting in relatively
higher skin conductance.
It is noteworthy that increased arousal for TD
children was not seen in skin conductance responses
(SCR), but only in skin conductance level (SCL).
Recent data have elucidated different neural mecha-
nisms for SCRs and SCL (Nagai, Critchley, Feather-
stone, Trimble, & Dolan, 2004). SCRs are related to
activation in the amygdala, and increase with activities
involving emotional processing and mental burden
(Patterson II, Ungerleider, & Bandettini, 2002; Wil-
liams et al., 2001). In the current study, children with
ASD showed more SCRs than their TD peers during all
conditions without animals. Navigating and engaging
in a social context may be a more emotionally complex
and mentally burdensome task for children with ASD
compared to their TD peers. However, when the
animals were present, children with ASD showed fewer
SCRs compared to other conditions, indicating that
they may have felt less burdened when they were with
the animals. In contrast, TD children showed no differ-
ences in SCRs across conditions. Thus, it is likely that
they experienced no differences in emotional process-
ing and mental burden across conditions. However, TD
children did show increased SCL when the animals
were present. Increases in SCL are related to decreased
activity in the ventromedial prefrontal cortex, which
occurs when individuals are orienting to external cues
or engaging in an attention-demanding task (Nagai
et al., 2004). Indeed, the presence of a novel animal
FIGURE 2 Skin conductance by experimental condition.
Panels represent (a) skin conductance responses (SCR) in
number per minute and (b) skin conductance level (SCL) in
mS. Vertical significance bars show differences between
children with autism spectrum disorder (ASD) and typically-
developing (TD) children at each time point, where *p<.05,
**p<.01, and ***p<.001. Horizontal significance bars show
differences between conditions for participants with ASD
(above lines) and TD participants (below lines) using
Bonferroni-adjusted p-values. Error bars represent standard
error of the mean.
Developmental Psychobiology Animals and Autism 9
may have offered a captivating external stimulus for
TD children, for whom the social environment was less
emotionally and mentally challenging.
The issue of novelty in the current study may be
considered a limitation. The children were exposed to a
new animal, compared to a new set of toys. It is likely
that over time, physiological responses to the novel
stimuli would habituate, possibly at different rates.
Existing data suggest that roughly half of teachers have
had an animal in their classroom at some stage (Daly
& Suggs, 2010; Rud & Beck, 2003). We suspect that
nearly all teachers have had toys in their classroom.
Given that animals may be less common, the arousal
patterns that we observed in the presence of animals, in
particular, could change over repeated assessments.
Further studies should include longitudinal data on
physiological responses to animals in order to evaluate
potential novelty effects of the presence of a new
animal, and to assess whether the presence of a familiar
animal also has anxiolytic effects for children with
ASD in social settings. It will also be informative in
future studies to directly connect physiological data to
specific behaviors to determine whether certain behav-
ioral patterns and activities characterize interactions in
the presence of animals, and how these behaviors may
be related to physiological arousal.
In conclusion, the current study demonstrates that
the presence of animals in a social context reduces
autonomic arousal among children with ASD. This
arousal-reducing effect of animals appears to be unique
for children with ASD, compared to their TD peers,
possibly because social situations are inherently more
arousal-inducing for children with ASD. Furthermore,
the animals induced positive emotions among children
with ASD. The combination of reduced arousal and
increased positive emotion may create an effective
environment for targeted social skills interventions.
Further investigation will be necessary to evaluate the
application of these findings to targeted therapeutic
protocols. The present findings suggest that this is a
worthwhile avenue for ongoing study and they contrib-
ute to a growing body of literature suggesting that
animals may function as effective social buffers for
individuals with ASD (O’Haire, 2013).
NOTES
The content is solely the responsibility of the authors and does
not necessarily represent the official views of the Eunice
Kennedy Shriver National Institute of Child Health and Human
Development or the National Institutes of Health. The funders
had no role in study design, data collection and analysis, decision
to publish, or preparation of the manuscript. We thank the
RSPCA Queensland, the Queensland Government Department of
Education, Training, and Employment, and Brisbane Catholic
Education for their assistance with school recruitment. We are
also grateful to the dutiful research assistants and volunteers who
assisted in data collection and coding, especially Fatima Issa,
Jinny Hong, Laura Fitzalan, and Sharlene Teo.
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- CitationsCitations10
- ReferencesReferences46
- Although the anxiety reducing effects of horses are not well studied, the anxiety reducing effects of the presence of a dog is of growing scientific interest, and deserves further investigation. Many reports indicate that dogs can bring a calming effect to human arousal37383913] , but some evidence is contrary to this indicating that dogs have an excitatory effect [40], or no effect [41] . A further possibility is that the presence of an animal may help to improve adaptability by increasing family freedom and ensuring child safety.
[Show abstract] [Hide abstract] ABSTRACT: Scientific literature exploring the value of assistance dogs to children with autism spectrum disorder (ASD) is rapidly emerging. However, there is comparably less literature reporting the effects of pet (as opposed to assistance) dogs to these children. In particular, there are no known validated scales which assess how children may alter their behaviours in the presence of the dog, to evaluate the efficacy of pet dogs to these families. Additionally, given the highly individualised nature of ASD it is likely that some children and families gain more benefits from dog ownership than others, yet no research has reported the effect of individual differences. This pilot study reports the development of a 28-item scale based on the perceived impact of a pet dog on a child with autism by parents (Lincoln Autism Pet Dog Impact Scale-LAPDIS). The scale is comprised of three mathematically derived factors: Adaptability, Social Skills and Conflict Management. We assessed how individual differences (aspects) may be associated with scores on these three factors. Family Aspects and Dog Aspects were not significantly associated with ratings on the three factors, but Child Aspects (including: contact with horses, child age, disability level and language abilities) were related to impact of the dog on all factors. Training Aspects were related to scores on Social Skills (formal training with children with ASD and dogs and attendance at PAWS workshops run by Dogs for Good). These results suggest that individual differences associated with the child and the training approach may be important considerations for a positive impact from dog ownership on families with children with ASD. Differences in family features and the dog may not be so important, but may be worthy of further investigations given the early stage of development in this field.- Results of two of the four RCTs were non-significant in terms of behavior or emotional state (e.g., self-reported loneliness, anger, or boredom (Conniff et al., 2005 ) and coping and subjective wellbeing (Boshoff et al., 2015). The third RCT, by Pendry et al. (2014), found significant differences in favor of the intervention group with respect to social competence and behavior, while the fourth, by O'Haire et al. (2015), found significant improvements in social skills based on teacher, but not parent report, and reductions in problem behaviors based upon both teacher and parent report, but no significant changes in academic competence based upon teacher report. Among the four non-RCT controlled studies, one found significant improvements in alertness in the intervention group (Prothmann et al., 2006).
[Show abstract] [Hide abstract] ABSTRACT: To systematically review experimental evidence regarding animal-assisted therapies (AAT) for children or adolescents with or at risk for mental health conditions, we reviewed all experimental AAT studies published between 2000–2015, and compared studies by animal type, intervention, and outcomes. Studies were included if used therapeutically for children and adolescents (≤21 years) with or at risk for a mental health problem; used random assignment or a waitlist comparison/control group; and included child-specific outcome data. Of 1,535 studies, 24 met inclusion criteria. Of 24 studies identified, almost half were randomized controlled trials, with 9 of 11 published in the past two years. The largest group addresses equine therapies for autism. Findings are generally promising for positive effects associated with equine therapies for autism and canine therapies for childhood trauma. The AAT research base is slim; a more focused research agenda is outlined.- [Show abstract] [Hide abstract] ABSTRACT: Within the last 3 decades, studies across a wide range of disciplines have provided evidence that the human-animal bond can contribute to good health, psychosocial well-being, and recovery from serious medical conditions. The purpose of this article is to provide a description of animal-assisted group therapy (AAGT) in terms of its applicability in an outpatient community mental health setting serving dually diagnosed adults. The results of this exploratory study are addressed in terms of member demographics, group description and preparation, group procedures, structure and format, primary clinical interventions, and directions for future research. Furthermore, a conceptual framework for facilitating the incorporation of animals in therapeutically meaningful ways within a group modality is described. Patient testimonials, clinical observations, and preliminary results of a brief stress measure indicate that the power of AAGT is greater than simply a reduction in self-reported stress. While future research is needed to support and expand on these findings, this study provides preliminary evidence indicating AAGT as an efficacious treatment option for individuals seeking relief from a wide range of stressors in a mental-health setting. A final aim of this study is to provide a general framework that can be replicated to motivate and inform interested providers in their efforts to collaborate with local animal-assisted therapy programs, expand group therapy options, and stimulate further research.
- [Show abstract] [Hide abstract] ABSTRACT: Previous research has demonstrated that both children and dogs might benefir from Animal-Assisted Activities (AAA), with some factors mediating/ moderating the results. The present study took these factors into consideration, by creating an AAA program consisting of two types of human-animal interactions (structured and unstructured activities), with an accent being put on the encouragement of positive behaviors. Differences in the frequency of behavioral indicators of positive affects were compared between sessions, in both species (humans and dogs). The preliminary analysis of the results indicated no significant differences between the structured and unstructured sessions in regards of the behavioral indicators of positive affects in humans and dogs, concluding that children and dogs enjoyed the activities in both types of sessions. A more in depth statistical analysis is currently being performed.
- [Show abstract] [Hide abstract] ABSTRACT: Background Despite growing interest in the value of human-animal interactions (HAI) to human mental and physical health the quality of the evidence on which postulated benefits from animals to human psychological health are based is often unclear. To date there exist no systematic reviews on the effects of HAI in educational settings specifically focussing on the perceived benefits to children of reading to dogs. With rising popularity and implementation of these programmes in schools, it is essential that the evidence base exploring the pedagogic value of these initiatives is well documented. Methods Using PRISMA guidelines we systematically investigated the literature reporting the pedagogic effects of reading to dogs. Because research in this area is in the early stages of scientific enquiry we adopted broad inclusion criteria, accepting all reports which discussed measurable effects related to the topic that were written in English. Multiple online databases were searched during January-March 2015; grey literature searches were also conducted. The search results which met the inclusion criteria were evaluated, and discussed, in relation to the Oxford Centre for Evidence Based Medicine levels of evidence; 27 papers were classified as Level 5, 13 as Level 4, 7 as Level 2c and 1 as Level 2b. Conclusion The evidence suggests that reading to a dog may have a beneficial effect on a number of behavioural processes which contribute to a positive effect on the environment in which reading is practiced, leading to improved reading performance. However, the evidence base on which these inferences are made is of low quality. There is a clear need for the use of higher quality research methodologies and the inclusion of appropriate controls in order to draw causal inferences on whether or how reading to dogs may benefit children’s reading practices. The mechanisms for any effect remain a matter of conjecture.
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