The authors tested susceptibility to
contagious yawning in 120 children, 1-6 years,
to identify the time course of its emergence
during development. Results indicated a
substantial increase in the frequency of
contagious yawning at 4 years. In a second
study, the authors examined contagious yawning
in 28 children with autism spectrum disorders
(ASD), 6-15 years. Children with ASD showed
diminished susceptibility to contagious yawning
compared with 2 control groups matched for
mental and chronological age, respectively. In
addition, children diagnosed with Pervasive
Developmental Disorder, Not Otherwise Specified
(PDD-NOS) a milder variant of autism, were more
susceptible to contagious yawning than were
children diagnosed with full Autistic Disorder.
The authors explore the implications of these
findings for theories about the development of
mimicry and emotional contagion.
Contagion refers to the tendency of a
particular behavior to spread through a group in
a "chain reaction." The behaviors that most
often trigger contagious reactions in others are
those that signify the inner states of others
(Hatfield, Caccioppo, & Rapson, 1994). For
example, infants in hospital nurseries begin to
cry when they hear other babies crying (Hoffman,
1978; Simner, 1971), and laugh tracks accompany
most television situational comedies because
hearing the laughter of others prompts our own
laughter (Bush, Barr, McHugo, & Lanzetta,
1989; Provine, 2000). Similarly, seeing another
person yawn, thinking about yawning, reading the
word yawn, or even hearing the word can elicit a
yawn in 40%-60% of normal adults when exposed to
such stimuli under experimental conditions
(Baenninger & Greco, 1991; Platek, Critton,
Myers, & Gallup, 2003; Provine, 1989). Such
forms of behavioral contagion may reflect or
facilitate emotional contagion, which refers to
the tendency of individuals to converge
emotionally with those around us. The property
of contagion, as applied to emotions, offers
psychologists an opportunity to study the roots
of automatic social behaviors that potentially
lay the foundations for the development of
empathy.
At least one mechanism by which emotional
contagion comes about is via the underlying
processes of mimicry and afferent feedback
(Hatfield et al., 1994). Whereas imitation
involves the conscious, effortful reproduction
of another's behavior, mimicry refers to
nonvolitional "matching" behavior (Want &
Harris, 2002). As we interact with someone, we
often subconsciously mimic (often at a level
undetectable to the naked eye or ear) their
facial expressions, bodily postures, and speech
patterns (see Niedenthal, Barsalou, Ric, &
KrauthGruber, 2005, for a review).
When a person mimics, the activation of his
or her emotional body schemas also creates an
emotional reaction that corresponds to the
movements being mimicked (i.e., the act of
smiling causes us to feel happier). This was
first known as facial feedback (Capella, 1993),
but research has now documented similar effects
for gesture, posture, and vocal prosody (see
McIntosh, 1996, for a review), and so may be
more accurately referred to as afferent feedback
(Hatfield et al., 1994). The coupling of our
automatic tendency to mimic others and the
effects of afferent feedback on our own
emotional states may explain the ubiquity of
emotional contagion: Because we unconsciously
match the emotional movements of others, we
unconsciously feel the emotions of others as we
interact with them. Similarly, this account of
mimicry may explain its psychological utility:
Emotional contagion may allow human beings to
intuit the feelings of those around us when we
interact socially (Rogers & Williams,
2006).
Yawning is a type of mimicry in that it is a
matching behavior that is produced
unconsciously. The robust effects for contagious
yawning found by Provine et al. (1986) when they
exposed participants to videos of people yawning
disappeared when the participants knew they were
being watched (Provine, 2005), supporting the
idea that contagious yawning is an unconscious
process that may actually be suppressed by
conscious awareness. However, contagious yawning
appears to be a special kind of mimicry. Unlike
the miniscule muscular movements, often
undetectable to the naked eye, that mimicry
typically entails, yawns-large, obvious
sequences of movements, difficult to stop once
initiated and lasting for up to 10 s-are a very
visible result of such mimicry. The explanation
for this may derive from the fact that yawning
is a fixed action pattern (Provine, 1986). A
fixed action pattern is a species-typical
behavioral sequence that is indivisible and,
once initiated, runs to completion. Fixed action
patterns are invariant and are triggered by a
neural network called the "innate releasing
mechanism" in response to a "sign stimulus" or
"releaser" (in this case, the yawns of others
act as an innate releasing mechanism; Tinbergen,
1951). Perhaps the phenomenon of contagious
yawning can be explained by the idea that
mimicking the first part of a fixed action
pattern (as would be expected if one were
mimicking the facial expressions or
vocalizations of a conspecific as he or she
begins to yawn) is likely to trigger the release
of the entire behavior.
In addition to being a form of mimicry,
contagious yawning appears to involve an
emotional component. Deputte (1994) identified
two contexts for yawns: the "rest yawn" observed
when the context involves a change in arousal
level, and the emotion yawn (which he noted
could also be referred to as a "social yawn").
He defined the emotion yawn as an action used as
an unconscious communication of psychological
decompression after a state of high alert.
Yawning is also similar to the other highly
contagious acts of crying and laughing, both of
which represent emotional states, in that it
produces a distinct sound, as well as a distinct
facial expression (Provine, 1996). The existence
of an emotion yawn suggests that contagious
yawning may be considered a form of emotional
contagion. On the other hand, yawning may not
signal an emotion but may simply be a facial
expression that is unintentionally mimicked, as
are other nonemotional facial expressions
(Heyes, 2001). If so, then its contagiousness
may simply be a by-product of ubiquitous facial
mimicry, perhaps evolutionarily adaptive because
it facilitates contagion of "true" emotions. In
either case, the disruption of mimicry, which
may be demonstrated by a disruption in
contagious yawning, should have consequences for
emotional resonance with others. Indeed,
empathetic people exhibit greater amounts of all
forms of mimicry (Chartrand & Bargh, 1999)
and are reportedly more susceptible to
contagious yawning (Platek et al., 2003).
Development of Mimicry, Emotional
Contagion, and Contagious Yawning
Some capacity for mimicry and emotional
contagion appears to be present from birth.
Infants as young as 3 hr old execute some
behaviors after witnessing them modeled by an
adult (Meltzoff & Moore, 1977), most
reliably, tongue protrusion (for a review, see
Rogers, 2006). Similarly, a case has been made
for the presence of emotional contagion from the
first days of life; specifically, newborn
infants will cry when they hear other babies
crying in the nursery, but not in response to
computergenerated sounds matched for acoustic
properties (Simner, 1971). According to one
point of view, newborn "matching" behaviors are
early examples of the strong link between the
perception of actions and emotions in others,
and the experience of these actions and emotions
in ourselves, thus setting the stage for
imitative abilities that emerge later and
underlie critical aspects of social and
emotional development. However, early mimetic
behaviors and contagious crying gradually become
less frequent after birth. Imitative tongue
protrusion disappears by 2-3 months (Abravanel
& Sigafoos, 1984), and whereas 84% of
newborns exhibit contagious crying, only 24% of
3- to 12-month-old infants do so (Buhler &
Hetzer, 1928). In place of full-blown contagious
crying, infants at 10-14 months are much more
likely to mimic the distressed facial
expressions of other crying children
(Zahn-Waxler, Radke-Yarrow, & King, 1979).
Given these decreases in matching behaviors
after 2-3 months, it is unclear whether these
early behaviors are continuous with later
developing capacities for mimicry and emotional
contagion. Mimicry and emotional contagion seem
to "reappear" during the second half of the 1st
year and then continue to expand thereafter. For
example, by 9 months, babies take on the basic
moods and facial expressions of their
caregivers, such as joy and sadness (Termine
& Izard, 1988). A longitudinal study by
Jones (1996) found that mimicry of distinct
actions appeared at distinct periods in
development between 6 and 18 months.
Spontaneous yawning (termed the "rest yawn"
according to Deputte, 1994) begins in utero. In
contrast, the limited data on contagious yawning
(presumably, the emotion yawn) hint that it may
not emerge until much later in development.
Piaget (1951) reported that his own children did
not begin to yawn contagiously until the 2nd
year of life. A more recent study suggested an
even later age of emergence for contagious
yawning, reporting that only children 5 years
and older yawned in response to videos of yawns
(Anderson & Meno, 2003). Children respond to
live stimuli well before they respond to video
stimuli (Troseth & deLoache, 1998), and so
in vivo yawning may be a more effective stimulus
for eliciting contagious yawning in younger
children. Furthermore, the instructions in the
Anderson and Meno (2003) study required
participants to clap whenever they witnessed a
yawn. Clapping is an arousing activity, and
increased arousal is associated with diminished
yawning (Provine, 2005). In addition, the
clapping instructions drew conscious attention
to yawning, which has also been shown to
diminish yawning (Provine, 2005). For all these
reasons, the extant results must be interpreted
with caution. Therefore, there are few data to
address the developmental course of contagious
yawning in typical development.
Mimicry, Emotional Contagion, and
Contagious Yawning Deficits in Individuals With
ASD
Consistent with the hypothesis that mimicry
facilitates emotional contagion (Hatfield et
al., 1994), children with autism spectrum
disorders (ASD) show deficits in both. McIntosh,
ReichmannDecker, Winkielman, and Wilbarger
(2006) found that, unlike controls, adults with
high-functioning autism did not unconsciously
copy the facial expressions of individuals
viewed on a video screen (despite being able to
imitate them when asked). Meanwhile, children
with ASD have been found to be less susceptible
to emotional contagion when provided with
prompts that typically elicit emotions that
match those of the model: for example, an
experimenter opening a box in a child's presence
and looking delighted or afraid (Scambler et
al., 2006) or an experimenter injuring herself
(Bacon, Fein, Morris, & Waterhouse,
1998).
One study has examined contagious yawning in
children and adolescents with diagnoses
including Autistic Disorder, Pervasive
Developmental Disorder, Not Otherwise Specified
(PDD-NOS), and Asperger's disorder. Participants
with ASD were less susceptible than age-matched
typically developing (TD) peers to contagious
yawning when exposed to video recordings of
people yawning (Senju et al., 2007). Results are
difficult to interpret, however, because the ASD
group had a lower mental age, and included fewer
females, and because of the use of video rather
than live models. Given that all these factors
could potentially play a role in mimicry,
further data are needed to clarify the
dimensions of the relative susceptibility of
individuals with ASD to contagious yawning.
Current Studies
Study 1 explored the chronological and
mental ages at which contagious yawning is
exhibited in typical development to provide
clues about psychological mechanisms underlying
this phenomenon. The study delivered yawning
stimuli in an implicit paradigm (i.e., no
instructions were given regarding yawning) by a
live model, and study procedures were the same
for all children-design factors intended to
maximize sensitivity to the phenomenon. If
contagious yawning is a primitive mimetic
response, like contagious crying, it should be
evident in the youngest members of the sample.
In this case, its reduction or absence in
individuals with ASD would imply that basic
building blocks of social connection may be
abnormal from birth. In contrast, a protracted
emergence of contagious yawning would be
consistent with the idea that mimicry becomes
more ubiquitous and/or finetuned as development
proceeds. In this case, diminished yawning
contagion among individuals with ASD would seem
to be a reflection of their diminished implicit
social and emotional learning and
experience.
Study 2 sought to measure the rates of
contagious yawning in a group of children with
ASD. This study provided more rigorous diagnosis
than Senju et al. (2007), via use of the Autism
Diagnostic Observation Scale (ADOS; Lord et al.,
2000), excluding children with Asperger's
disorder (a variant of the disorder in which
language is not affected and potentially
involving distinct neural systems; Goodman,
2005), and using live, rather than videotaped,
stimuli. In addition, the study sought to
examine whether these group differences could be
accounted for by differences in mental age,
gender, symptom profile, or diagnosis.
Study 1
Method
Participants
Participants were 123 TD children, ages 1-6
years (approximately 20 at each year of age
studied), recruited through two local day-care
centers. Parents, teachers, and day-care workers
were asked to report any known or suspected
developmental difficulties for each child. For
children age 2 and above, parents or teachers
completed the Behavioral Assessment System for
Children, Second Edition (BASC-2; Reynolds &
Kamphaus, 2004) to screen for any developmental
problems. The data of 3 children were
excluded-one due to concerns about Tourette's
syndrome, one due to coding problems, and one
due to lack of attention -for a final sample of
120 children. Sex distribution varied for each
year of age with approximately 57% (n = 68) of
the total sample being female (see Table 1 for
gender breakdown by age). The ethnic background
of this group was as follows: 3 children were
African American, 5 children were Asian, 32
children were Latino, 3 children were
multiethnic, and 80 children were
Caucasian.
Procedure
A letter describing the study and obtaining
consent was sent home to parents. Parents were
asked to either fill out a BASC-2 for their
child or give permission for the child's teacher
to fill out a BASC-2 for the child. Children
whose parents consented to the study were taken
individually from their classrooms into a quiet
room, seated across from the experimenter. After
introducing herself and explaining, "Now we're
going to read some stories together, and then
you can pick a prize from this basket" and
showing the child the various toy prizes, the
experimenter read aloud one to four stories
(depending on the child's age and the complexity
of the stories) for a total reading time of
approximately 12 min (sometimes with a brief
break, again dependent upon the child's
developmental level). During the first 2 min of
reading, the experimenter did not yawn at all.
This, in addition to the first few minutes of
introductions before reading, was to control for
any changes in arousal level that may have
occurred when the children sat down to listen to
a story. During the last 10 min of reading, the
experimenter paused four times to yawn and
discreetly recorded on a coding sheet when a
child yawned. Approximately 40% of the sessions
(49 of 120), randomly selected, were videotaped
and coded by two independent raters (who had not
assisted in data collection) for
reliability.
For coding purposes, contagious yawns were
defined as yawns occurring within 90 s of the
yawning stimulus. Although subconscious
reactions typically occur much more rapidly,
previous reports of contagious yawning (e.g.,
Provine, 2005) indicate that contagious yawning
reactions may be somewhat slower and we wanted
to allow for the most liberal possible estimate
of the phenomenon, as well as for the
possibility that yawning contagion may be
mediated by some cognitive processes. Because
contagious yawning is a low base rate
phenomenon, yawning was coded as a dichotomous
variable (present or absent) rather than a
measure of yawning frequency (number of yawns
total). (Analysis of yawning frequency in all
statistics examined in Studies 1 and 2 did not
yield a different pattern of results.) Children
were considered to be contagious yawners if they
yawned in response to at least one of the
experimenter's four yawns within a 90-s window.
(Yawns occurring outside the 90-s window were
exceedingly rare, with only two occurring over
the 196 videotaped trials.) Coding criteria
required the presence of all of the physical
manifestations of a yawn (Provine, 2005): open
mouth, narrowed eyes, and an indrawn breath. The
data of one 3-year-old girl had to be excluded
because she covered her mouth and made a sighing
sound but her eyes did not narrow at all. Thus,
neither the experimenter nor the research
assistants were able to determine whether the
child was pretending to yawn in order to imitate
the experimenter or was truly yawning.
Interrater reliability was 100%, when the one
ambiguous responder was removed.
Videotaped sessions were also coded for
children's looking behavior toward the
experimenter during the 10-s segment in which
the yawns were presented by assigning each child
a rating of 1 (not looking at all), 2 (looking
for less than 5 s of the 10 s block coded), 3
(looking for 5 or more seconds of the 10 s block
coded), or 4 (looking throughout the 10 s block
in which the yawn stimulus was presented) for
each of the four trials, resulting in a visual
attention score of 1-16 for each child. The data
of children with scores of less than 12 (n = 1
in Study 1) were excluded from analysis.
Results and Discussion
Results showed that, when exposed to the
yawns of a live model over four trials, the
proportions of children in each age group who
yawned contagiously for at least one trial were
as follows: 0% (0/20) of 1-year-olds, 5% (1/20)
of 2-year-olds, 10% (2/20) of 3-year-olds, 35%
(7/20) of 4-year-olds, and 40% (8/20) of both 5-
and 6-year-olds (see Figure 1). Binary logistic
regression revealed a significant effect for
age, 2(1, N = 120) = 22.254, p < .001, but
not for visual attention, p = .22, or gender, p
= .37, in predicting whether or not a child will
yawn contagiously at least once across the four
trials of the experiment, with each year of age
increasing the odds of contagious yawning by a
factor of 2.2. However, the data suggest that
these variables do not have a linear relation.
Thus, age was recoded dichotomously as "under 4
years" or "4 years and over," 2(1, N = 120) =
22.69, p < .001, revealing that being 4 years
or older increased each child's odds of yawning
contagiously by a factor of 14.7 (visual
attention and gender remained
insignificant).
Although the older children appeared to make
more sustained eye contact in the direction of
the experimenter's face and the book throughout
the session, the experimenter yawned when she
had each child's attention, resulting in good
visual attention to the yawns from all age
groups (see Table 1). The amount of visual
attention that children directed toward the
examiner's face was examined in one-way analysis
of variance. There was a statistically
significant difference in visual attention
scores for the six age groups, p < .01. Post
hoc comparisons indicated that the mean
attention score for 1-year-olds was
significantly different from that for
5-year-olds, p < .001, and 6-year-olds, p =
.02. In addition, the mean score for the
2-year-olds differed from that for the
5-yearolds, p < .01.
These results indicate that children younger
than 4 years are significantly less likely than
children 4 years and older to yawn after being
exposed to the yawn of another. In contrast to
Anderson and Meno (2003), who observed no
contagious yawning prior to age 5, the present
study observed contagious yawning as early as 2
years with a significant shift in frequency at 4
years. The differing results between the present
data and those of Anderson and Meno (2003) may
be the result of presenting the yawning stimuli
in a live, implicit paradigm rather than a
video, explicit paradigm. Only a single child
exhibited contagious yawning at age 2-the age at
which Piaget (1951) observed his children to
begin yawning contagiously. Given that
individuals tend to engage in more mimicry with
individuals with whom they have rapport
(Chartrand & Bargh, 1999), parents may
elicit contagious yawning in their own children
earlier than it can be measured by an unfamiliar
experimenter. It is also possible that parents
may notice a pattern of earlier onset because
they have a much larger window in which to
observe their children compared with this
relatively brief experiment.
The temporal discrepancy between the
emergence of spontaneous (rest) yawning and
contagious crying (evident from birth), and that
of contagious (social-emotional) yawning,
indicate that they may not share a common basis.
Rather, this later emergence of contagious
yawning suggests that it may build upon early
empathic or cognitive development.
Study 2
Method
Participants
Participants were 30 children with a
diagnosis of an ASD, in addition to 63 TD
children. Diagnosis for the ASD group was
confirmed by the experimenter (MH) using the
Autism Diagnostic Observation Scale (ADOS) using
D SM-I V criteria (American Psychiatric
Association, 1994); see Table 2 for group
characteristics. Fifteen children met criteria
for autistic disorder on the ADOS, whereas 13
children met criteria for a milder form of
autism (PDD-NOS).
PDD-NOS refers to cases in which a child
experiences marked impairment in social
interaction, as well as difficulties with
communication and/or stereotyped behaviors
patterns or interests but does not meet full
diagnostic criteria for autistic disorder. The
ethnic background of this group was as follows:
One child was African American, 1 child was
Asian, and 28 children were Caucasian.
The two TD groups were matched to children
with ASD on either chronological age (within 6
months) or mental age (within 6 months) as well
as gender. No TD child was used in both mental
age (MA) and chronological age (CA) control
groups, and none of the children in Study 2
participated in Study 1. The data of 7 TD
children were excluded because they were not
matched to the ASD group on these parameters.
Children with ASD were recruited via flyers at
local autism events whereas TD children were
recruited via flyers at local family events. In
the TD group, 2 children were Asian, 12 children
were Latino, 3 children were multiethnic, and 46
children were Caucasian.
Measures
The Socialization domain of the Vineland
Scales of Adaptive Behavior-Interview Edition.
The Vineland (Sparrow, Balla, & Cicchetti,
1984) is a semistructured parent interview
designed to assess a child's adaptive
functioning. This study utilized the
Socialization domain. Age-equivalent and
standard scores for social skills were used in
the present analyses.
Autism Diagnostic Observation Scale. The
ADOS (Lord et al., 2000) consists of a
structured play session that provides
participants opportunities to engage in
conversation, narrative, problem-solving, and
imaginative tasks. The ADOS is scored according
to DSM-IV criteria for the autism spectrum
diagnoses.
Stanford-Binet Intelligence Scale: Fifth
Edition (Roid, 2003). In the Stanford-Binet
Abbreviated IQ scales, children provide word
definitions, yielding a verbal IQ score, and
solve a series of picture puzzles, yielding a
performance IQ score. This measure provided an
index of MA.
Procedure
Children with ASD and TD children sat across
the table from a live examiner. Children were
tested in a quiet room in their home or in the
University of Connecticut Psychological Services
Clinic. After an introduction and discussion of
the procedure, the experimenter read each child
a story, yawning four times during the story.
She then administered the Stanford-Binet and
(for the ASD group) the ADOS. Because older
children, and those who are fluent readers, may
have felt uncomfortable with an adult reading to
them, those children were told, "First, I'm
going to read you a story, and then I'll ask you
some questions about it" as opposed to simply,
"First, I'm going to read you a story." Thus, 14
of the 28 participants in both the ASD and
mental-age-matched typically developing control
(MA-TD) groups and 22 of the 28 participants in
the chronological-age-matched typically
developing control (CA-TD) group were told they
would be asked questions following the story. In
order to explore whether children with ASD
yawned spontaneously (as opposed to
contagiously) less often than TD children, the
test period of the StanfordBinet administered
after the yawning stimuli were also coded for
the presence or absence of yawns.
All story sessions were recorded on
videotape and coded for looking and yawning
behavior by raters blind to group status using
the same coding procedures as in Study 1.
Interrater reliability, coded for each block,
was 83% for looking behavior and 100% for
yawning. After the story and test session,
parents completed the socialization portion of
the Vineland interview.
Results and Discussion
Children with ASD were significantly less
likely than TD children to yawn after being
exposed to the experimenter's yawn. Only 11%
(3/28) of the children with ASD aged 5-12
yawned, compared with 43% (12/28) of a TD
control group matched for CA-TD, Fisher's exact
p = .009, and 36% (10/28)
of a control group matched for MA-TD,
Fisher's exact p = .037 (see Table 3 for group
characteristics). When the ASD group was further
divided by diagnosis, it became clear that
children diagnosed with autistic disorder were
less likely to exhibit contagious yawning than
children diagnosed with PDDNOS, 2(1) = 3.88, p =
.05. Specifically, none of the children with
autistic disorder (n = 15) showed contagious
yawning, whereas 23% of the children with
PDD-NOS (n = 13) did. CA, MA, instruction type,
visual attention scores, Vineland socialization
scores, and diagnosis were entered into a single
binary logistic regression model with contagious
yawning as a dichotomous variable. In contrast
to the results for younger children (ages 1-6
years) found in Study 1, binary logistic
regression on contagious yawning in children
ages 5-15 years revealed no main effect for age,
p = .80 (see Figure 1). These data are
consistent with the possibility that the rate of
contagious yawning remains relatively stable
after 5 years, though the relatively small
sample size for the current study prevents us
from drawing a firm conclusion. No significant
effect was found for instruction type (p = .83)
or MA (p = .87). Surprisingly, no significant
effect was found for Vineland socialization
scores (p = .924). The only significant
predictor of contagious yawning was diagnosis (p
= .014), with the absence of an autism spectrum
diagnosis increasing the odds of contagious
yawning by a factor of 5.8.
A second binary logistic regression was used
on the ASD group data only to determine whether
autism symptom severity (as indexed by ADOS
scores) showed a relation with contagious
yawning. Despite the effect of diagnostic
severity on yawning contagion, the results
suggested no relation between contagious yawning
and total ADOS scores, 2(1, N = 28) = 1.08, p =
.30, or communications (p = .276) and
socialization (p = .919) subscales. A possible
explanation for this discrepancy is that
although the ADOS is an exceptional instrument
for diagnosing autism, ADOS scores have not been
standardized for the purposes of using it as a
continuous measure of autism severity. Indeed,
individual items on the ADOS vary with respect
to their correlation with both IQ and CA
(Gotham, Pickles, & Lord, 2009). It is also
likely that the very low rate of contagious
yawning in the ASD group may have masked
relations between contagious yawning and symptom
profiles in this group.
Two children with ASD were excluded from
analysis because their visual attention scores
fell below 12. For the remaining children, ASD
(M = 14.6) and TD (M = 15.1) groups did not
differ significantly, t = .74, p = .14, on the
amount of time spent looking toward the
experimenter during the 10 s periods in which
the yawning stimuli were presented. As in Study
1, this is likely because the experimenter
yawned at limes when she was confident that she
had the child's attention, not because there are
no general differences in visual attention
between groups.
Finally, TD children were no more likely to
yawn (19.6%) than children with ASD (14.3%)
during the nonexperimental portion of the study
(such as the Stanford-Binet administration),
x2(1, N = 28) = .091, p = .76. In addition, the
experimenter asked the parents of the ASD
children whether they believed that their child
yawns less frequently than TD children; only one
parent responded in the affirmative. Taken
together, these data imply that the ASD deficit
observed is specific to the contagious, or
emotion yawn and does not affect the
spontaneous, or rest yawn.
The diminished tendency for participants in
the ASD group to yawn contagiously to a live
stimulus is consistent with previous findings
that individuals with ASD show diminished
contagious yawning with a video stimuli (Senju
et al., 2007) as well as general deficits in
mimicry (McIntosh et al., 2006). The current
study is novel in several regards. First, the
data demonstrate that individuals with ASD are
less likely to yawn contagiously than their TD
peers, even when controlling for MA and gender.
Second, the magnitude of this difference in
autistic disorder is much greater than
previously reported, when using live rather than
videotaped stimuli. Most importantly, the
current data demonstrated a striking effect of
diagnosis, with children with autistic disorder
being less likely to show contagious yawning
than children with PDD-NOS. Autistic disorder is
characterized by more marked deficits in the
realms of communication, social relatedness, and
stereotyped interests and behaviors. Thus, the
latter findings indicate a significant relation
between diagnostic severity in ASD, and
susceptibility to contagious yawning.
At a broad level, the late onset of this
phenomenon in typical development implies that
an autistic deficit in contagious yawning may be
a reflection of a deficit in early social
learning that affects the ability or tendency to
mimic the actions and emotions of others.
Nonemotional sounds and mouth movements, such as
mouth opening when feeding a baby, are
unintentionally imitated (Heyes, 2001) and
modulated by experience (Heyes, 2005). Future
research is needed to explore whether these
forms of mimicry are unconsciously imitated by
children with autism (work that is currently
underway in this lab). If they are not, this
finding would lend further support to the
proposal that there is an autistic deficit in
recognizing or acting on the correspondence
between oneself and others (an ability that all
mimetic and imitative acts depend upon).
Alternatively, individuals with autism may
demonstrate a specific deficit in mimicking
emotional behavior. Indeed, emotion perception
is a documented area of weakness for individuals
with autism (e.g., Moody, McIntosh, Mann, &
Weisser, 2007).
General Discussion
The present study demonstrates that children
younger than 4 years are significantly less
likely to yawn contagiously when exposed to a
live stimulus-that is, after seeing another,
nearby person yawn-than children ages 4 years
and older. The very early emergence of
spontaneous yawning (by the end of first
trimester of pregnancy) offers an informative
contrast to the much later, postnatal
development of contagious yawning. This
developmental lag may reflect the phylogenetic
antiquity of the motor act of yawning
(demonstrated in most vertebrates) relative to
the recent evolution of contagion (convincingly
demonstrated only in humans and chimpanzees;
Anderson, Myowa-Yamakoshi, & Matsuzawa,
2004). The present study also demonstrates that
children with ASD are significantly less likely
to yawn contagiously when exposed to a live
stimulus than TD children. Furthermore, those
with a diagnosis indicative of more severe
autistic symptoms (autistic disorder) are
significantly less likely to yawn contagiously
than those with a diagnosis indicative of milder
autistic symptoms (PDD-NOS). Taken together,
these studies provide further validation for the
distinction between spontaneous (or "rest")
yawns and contagious (or "emotion") yawns, and
suggest that contagious yawning is linked with
social development.
More research is needed to establish whether
contagious yawning is unique or whether all
forms of mimicry increase over the course of
typical development (potentially with a
substantial shift in competence occurring around
the age of 4). However, one potential
implication of the late onset of contagious
yawning in typical development and its near
absence among individuals with ASD is that
mimicry, and hence emotional contagion, may
increase with social experience. It is fairly
easy to imagine how mimicry may come to
substantially increase during the first years of
life. First, it is adaptive for an individual to
learn to "automatically" experience the emotions
displayed on the faces of conspecifics (i.e.,
experience those emotions without deliberation
or analysis). For example, if an individual
becomes afraid and retreats upon seeing a
predator, it is adaptive for an individual to
retreat rather than analyze the situation.
Likewise, automatically experiencing a
conspecific's disgust may protect an individual
from ingesting the same harmful food item
(Goldman, 2005).
In the case of yawning, experiencing fatigue
along with conspecifics may have served the
primary evolutionary function of synchronizing a
social group's biological rhythms (Schurmann et
al., 2004). Indeed, there is some evidence that
social cues alone may sustain shared circadian
rhythms in the absence of light (Aschoff et al.,
1971). Alternalively, rather than serving a
direct evolutionary purpose, contagious yawning
may have arisen as a by-product of the automatic
tendency to facially mimic others (adaptive in
rapidly spreading signals of risk and reward
throughout a group).
In addition to facilitating emotional and
biological synchronization, mimicry may serve to
increase feelings of closeness and connection
between individuals (Lakin, Jefferis, Cheng,
& Chartrand, 2003). These feelings of
affiliation, in turn, increase the amount of
mimicry individuals display toward one another
(Lakin et al., 2003). This process may escalate
in a continuous cycle first between child and
parent and, later, child and other members of
the community, during the early years of
development. Out of such increasingly
synchronous bonds may develop abilities such as
speech (i.e., Bruner's "proto-conversations";
Bruner, 1983), joint attention, and deliberate
imitation.
It is possible that infants with autism are
not able to perceive that they are being
mimicked (due to reduced social attention or
difficulties with emotion perception) or are
unable to mimic accurately (due to difficulties
in motor function or self-other mapping), and so
synchronization with mother and other members of
the social group is less available throughout
development. This lack of early mimicry could
also affect feelings of psychological connection
and opportunities for social learning. These
changes could thus leave children with autism
unable to recognize primitive socioemotional
cues that could otherwise serve to biologically
and emotionally synchronize them with people
around them.
Speculation About Underlying Neural
Mechanisms
Brain imaging studies may hold some promise
for shedding light on the neurological substrate
of contagious yawning. Two neuroimaging studies
have explored contagious yawning by exposing
participants to videos of others yawning. One
study (Platek, Mohamed, & Gallup, 2005)
showed increased activation in the precuneus and
posterior cingulate gyrus when participants
viewed videos of yawning relative to videos of
laughter (another emotionally contagious
stimulus). The authors interpreted this
activation as evidence that contagious yawning,
compared with laughter, involves nonconscious
aspects of self-referencing. A second study
(Schurmann et al., 2004) found that watching
yawn videos elicited activation in a region
associated with perception of biological
movement-particularly perception of eye and
mouth movements (the superior temporal sulcus).
In addition, they reported that self-reported
desire to yawn was negatively correlated with
periamygdalar activation (a region implicated in
arousal)-a finding that likely derives from the
negative relation between arousal and yawning.
Neither study found any special involvement of
the mirror neuron system (MNS)-a system that is
active both when one observes and executes an
action-for yawning over and above that recruited
for the control stimuli (laughing or neutral
faces, and meaningless mouth movements,
respectively). An obvious limitation of these
studies is that the participants in these
studies did not "catch" the yawns; they simply
reported upon their desire to yawn while viewing
the yawning stimuli and thus did not actually
experience any form of emotional contagion.
Studies investigating forms of empathy and
emotional convergence that more readily lend
themselves to neuroimaging have consistently
found activation in the insula and anterior
cingulate cortex (ACC). We speculate that these
areas are likely candidates for distinguishing
the neural activation associated with contagious
yawning over and above that associated with any
type of action (and thus the MNS) including
spontaneous yawning or other mouth movements,
that is, the regions we speculate underlie the
contagious component of yawning. Just as the
"MNS" may underlie common coding of actions,
studies have demonstrated the same common coding
in the insula and ACC between first- and
third-person experiences of emotional
information, such as disgust (Wicker et al.,
2003), pain (Singer et al., 2004), emotional
body language (de Gelder & Had jikhani,
2006), and emotional expressions (Carr,
lacoboni, Dubeau, Mazziotta, & Lenzi, 2003).
A recent study of children ages 9-10 years
supports the involvement of the insula, as well
as inferior frontal mirror areas and the
amygdala, in the observation and imitation of
emotional expressions (Pfeifer, lacoboni,
Mazziotta, & Dapretto, 2008). Furthermore,
activation in these areas was associated with
the children's empathy levels. In children with
autism, activity in these same areas during the
observation of emotional expressions has been
found to be negatively correlated with symptom
severity (Dapretto et al., 2006).
One type of neuron unique to the insula and
the ACC is the spindle cell, also known as the
Von Economo neuron (VEN). Spindle cells are a
late-evolving class of neurons that allow for
the conscious monitoring of visceral signals
from the body, a process that may underlie the
impact of afferent feedback. These neurons do
not achieve their ultimate postnatal number
until the age of 4 years (the age at which we
demonstrate the robust emergence of contagious
yawning) and have been reported to be disordered
in autism (Allman, Watson, Tetrault, &
Hakeem, 2005). VENs are responsible for rapidly
extracting statistical probabilities from
sensory input based on previous information,
giving rise to nonconscious emotional reactions.
The more experience we gain, the more we may be
able to recognize such patterns and
associations, and the more developed these
neurons may become. The diminished tendency for
contagious yawning in children with ASD could be
the result of primary or secondary neurological
differences affecting these neurons.
Limitations
While study results were fairly unambiguous,
findings are necessarily limited in several
dimensions. First, although looking time, or
general attention to the experimenter, was
accounted for in the present studies, we could
not unequivocally verify whether participants
were attending to the eye or the mouth region of
the speaker; this would have required additional
eye tracking methods. This limitation is
relevant because Provine (1989) has found that
yawning contagion, when elicited by pictures of
others yawning, is dependent upon attending to
the region of the eyes rather than the mouth.
Eye tracking studies have revealed that
individuals with autism preferentially fixate on
the mouth rather than the eye regions (Klin,
Jones, Schultz, Volkmar, & Cohen, 2002),
leaving open the possibility that a lack of
attention to the eye region of others' faces
(rather then a deficit in unintentional mimicry)
is responsible for diminished yawning contagion
in this group. Similarly, as typical children
age, they may pay closer attention to the faces
of others, resulting in more facial mimicry, and
hence, greater emotional and biological
attunement with those around them. In contrast,
children with autism may never learn to pay
closer attention to the faces of those around
them, and so their tendency to mimic others, as
well as their emotional attunement with others,
may not increase over time in the way one
observes in typical development. If so, this
lack of attention to faces may have a previously
unsuspected significance in that it may serve to
impair mimicry, resulting in decreased emotional
resonance, and perhaps even decreased biological
synchrony with others.
An argument against this explanation of the
findings is that yawning, like crying and
laughing, is a contagious act that produces a
sound, and the sound alone is often sufficient
to trigger its contagion (Provine, 1996).
Indeed, the experimenter in this study produced
yawns that included the prototypical auditory
accompaniment of an indrawn breath followed by a
voiced sigh. In addition, given that there were
no significant differences in visual attention
to the yawns between the 4-year-olds (the age at
which a major susceptibility shift was observed)
and the other age groups, the developmental
results seem unlikely to be due merely to
age-related shifts in visual attention.
Finally, although the low rate of contagious
yawning in the ASD group speaks to its
significance, it made it impossible to determine
the extent to which contagious yawning in this
population, when it does occur, is correlated
with specific autistic symptoms. If more
children with ASD could be found who do yawn
contagiously, it might be possible to determine
whether such factors correlate with contagious
yawning in autism, shedding increased light on
the implications of this deficit.
Summary and Conclusions
In order to elucidate the developmental
properties of automatic facial mimicry in the
form of contagious yawning, we investigated the
extent to which groups of children at various
stages of social development (TD children ages
1-6, as well as children with ASD) are
susceptible to contagious yawning. Findings
strongly suggested that children under the age
of 4 and children with ASD are less likely to
yawn when exposed to another's yawn. The
developmental curve associated with the onset of
contagious yawning implies that emotional
contagion becomes more developed and more
sensitive over time, resulting in increased
affective attunement with others as children
grow older. Meanwhile, individuals with ASD may
not experience increased emotional contagion
during the early years of development, causing
them to be deficient in the automatic emotional
reciprocity that psychologically binds most
individuals together. More research is necessary
to determine what mediates this phenomenon;
however, it is possible that in the future
contagious yawning may prove to provide a simple
measure of automatic facial mimicry, empathy, or
perhaps even a biomarker of clinically important
neurological characteristics that does not
require specialized equipment or testing to
detect.
-Arnott
SR et al. An investigation of auditory
contagious yawning Cognitive, Affective,
Behavioral Neurosci 2009;9(3):335-342
-Anderson
JR et al Contagious yawning in chimpanzees
The Royal Society Biology Proc R Soc Lond B Biol
Sci 2004; 271 Suppl 6; S468-470
-Anderson
JR et al Psychological influences on yawning
in children Current Psychology Letters
Behaviour, Brain, Cognition 2003;2:11
-Anderson
JR, Matsuzawa T. Yawning: An Opening into
Empathy? Cognitive Development in Chimpanzees. T
Matsuzawa, M Tomonaga, M Tanaka Editors.
Springer 2006
-Caswell
TA, The effects of status on yawning
behavior. Thesis 1991
-Campbell
MW et al. Do chimpanzees yawn
contagiously in response
to 3d computer animations? 2008
-Cooper NR,
Puzzo I, Pawley A Contagious yawning: the
mirror neuron system may be a candidate
physiological mechanism Medical Hyportheses
2008;71(6):975-976
-Cooper NR,
Puzzo I, et al. Bridging a yawning chasm:
EEG investigations into the debate concerning
the role of the human mirror neuron system in
contagious yawning.Cogn Affect Behav Neurosci.
2012;12(2):393-405
-Demuru E,
Palagi E. In Bonobos Yawn Contagion Is
Higher among Kin and Friends. PLoS One. 2012;
7(11): e49613
-Dijksterhuis
A, Bargh JA The perception-behavior
expressway:automatic effects of social
perception on social behavior Advances in
Experimental Social Psychology
2001;33:1-40.
-Estow,
S Jamieson JP, Yates JR Self-monitoring and
mimicry of positive and negative social
behaviors Journal of Research in Personality
2007;41(2):425-433
-Gallagher
HL, Frith CD Functional imaging of theory of
mind Trends in Cognitive Scie.
2003;7(2):77-83
-Giganti
F, Ziello ME Contagious and spontaneous
yawning in autistic and typically developing
children CPL 2009
-Giganti
F, Zilli I. The daily time course of
contagious and spontaneous yawning among humans.
J Ethol 2011;29(2):215-216
-Lindsay
SR Coping with fear and stress: licking and
yawning. Handbook of applied dog behavior and
training 2000
-Madsen EA,
Persson T. Contagious yawning in domestic
dog puppies (Canis lupus familiaris): the effect
of ontogeny and emotional closeness on low-level
imitation in dogs. Anim Cogn. 2012
-Massen
JJ, Vermunt DA, Sterck EH. Male Yawning Is
More Contagious than Female Yawning among
Chimpanzees (Pan troglodytes). PLoS One.
2012;7(7):e40697.
-Norscia I,
Palagi E. Yawn Contagion and Empathy in Homo
sapiens. PLoS ONE. 2011;6(12): e28472
-O'Hara SJ, Reeve
AV A test of the yawning contagion and
emotional connectedness hypothesis in dogs,
Canis familiaris. Animal Behaviour
2011;81:335-340
-Palagi E,
Leone A, Mancini G, Ferrari PF. Contagious
yawning in gelada baboons as a possible
expression of empathy. Proc Natl Acad Sci USA.
2009;106(46):19262-19567
-Paukner
A, Anderson JR
Video-induced yawning in stumptail
macaques (Macaca
arctoides) Biol Lett 2006;2(1):36-38
-Perkins
JR Teaching Dogs to Yawn, Sneeze, and
Implications for Preparedness Theory and
Observational Learning.
In: Kusonose, Ryo and Sato, Shusuke 39th
Congress of the International Society for
Applied Ethology, Kanagawa, Japan. 20-24 August,
2005
-Platek
SM, SR Critton, et al Contagious yawning:
the role of self-awareness and mental state
attribution Cogn Brain Res
2003;17(2):223-227
-Platek S et
al. Neural correlates of self-face
recognition 2008 Brain Res;1232:173-184
-Senju A,
Kikuchi Y, Akechi H et al. Does eye contact
induce contagious yawning in children with
autism spectrum disorder? J of Autism and
Developmental Disorders.
2009;39(11):1598-1602
-Silva K, Bessa J, de
Sousa L. Auditory contagious yawning in
domestic dogs (Canis familiaris): first evidence
for social modulation. Anim Cogn. 2012.
-Yoon JMD, Tennie C
Contagious yawning: a reflection of empathy,
mimicry, or contagion. Anim Behav
2010;79:e1-e3
-Walusinski
O Echokinetic yawning, theory of mind, and
empathy
