Most previous studies suggest diminished
susceptibility to contagious yawning in children
with autism spectrum disorder (ASD). However, it
could be driven by their atypical attention to
the face. To test this hypothesis, children with
ASD and typically developing (TD) children were
shown yawning and control movies. To ensure
participants' attention to the face, an eye
tracker controlled the onset of the yawning and
control stimuli. Results demonstrated that both
TD children and children with ASD yawned more
frequently when they watched the yawning stimuli
than the control stimuli. It is suggested
therefore that the absence of contagious yawning
in children with ASD, as reported in previous
studies, might relate to their weaker tendency
to spontaneously attend to others' faces.
Introduction
Yawning is widespread among vertebrate
species, including a wide range of mammals
[1]. In humans, yawning is detectable
even in the foetus [2]. The function of
yawning is still unclear, but a recent theory
highlighted that it may have a communicative
function [3]. This hypothesis suggests
that yawning is a nonverbal form of
communication that synchronizes the behavior of
a group [4-7]. It has been suggested
that yawning transmits physiological and
psychological states, such as drowsiness [8,
9], boredom [10], hunger, and mild
psychological stress [7], to other
members of the group. Among the evidence that
supports this theory, studies of contagious
yawning have attracted the most attention in
recent years.
Contagious yawning, in which observation of
another's yawn induces yawning behaviour in the
observer, is a well-documented phenomenon. In
humans, contagious yawning can be elicited by
viewing or hearing others' yawning or imagining
yawning (e. g., [5, 11-14]). During the
course of development, contagious yawning can be
reliably observed by around 4 to 6 years of age
[15, 16] but might not be present in
younger infants and toddlers [17]. The
presence of contagious yawning has also been
reported in several nonhuman animals (e. g.,
[18-20]). Several neuroimaging studies
have been conducted to investigate the cortical
and subcortical structures relevant to the
contagious yawning [21-24], but the
results are inconsistent. This is possibly due
to differences in the yawning stimuli and/or
control stimuli used for recording
[25].
To date, three independent studies have
consistently demonstrated the absence of
contagious yawning in individuals with autism
spectrum disorder (ASD), a developmental
disorder with profound impairments in social
interaction and communication [26].
First, Senju et al. [27] presented video
clips of yawning faces, as well as faces
demonstrating mouth-opening actions, the latter
serving as control stimuli. TD children yawned
more during or after observing yawn video clips
than during or after control video clips, while
the type of video clips observed did not affect
the amount of yawning in children with ASD.
Second, Giganti and Esposito Ziello [12]
reported the absence of contagious yawning in
children with ASD when seeing or listening to
others' yawning, even though these children
demonstrated the same frequency of spontaneous
yawns as control children. Third, Helt et al.
[16], using live yawning stimuli,
reported less susceptibility to contagious
yawning in children with ASD compared with
control children. These results are interpreted
as a manifestation of the impairment in
"empathy" in this population. Based on this
interpretation, the absence of contagious
yawning in ASD results from the difficulty in
empathizing with a yawning person.
However, these studies cannot rule out the
possibility that individuals with ASD failed to
show contagious yawning in previous experiments
because of the absence of spontaneous attention
to others' faces [28-30]. The
possibility of this was discussed even in some
of these initial reports of the absence of
contagious yawning in ASD [16, 27]. To
test this hypothesis, Senju et al. [31]
studied whether children with ASD "catch" yawns
when their attention is navigated to yawning
faces. The study used exactly the same
experimental design as Senju et al.
[27], except that a small cartoon
animation was presented for 1 s in the location
where the eyes of the face stimuli would appear,
just before the presentation of each face, and
children were instructed to fixate on the
animation. Both TD children and children with
ASD were found to yawn equally frequently in
response to the yawning stimuli. However, as
both groups also yawned as frequently in
response to the control (i. e., nonyawning)
stimuli as to the yawning stimuli, it remained
open to an alternative interpretation, that
controlled fixation on the face might modulate
the frequency of spontaneous yawning irrelevant
to the perception of others' yawns, not the
contagious yawning.
The aim of the current study is to test the
presence of contagious yawning in ASD, when
children's attention is navigated to yawning
stimuli. To achieve that, we designed a
gaze-contingent stimulus display, in which the
participants' gaze was monitored with an eye
tracker, and the yawning and control movies
started only when participants were fixating on
the eyes (Experiment 1) or the mouths
(Experiment 2) of the stimuli. We also asked
participants to count the number of people
wearing eyeglasses (Experiment 1) or having a
beard (Experiment 2), to further ensure that
they were attending to the face. We adopted a
block design with an interval between blocks,
instead of the event-related design with a
1-minute interstimulus interval used in Senju et
al. [27] and Senju et al. [31].
This was to prevent any possible long-latency
effects of the yawning stimuli carried over to
control stimuli, which might have affected
previous results. Other studies adopting block
designs have demonstrated clearer effects of
yawning stimuli (e. g., [12]).
Three alternative predictions can be derived
from different hypotheses. Firstly, if
individuals with ASD have an inherent impairment
in empathizing which impedes contagious yawning,
we should not observe contagious yawning (i. e.,
an increase in participants' yawning in response
to the observation of yawning stimuli).
Secondly, if atypical attention to the face is
relevant to the absence of contagious yawning in
individuals with ASD, they should show
contagious yawning when presentation of yawning
stimuli is contingent on their attention to the
face. Thirdly, if the fixations on the eyes have
a critical role in the processing of yawning
face [14] or attentional engagement to
the face [29] in individuals with ASD,
we should only see the contagious yawning when
their attention is navigated to the eyes
(Experiment 1), but not to the mouth (Experiment
2). Further, as previous studies have reported
that children with ASD show equally frequent
spontaneous yawning as TD children [12, 27,
31], we predict that there should be no
difference between groups in the number of yawns
in the control condition.
Discussion
In both experiments, more children with ASD
yawned in response to yawning stimuli than to
control stimuli, which demonstrates that video
images of yawning faces can elicit yawning in
children with ASD, when the onset of a stimulus
presentation is contingent on participants'
fixation on the face. Around 30% of children
with ASD showed contagious yawning, which is
equivalent to the rates of contagious yawning in
the control children and significantly more than
those who yawned in response to the nonyawning
stimuli. The rate of contagious yawning in the
current study is well within the range of the
rate of contagious yawning in other studies
around the same age range (12-60% [12, 15,
16]). The results suggest that individuals
with ASD do not have a fundamental impairment in
catching others' yawns, such as the impairment
to empathize with others [41]. Instead,
it is possible that the previous finding that
children with ASD were less susceptible to
contagious yawning is modulated by the atypical
development of spontaneous social attention to
the face (e. g., [28, 29]). The current
study corroborates previous findings that
individuals with ASD can demonstrate behavioural
contagion [42], attentional engagement
[29], and partially normalized neural
processing of the face [43-45] when the
experimental control effectively navigates the
attention of the participants to the face.
The results do not fully support the special
role of initial fixations on the eyes to elicit
contagious yawning (e. g., [14]),
because we observed contagious yawning when
participants' attention was drawn to the mouth
(Experiment 2). However, we emphasize that our
results should not be taken as the evidence that
observation of yawning eyes is irrelevant to
contagious yawning for the following reasons.
Firstly, our yawning stimuli lasted 5 seconds,
which provides sufficient opportunity for the
participants to saccade from the mouth to the
eyes in Experiment 2. Secondly, initial
attention to the eyes (Experiment 1) elicited
twice as frequent yawning as the initial
attention to the mouth (Experiment 2) in
children with ASD, even though this difference
did not reach statistical significance
(Mann-Whitney test). Further studies will be
necessary to test the role of the pattern of
face fixation on contagious yawning, especially
in individuals with ASD.
One limitation of the current study is that
atypical fixation on the face cannot explain all
previous reports of the absence of contagious
yawning in ASD, because this absence has also
been reported in response to yawning voices,
where there was no visual presentation of
yawning eyes [12]. Further studies,
which do not involve visual stimuli, will
therefore be required to study the role of
atypical social orienting to the absence of
contagious yawning in ASD. Note that the only
neuroimaging study that has demonstrated
activation of the mirror neuron system (i. e.,
inferior frontal cortex) used auditory stimuli
[21], which might suggest that the
mirror neuron system plays a critical role in
contagious yawning when visual stimuli are not
available.
The current study has demonstrated that
experimentally controlled fixations on yawning
eyes can induce contagious yawning in
individuals with ASD. The results suggest that
contagious yawning requires attention to the
yawning individuals, which could be affected in
individuals with ASD. Further studies will be
beneficial to investigate whether this is also
the case for other clinical populations, such as
individuals with schizophrenia, who also
demonstrate an absence of contagious yawning
[46]. It is important to explore the
effect of induced contagious yawning on social
cognition and behaviour in these clinical
populations, which will help us understand the
function of contagious yawning. Other important
questions include whether individual differences
in susceptibility to contagious yawning are
related to an individual's tendency to
spontaneously orient to others' faces and
whether the relationship between contagious
yawning and attention to others can be observed
in nonhuman animals too. These studies will help
to reveal the neural and cognitive mechanisms
underlying contagious yawning, as well as its
function, development, and evolution.
