Individuals with autism spectrum disorder
(ASD) reportedly fail to show contagious
yawning, but the mechanism underlying the lack
of contagious yawning is still unclear. The
current study examined whether instructed
fixation on the eyes modulates contagious
yawning in ASD. Thirty-one children with ASD, as
well as 31 age-matched typically developing (TD)
children, observed video clips of either yawning
or control mouth movements. Participants were
instructed to fixate to the eyes of the face
stimuli. Following instructed fixation on the
eyes, both TD children and children with ASD
yawned equally frequently in response to yawning
stimuli. Current results suggest that contagious
yawning could occur in ASD under an experimental
condition in which they are instructed to fixate
on the yawning eyes.
Introduction
Contagious yawning (i.e., yawning triggered
by perceiving others' yawning) is a
well-documented phenomenon (e.g. Platek,
Critton, Myers, & Gallup, 2003; Provine,
1986, 1989; Senju et al., 2007), reported in
humans and other primate species (Anderson,
Myowa-Yamakoshi, & Matsuzawa, 2004; Paukner
& Anderson, 2006) and in dogs (Joly-
Mascheroni, Senju, & Shepherd, 2008).
Although little is known about the mechanism
underlying contagious yawning, several
hypotheses have been proposed. These hypotheses
include the innate releasing mechanism
responding to the perceived yawning (Provine,
1986, 1989), the capacity for empathy (Platek et
al., 2003; Preston & de Waal, 2002), and the
mirror neuron system (Cooper, Puzzo, &
Pawley, 2008). In addition, a neuroimaging study
(Schürmann et al., 2005) reported that
observation of others' yawning and
susceptibility to yawning in response are
related to the activity of the superior temporal
sulcus (STS) and periamygdalar regions. As both
STS and amygdala are the core components of the
social brain (Brothers, 1990; Senju &
Johnson, 2009), it has been suggested that the
mechanism underlying contagious yawning overlaps
with mechanisms underlying other social
cognition.
Recently, Senju et al. (2007) tested whether
individuals with Autism Spectrum Disorder (ASD)
show contagious yawning, using video clips of
yawning as stimuli and control video clips of a
mouth-opening action. Observing yawning videos
elicited less yawning in children with ASD than
in TD children, while the amount of yawning did
not differ between groups during or after the
observation of control videos. Giganti and
Esposito Ziello (2009) replicated the absence of
contagious yawning in children with ASD, even
though these children showed equally frequent
spontaneous yawns as the control children. These
results suggest that individuals with ASD lack
the capacity for contagious yawning, which may
relate to clinical characteristics such as
impairment in social and communicative
development (American Psychiatric Association,
2000).
One possible mechanism underlying the lack
of contagious yawning in ASD is atypical face
fixation, especially reduced spontaneous
fixation on others' eyes (e.g. Klin, Jones,
Schultz, Volkmar, & Cohen, 2002; Pelphrey et
al., 2002). Since the perception of the eye
region of yawning people is a potent stimulus
for yawn contagion (Provine, 1989), it is
possible that shorter fixation on the eyes of
yawning stimuli may impede contagious yawning in
children with ASD.
Other studies have demonstrated that
instructed fixation on the eyes can diminish, or
at least reduce, the manifestation of atypical
face processing in individuals with ASD
(Hadjikhani et al., 2004). This study explores
the effect of instructed fixation on the eyes on
contagious yawning in children with ASD, by
replicating Senju et al. (2007) with additional
instruction about the fixation on the eyes. The
stimuli are exactly the same as those used in
Senju et al. (2007), except that a fixation
stimulus appeared in the future location of the
eyes of stimulus faces just before the onset of
face stimuli.
Children were instructed to maintain
fixation on the location of the fixation
stimulus. If the lack of spontaneous eye
fixation impedes contagious yawning in ASD,
children with ASD should yawn equally frequently
as typically developing children when their
fixations are guided to the eyes of yawning
stimuli. By contrast, if the lack of contagious
yawning is caused by the lack of the mechanism
to decode others' yawns or to coordinate their
own yawning with the perceived yawning, children
with ASD should show reduced numbers of yawns
compared to typically developing children, as in
Senju et al. (2007).
Discussion
In the current study, yawning stimuli
elicited an equally frequent yawning response in
both TD children and children with ASD. It
contrasts with the previous study (Senju et al.,
2007), which found the absence of contagious
yawning in children with ASD using exactly the
same stimuli. On average, children with ASD in
the current study yawned twice as frequently as
those in Senju et al. (2007) in the yawning
condition (Figure 1), although the difference
did not reach statistical significance. By
contrast, the frequency of yawning in TD
children in the yawning condition was comparable
between the current study and in Senju et al.
(2007). Thus, the current results suggest that
instructed fixation on the eyes of the yawning
face induced contagious yawning in ASD.
The current results are consistent with the
hypothesis that atypical functioning of the
social brain network in ASD can be at least
partly explained by atypical orienting to social
stimuli such as face and eyes, possibly due to
atypical functioning of the amygdala (Grelotti,
Gauthier, & Schultz, 2002; Hadjikhani et
al., 2004; Schultz, 2005; Senju & Johnson,
in press). In typical development, it is
hypothesized that subcortical structures
including the amygdala work as a 'face detector'
or 'eye contact detector', which then control
social orienting as well as modulate cortical
responses to social stimuli (Johnson, 2005;
Senju & Johnson, in press). The current
results also suggest that the same subcortical
structures may contribute to contagious yawning
by guiding spontaneous orienting to the eyes of
yawning face (Schürmann et al., 2005).
It is also reported that increased attention
to the face can elicit other empathetic
response, such as spontaneous mimicry of facial
expression, in ASD (Magnee, de Gelder, van
Engeland, & Kemner, 2007). By contrast, the
current results are inconsistent with the
hypothesis that the lack of contagious yawning
in ASD is based on the impairment of the mirror
neuron system (Cooper et al., 2008). This theory
should predict the lack of contagious yawning in
ASD children even when they fixate to the eyes
of a yawning face. Other researchers have also
argued that current evidence is often
inconsistent with the hypothesized impairment in
the mirror neuron system in ASD (e.g. Dinstein,
Thomas, Behrmann, & Heeger, 2008; Southgate
& de C. Hamilton, 2008).
Note that there are several limitations in
these results. Firstly, it is not clear why the
yawning response was observed equally frequently
during and after the presentation of the control
stimuli as in the yawning condition, especially
in TD children. It might be due to the
carry-over effect: eye fixation may have
enhanced yawn contagion in both groups and the
effect persisted longer than 1 minute, which
then affected the response to the following
stimuli. Alternatively, it is possible that even
the non-yawning mouth-opening action used in the
current study may elicit contagious yawning when
participants fixate to the eyes. The current
results need to be treated with caution because
of the non-significant results in the TD
group.
Further studies will be required to
systematically control the duration of the
stimulus interval, as well as the control
stimuli to test the effect of eye fixation on
yawn contagion in both the typically developing
population and in individuals with ASD.
Secondly, we cannot completely exclude the
possibility that increased attention to the
face, not specifically to the eyes, may have
increased the susceptibility to contagious
yawning, because the relatively longer duration
of stimulus presentation (7s) allowed
participants to freely scan the face after the
initial fixation on the eyes. Further studies
with stricter control of fixations, ideally with
the use of an eye-tracker to monitor fixations,
will be required to further investigate the
relationship between the exact points of
fixations and the susceptibility to contagious
yawning. Thirdly, we could not obtain the 'gold
standards' of clinical information such as ADI-R
(Lord, Rutter, & Couteur, 1994) or ADOS
(Lord, Risi, Lambrecht, Cook, Leventhal,
DiLavore, et al., 2000) from the current
participants.
Further studies with the use of these
measures is required. Our results add to the
growing body of evidence suggesting that
atypical social cognition and social behaviour
in ASD is related to atypical orienting to
social stimuli, possibly due to the atypical
development and functioning of subcortical
structures including the amygdala (Adolphs,
2008; Grelotti et al., 2002; Schultz, 2005;
Senju & Johnson, in press). Future studies
will be required to discover the cognitive and
neural basis of such atypical social orienting,
with the aid of eye-tracking and/or neuroimaging
techniques. In addition, the current study also
suggests that the apparent relationship between
the susceptibility to contagious yawning and the
capacity for social cognition such as
mentalizing and self-processing (Platek et al.,
2003) could be mediated by individual
differences in social orienting, not by the
shared mechanism to process yawn contagion and
theory of mind. It is consistent with the recent
evidence that dogs, which are known to have a
limited capacity in mentalizing and
self-processing (Miklósi, 2007), also
show contagious yawning (Joly-Mascheroni et al.,
2008).
It is possible that the relationship between
contagious yawning, the capacity for mentalizing
and social orienting could be developmental, as
spontaneous social orienting may be the
developmental precursor of mentalizing (e.g.
Klin, Jones, Schultz & Volkmar, 2003) as
well as contagious yawning. Further study will
be required to examine the mechanism underlying
contagious yawning, as well as its developmental
and evolutionary origin.
