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Fetal yawning assessed by 3D and 4D sonography
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mise à jour du
12 août 2013
Autism Research and Treatment
Volume 2013
Article ID 971686
 Presence of Contagious Yawning
in Children with Autism Spectrum Disorder
Saori Usui, Atsushi Senju, Yukiko Kikuchi, Hironori Akechi,
Yoshikuni Tojo, Hiroo Osanai, Toshikazu Hasegawa  
 Department of Cognitive and Behavioral Science, University of Tokyo, Japan

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Abstract
 
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.