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Clinical Study Presence of Contagious Yawning in Children with Autism Spectrum Disorder Hindawi Publishing Corporation Autism Research and Treatment Volume 2013, Article ID 971686, 8 pages http://dx.doi.org/10.1155/2013/971686 Clinical Study Presence of Contagious Yawning in Children with Autism Spectrum Disorder Saori Usui,1 Atsushi Senju,2 Yukiko Kikuchi,1 Hironori Akechi,1 Yoshikuni Tojo,3 Hiroo Osanai,4 and Toshikazu Hasegawa1 1 Department of Cognitive and Behavioral Science, University of Tokyo, Tokyo, Japan 2 Centre for Brain and Cognitive Development, Birkbeck, University of London, Malet Street, London WC1E 7HX, UK 3 Department of Education for Children with Disabilities, Ibaraki University, Ibaraki, Japan 4 Musashino Higashi Center for Education and Research, Musashino Higashi Gakuen, Tokyo, Japan Correspondence should be addressed to Atsushi Senju; [email protected] Received 15 April 2013; Accepted 2 July 2013 Academic Editor: Elizabeth Aylward Copyright © 2013 Saori Usui et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 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. Totest 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. 1. Introduction development, contagious yawning can be reliably observed by around 4 to 6 years of age [15, 16]butmightnotbe Yawning is widespread among vertebrate species, including a present in younger infants and toddlers [17]. The presence wide range of mammals [1]. In humans, yawning is detectable of contagious yawning has also been reported in several even in the foetus [2]. The function of yawning is still unclear, nonhuman animals (e.g., [18–20]). Several neuroimaging but a recent theory highlighted that it may have a commu- studies have been conducted to investigate the cortical and nicative function [3].Thishypothesissuggeststhatyawning subcortical structures relevant to the contagious yawning is a nonverbal form of communication that synchronizes [21–24], but the results are inconsistent. This is possibly due thebehaviorofagroup[4–7]. It has been suggested that to differences in the yawning stimuli and/or control stimuli yawning transmits physiological and psychological states, used for recording [25]. such as drowsiness [8, 9], boredom [10], hunger, and mild To date, three independent studies have consistently psychological stress [7], to other members of the group. demonstrated the absence of contagious yawning in individ- Among the evidence that supports this theory, studies of uals with autism spectrum disorder (ASD), a developmental contagious yawning have attracted the most attention in disorder with profound impairments in social interaction and recent years. communication [26]. First, Senju et al. [27]presentedvideo Contagious yawning, in which observation of another’s clips of yawning faces, as well as faces demonstrating mouth- yawninducesyawningbehaviourintheobserver,isawell- opening actions, the latter serving as control stimuli. TD documented phenomenon. In humans, contagious yawning children yawned more during or after observing yawn video can be elicited by viewing or hearing others’ yawning or clips than during or after control video clips, while the type imagining yawning (e.g., [5, 11–14]). During the course of of video clips observed did not affect the amount of yawning 2 Autism Research and Treatment in children with ASD. Second, Giganti and Esposito Ziello Table 1: Mean, standard deviation (SD) and range of chronological [12] reported the absence of contagious yawning in children age, full intelligence quotient (FIQ), and scores on the Japanese ver- with ASD when seeing or listening to others’ yawning, even sion of the Autism Screening Questionnaire (ASQ-J) of participants though these children demonstrated the same frequency of in Experiment 1. spontaneous yawns as control children. Third, Helt et al. [16], Age (years) FIQ ASQ-J using live yawning stimuli, reported less susceptibility to con- TD (=46) tagious yawning in children with ASD compared with control children. These results are interpreted as a manifestation of M (SD) 11.2 (3.1) 105.5 (11.7) 2.3 (2.4) the impairment in “empathy” in this population. Based on Range 6.7–18.6 82–136 0–8 this interpretation, the absence of contagious yawning in ASD ASD (=26) results from the difficulty in empathizing with a yawning M (SD) 12.4 (3.5) 91.6 (25.3) 22.7 (5.4) person. Range 6.6–18.8 46–127 14–31 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 when presentation of yawning stimuli is contingent on their attention to others’ faces [28–30]. The possibility of this was attention to the face. Thirdly, if the fixations on the eyes discussedeveninsomeoftheseinitialreportsoftheabsence have a critical role in the processing of yawning face [14]or of contagious yawning in ASD [16, 27]. Totest this hypothesis, attentional engagement to the face [29]inindividualswith Senju et al. [31] studied whether children with ASD “catch” ASD, we should only see the contagious yawning when their yawns when their attention is navigated to yawning faces. The attention is navigated to the eyes (Experiment 1), but not study used exactly the same experimental design as Senju et to the mouth (Experiment 2). Further, as previous studies al. [27], except that a small cartoon animation was presented have reported that children with ASD show equally frequent for1sinthelocationwheretheeyesofthefacestimuliwould spontaneous yawning as TD children [12, 27, 31], we predict appear, just before the presentation of each face, and children that there should be no difference between groups in the were instructed to fixate on the animation. Both TD children number of yawns in the control condition. andchildrenwithASDwerefoundtoyawnequallyfrequently in response to the yawning stimuli. However, as both groups 2. Experiment 1 also yawned as frequently in response to the control (i.e., nonyawning) stimuli as to the yawning stimuli, it remained 2.1. Method open to an alternative interpretation, that controlled fixation onthefacemightmodulatethefrequencyofspontaneous 2.1.1. Participants. The data of 46 TD participants (25 males yawning irrelevant to the perception of others’ yawns, not the and 21 females) and 26 participants with ASD (20 males and contagious yawning. 6 females) were included in the final analyses (Table 1). Theaimofthecurrentstudyistotestthepresenceof Additional four participants were tested but not included contagious yawning in ASD, when children’s attention is in the analyses because their eye-tracking data was not re- navigated to yawning stimuli. To achieve that, we designed corded. This was either due to eye tracker problems or not a gaze-contingent stimulus display, in which the participants’ providing valid gaze data in 50% or more observations during gaze was monitored with an eye tracker, and the yawning and theperiodofstimuluspresentationinayawnblock(amale control movies started only when participants were fixating participant with ASD and 3 TD male participants [32–34]). on the eyes (Experiment 1) or the mouths (Experiment 2) of Moreover, an additional male participant with ASD was thestimuli.Wealsoaskedparticipantstocountthenumber tested but not included in the analyses because he was unable ofpeoplewearingeyeglasses(Experiment1)orhavingabeard to answer the question about what the models were doing (Experiment 2), to further ensure that they were attending to after the yawning block [11]. the face. We adopted a block design with an interval between Most of the children were recruited from Musashino blocks, instead of the event-related design with a 1-minute HigashiGakuenwhichhasaprogramtoeducateTDchildren interstimulus interval used in Senju et al. [27]andSenjuet and children with ASD. All the children with ASD had been al. [31]. This was to prevent any possible long-latency effects diagnosed with autism (=14) or pervasive developmental of the yawning stimuli carried over to control stimuli, which disorder (=12) by at least one child psychiatrist, clinical might have affected previous results. Other studies adopting psychologist, or pediatrician before they participated in block designs have demonstrated clearer effects of yawning this experiment. The participants’ parents all completed the stimuli (e.g., [12]). Japanese version of the Autism Screening Questionnaire Three alternative predictions can be derived from differ- (ASQ-J [35, 36]). All ASQ-J scores of the TD children were ent hypotheses. Firstly, if individuals with ASD have an inher- below the cut-off point (13), and those of the children with ent impairment in empathizing which impedes contagious ASD were at or above the cut-off point. yawning, we should not observe contagious yawning (i.e.,
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