J Autism Dev Disord (2009) 39:15981602 DOI 10.

1007/s10803-009-0785-5

BRIEF REPORT

Brief Report: Does Eye Contact Induce Contagious Yawning in Children with Autism Spectrum Disorder?
Atsushi Senju Yukiko Kikuchi Hironori Akechi Toshikazu Hasegawa Yoshikuni Tojo Hiroo Osanai

Published online: 16 June 2009 Springer Science+Business Media, LLC 2009

Abstract 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 xation on the eyes modulates contagious yawning in ASD. Thirty-one children with ASD, as well as 31 agematched typically developing (TD) children, observed video clips of either yawning or control mouth movements. Participants were instructed to xate to the eyes of the face stimuli. Following instructed xation 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 xate on the yawning eyes. Keywords Yawning Contagious yawning Autism spectrum disorder Empathy Eye xation Gaze

Introduction Contagious yawning (i.e., yawning triggered by perceiving others yawning) is a well-documented phenomenon (e.g., Platek et al. 2003; Provine 1986, 1989; Senju et al. 2007), reported in humans and other primate species (Anderson et al. 2004; Paukner and Anderson 2006) and in dogs (JolyMascheroni et al. 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 and de Waal 2002), and the mirror neuron system (Cooper et al. 2008). In rmann et al. 2005) addition, a neuroimaging study (Schu 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 and 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

A. Senju (&) Centre for Brain and Cognitive Development, Birkbeck, University of London, Malet Street, London WC1E 7HX, UK e-mail: a.senju@bbk.ac.uk Y. Kikuchi H. Akechi T. Hasegawa Department of Cognitive and Behavioral Science, University of Tokyo, Tokyo, Japan Y. Tojo Faculty of Education, Ibaraki University, Ibaraki, Japan H. Osanai Musashino Higashi Gakuen, Tokyo, Japan

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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 xation, especially reduced spontaneous xation on others eyes (e.g., Klin et al. 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 xation on the eyes of yawning stimuli may impede contagious yawning in children with ASD. Other studies have demonstrated that instructed xation 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 xation on the eyes on contagious yawning in children with ASD, by replicating Senju et al. (2007) with additional instruction about the xation on the eyes. The stimuli are exactly the same as those used in Senju et al. (2007), except that a xation stimulus appeared in the future location of the eyes of stimulus faces just before the onset of face stimuli. Children were instructed to maintain xation on the location of the xation stimulus. If the lack of spontaneous eye xation impedes contagious yawning in ASD, children with ASD should yawn equally frequently as typically developing children when their xations 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).

children with ASD had been diagnosed with an autistic disorder by a clinician according to DSM-IV (American Psychiatric Association 2000). In addition, parents of all the participants completed a Japanese version of the autism screening questionnaire (ASQ-J; Berument et al. 1999; Dairoku et al. 2004; the English version is currently published as Social Communication Questionnaire; Rutter et al. 2003), and only the children who scored above the cut-off point (13) were included in the analysis. Four additional children did not meet this criterion and were excluded from the analyses. Note that all TD children scored well below the cut-off in ASQ-J. An abbreviated version of Japanese WISC-III (Japanese WISC-III Publication Committee 1998) was also administered to measure IQ. Note that children with ASD as a group had lower IQs than TD children (t (60) = 5.89, p \ .01) and the ratio of participants gender was different between groups (Table 1), as we matched groups by chorological age. This was to maximize the sample size, thus increasing the statistical power. In addition, we did not predict any effect of IQ or gender because neither affected the frequency of contagious yawning in our previous study (Senju et al. 2007). However, the potential effect of age, IQ and gender was also assessed in the current study (see Results for details). Informed consent was obtained both from the children and their parents. The study was approved by the University of Tokyo Research Ethics Committee and was conducted in the Center for Evolutionary Cognitive Sciences, the University of Tokyo. Stimuli and Procedure The stimuli consisted of six video clips of yawning faces (7 s each) taken from different adult models, and six control video clips (mouth opening, 7 s each) of the same six models. The gaze of the models was straight ahead except in the yawning condition, in which the eyes of the models were closed briey during the yawning reex. All the models were unfamiliar to the participants. Stimuli were presented in a pseudorandom order, with a 1-min

Methods Participants Data from 31 children with ASD and 31 age-matched TD children were included in the analyses (Table 1). All the

Table 1 Participants age, verbal, performance and full IQ and score on the Japanese version of autism screening questionnaire (ASQ-J) Group ASD (n = 31, 4 females, 27 males) M(SD) Age (years) Verbal IQ Performance IQ Full IQ ASQ-J 12.0(3.1) 84.7(27.4) 87.2(22.8) 85.8(22.2) 22.9(5) Range 717 46148 46124 46133 1331 TD (n = 31, 19 females, 12 males) M(SD) 11.9(2.1) 116.6(15.3) 109.5(15.9) 112.6(12) 1.4(1.9) Range 717 94154 82154 91145 07

ASD children with autism spectrum disorders; TD typically developing children; IQ intelligence quotient

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inter-stimulus interval. These stimuli were exactly the same as in our previous study (Senju et al. 2007), except that a small xation stimulus was presented for 1 s on the location where the eyes of the face stimuli would appear, just before the presentation of each face. During the interval, a silent cartoon animation was presented to focus the participants attention on the display. Stimulus sequences were presented on the 14.1-inch TFT monitor of a laptop computer placed about 70 cm from the participant. The face that appeared measured 10 9 15 cm and the xation measured 1 9 1 cm, on the monitor. All the participants viewed the movies by themselves in a soundproofed room. They were asked to xate to the xation point whenever it appeared, and count the number of female faces that appeared during the movie. All the children correctly counted the faces, which ensured that they attended to the display. The faces of the participants were recorded using a custom-built hidden video recorder. The videos were coded off-line. The coder was blind to the stimulus the children were watching. Yawning was dened as the presence of the stereotyped motor pattern of deep inspiration, a brief pause accompanying eye occlusion, and following expiration with open mouth (Provine 1986). After the coding, the number of yawns during or after the observation of each stimulus (and before the onset of the following stimulus) was calculated and analyzed. A second coder also coded a subset of the video recordings (i.e., eight children for each group), and inter-rater reliability was very high (j = .902).

yawns reached signicance in yawning or control conditions (MannWhitney tests: zs [ -1.44, ps [ .15) (Fig. 1b). Similarly, within-group analyses also did not show any difference between yawning and control videos in the ASD or TD group (Wilcoxons signed rank tests: zs [ -.17, p [ .13). In both children with ASD and TD children, the number of yawns did not correlate with age, IQ or scores of ASQ-J (Spearman: all rho \ .25, p [ .10). The effect of gender on the frequency of yawning in the yawn and control conditions was examined in both the ASD and TD group, and no signicant effect of gender was found (MannWhitney tests: zs [ -1.56, ps [ .15). We also analyzed whether the number of yawns differed between the current experiment and Senju et al. (2007), to test whether instructed xation on the eyes signicantly increased the number of yawns in children with ASD. However, the difference between experiments did not reach signicance (MannWhitney tests: zs [ -1.23, ps [ .21).

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 (Fig. 1), although the difference did not reach statistical signicance. 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 xation 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

Results On average, TD children yawned 1.0 times in the yawning condition and 1.2 times in the control condition. Children with ASD yawned .9 times in the yawning condition and .7 times in the control condition (Fig. 1b). Unlike in Senju et al. (2007), in which the yawning videos elicited more yawning in TD children than in children with ASD (Fig. 1a), no difference between groups in the number of

Fig. 1 Average frequency of yawns of participants during or after the observation of yawn and control conditions a in Senju et al. (2007) and b in the current study. TD, typically developing children; ASD, children with autism spectrum disorder; **, p \ .01; *, p \ .05. Modied, with permission, from: Senju et al. (2007)

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to social stimuli such as face and eyes, possibly due to atypical functioning of the amygdala (Grelotti et al. 2002; Hadjikhani et al. 2004; Schultz 2005; Senju and Johnson 2009). 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 and Johnson 2009). 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 rmann et al. 2005). It is also reported that increased (Schu attention to the face can elicit other empathetic response, such as spontaneous mimicry of facial expression, in ASD e et al. 2007). (Magne 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 xate 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 et al. 2008; Southgate and 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 xation may have enhanced yawn contagion in both groups and the effect persisted longer than 1 min, 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 xate on the eyes. The current results need to be treated with caution because of the non-signicant 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 xation 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 specically to the eyes, may have increased the susceptibility to contagious yawning, because the relatively longer duration of stimulus presentation (7 s) allowed participants to freely scan the face after the initial xation on the eyes. Further studies with stricter control of xations, ideally with the use of an eye-tracker to monitor xations, will be required to further investigate the relationship between the exact points of xations and the susceptibility to contagious yawning. Thirdly, we could not

obtain the gold standards of clinical information such as ADI-R (Lord et al. 1994) or ADOS (Lord 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 and Johnson 2009). 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 si 2007), also show mentalizing and self-processing (Miklo 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 et al. 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.
Acknowledgments We thank all the children and their parents for participation, Makiko Maeda for the preparation of the stimuli, and Katarina Begus and Sara Serbin for the help in video coding. This study was supported by Grant-in-Aid for Scientic Research (KAKENHI, B, 19330210) from Japanese Society for the Promotion of Science, and A.S. was supported by an ESRC Research Fellowship (RES-063-27-0207).

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