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26 août 2007
Biology Letters
2007;3:706-708
Absence of contagious yawning
in children with autism spectrum disorder
Senju A, Maeda M, Kikuchi Y, Hasegawa T, Tojo Y, Osanai H
Centre for Brain and Cognitive Development, University of London,
Department of Cognitive and Behavioral Science, University of Tokyo

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This study is the first to report the disturbance of contagious yawning in individuals with autism spectrum disorder (ASD). Twenty-four children with ASD as well as 25 age-matched typically developing (TD) children observed video clips of either yawning or control mouth movements. Yawning video clips elicited more yawns in TD children than in children with ASD, but the frequency of yawns did not differ between groups when they observed control video clips. Moreover, TD children yawned more during or after the yawn video clips than the control video clips, but the type of video clips did not affect the amount of yawning in children with ASD.
 
Current results suggest that contagious yawning is impaired in ASD, which may relate to their impairment in empathy. It supports the claim that contagious yawning is based on the capacity for empathy.
 
INTRODUCTION Contagious yawning (i.e. yawning triggered by perceiving others' yawning) is a well-documented phenomenon (e.g. Lehmann 1979; Provine 1986, 1989; Anderson & Meno 2003; Platek et al. 2003), but surprisingly little is known about the mechanisms underlying it. Contagious yawning is reported in humans and in only a few other primates such as chimpanzee (Pan troglodytes; Anderson et al. 2004) and possibly in stumptail macaques (Macaca arctoides; Paukner & Anderson 2006), even though spontaneous yawning is widespread among vertebrate species (Baenninger 1987).
 
Some authors argue that contagious yawning is a response to an innate releasing mechanism (Provine 1986, 1989), whereas others claim that it is based on the capacity for empathy (Lehmann 1979; Preston & deWaal 2002; Platek et al. 2003). Although various neurological or psychiatric disorders are known to cause abnormal patterns of spontaneous yawning (Daquin et al. 2001), no study has tested whether a neuropathology causes contagious yawning to be impaired. We predicted that individuals with autism spectrum disorder (ASD) would have impaired contagious yawning. ASD is a pervasive developmental disorder, which severely affects social and communicative development (America Psychiatric Association 1994), including empathy (Baron-Cohen et al. 2005; Blair 2005).
 
If contagious yawning is related to the capacity for empathy, then it is possible that individuals with ASD, who have impairment in empathy, show the disturbances in contagious yawning. In addition, a recent neuroimaging study (Schu¨ rmann et al. 2005) reported that observation of others' yawning and susceptibility to yawn in response are related to the activity of the superior temporal sulcus and periamygdalar regions. Since structural abnormalities of these regions are reported in ASD (Schumann et al. 2004; Zilbovicius et al. 2006), they should show disturbances in contagious yawning. However, to date, there are no empirical studies that systematically investigated contagious yawning in ASD.
 
The aim of this study is to assess the contagious yawning of children with ASD, using video clips of yawning as stimuli. Children at or over the age of 7 years participated in the study because Anderson & Meno (2003) reported that children older than 4 years reliably show contagious yawning. In addition to the yawning video clips, control video clips of mouth-opening action were also presented to the participants. If the children with ASD have disturbances specific to contagious yawning, observing yawning videos should elicit less yawning in children with ASD than in typically developing (TD) children, while the amount of yawning should not differ between groups during or after the observation of control videos.
 
 
DISCUSSION This study is the first to demonstrate an impairment in contagious yawning in children with ASD. During or after the observation of a video of a yawning adult, children with ASD yawned significantly less than TD children. This cannot be attributed to the overall differences in the frequency of spontaneous yawning because the amount of yawning did not differ between groups during or after they observed mouth-opening, control, videos. In addition, the results of typically developing TD children replicated a previous study (Anderson & Meno 2003) that TD children yawn more during the observation of others' yawning than other mouth movements. However, others' yawning did not modulate the frequency of yawns in children with ASD.
 
To the best of the authors' knowledge, this is the first report to demonstrate that a neurodevelopmental disorder can lead to an impairment specific to contagious yawning, and not spontaneous yawning. Since atypical development of empathy is reported in ASD (Baron-Cohen et al. 2005; Blair 2005), current results support the claim that contagious yawning and the capacity of empathy share common neural and cognitive mechanisms (Lehmann 1979; Preston & de Waal 2002; Platek et al. 2003).
 
To further examine the involvement of empathy in contagious yawning, it will be important to investigate whether contagious yawning is impaired in other 'empathy disorders' (Preston & de Waal 2002) such as psychopathy, prefrontal damage or front-temporal dementia. One might argue that impaired contagious yawning in ASD relates to the dysfunction of the mirrorneuron system (MNS), as is their imitative impairment (Ramachandran & Oberman 2006). However, this argument needs to be treated with caution.
 
For example, Schürmann et al. (2005) did not find selective activation of Broca's area, the essential component of MNS (Rizzolatti & Craighero 2004), during observation of others' yawning. It suggests 'the non-imitative nature of the yawn contagion that can occur without detailed action understanding' (Schu¨ rmann et al. 2005, p. 1264). Individuals with ASD are known to fixate more to the mouth than to the eyes when watching dynamic facial stimuli (e.g. Klin 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 less fixation to the eyes of yawning stimuli may impede the contagious yawning in children with ASD.
 
Further studies will be beneficial to examine whether the atypical pattern of face fixation contributes to the impairment in contagious yawning. As mentioned above, little is known about the mechanism and development, as well as the function, of contagious yawning. Further studies are required to investigate the relation between contagious yawning and other symptoms of ASD, such as empathy, imitation and/or face fixation. In addition, further studies will be beneficial to explore the developmental course of contagious yawning in ASD. Although we did not find any effect of age or IQ in the current age group, it is still possible that chronological or mental age would affect the manifestation of contagious yawning in other age groups. These would be fruitful lines of research, not only in order to clarify the mechanism and function of yawning, but also to better understand the nature of social and communicative impairment in ASD.
 
 
American Psychiatric Association 1994 Diagnostic and statistical manual of mental disorders. 4th edn. Washington, DC: American Psychiatric Association.
 
Anderson, J.R. & Meno, P. 2003 Psychological influences on yawning in children. Curr. Psychol. Lett. Behav. Brain Cogn. 11,
 
Anderson, J.R., Myowa-Yamakoshi, M. & Matsuzawa, T. 2004 Contagious yawning in chimpanzees. Proc. R. Soc. B 271, (Suppl. 6), S468&endash;S470
 
Baenninger, R. 1987 Some comparative aspects of yawning in Betta splendens, Homo sapiens, Panthera leo, and Papio sphinx. J. Comp. Psychol. 101, 349&endash;354
 
Baron-Cohen, S., Knickmeyer, R.C. & Belmonte, M.K. 2005 Sex differences in the brain: implications for explaining autism. Science 310, 819&endash;823
 
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