mise à jour du
15 juillet 2009
Journal of Autism and Developmental Disorders
Does eye contact induce contagious yawning
Atsushi Senju, Yukiko Kikuchi, Hironori Akechi,
Toshikazu Hasegawa , Yoshikuni Tojo,Hiroo Osanai
Centre for Brain and Cognitive Development, Birkbeck, University of London
University of Tokyo, Department of Cognitive and Behavioral Science


Tous les articles sur la contagion du bâillement
All articles about contagious yawning
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.
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).
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.