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mise à jour du
1 février 2009
Current Psychology Letter
2009;25(1)
Contagious and spontaneous yawning
in autistic and typically developing children
Fiorenza Giganti and Maria Esposito Ziello
Department of Psychology, University of Florence, Italy

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 Tous les articles sur la contagion du bâillement
All articles about contagious yawning
 
Abstract
Previous studies have reported the absence of a contagious effect when autistic children view another's yawning. This result could be due to the difficulty of autistic children in establishing reciprocal gaze behaviour with human partners.
 
Furthermore, the presence of a contagious effect in autistic children could change according their degree of functioning. We evaluated the contagious effect of yawning in both autistic children with different degrees of functioning and in typically developing children exposed to the viewing and hearing of others yawn.
 
Furthermore the frequency and the daily distribution of spontaneous yawning were evaluated and compared among three groups. Autism Spectrum Disorder can selectively affect some behaviour. In autistic children the contagious effect of yawning is largely impaired, whereas the spontaneous production and daily distribution are not. These results support the hypothesis of a link between contagious yawning and social abilities and the existence of different processes underlying spontaneous and contagious yawning.
 
Résumé
L'absence de sensibilité à la contagion du bâillement des enfants autistes, a déjà été rapportée dans un précédent article. Leur difficulté à lier un contact visuel dyadique pourrait en être la cause. En fait, il est possible que cet état diffère suivant le niveau d'atteinte autistique.
 
En projetant une vidéo de bâillements ou faisant écouter un enregistrement sonore de bâillements, nous avons évalué l'effet contagieux projetant une vidéo de bâillements ou faisant écouter un enregistrement sonore de bâillements, nous avons évalué l'effet contagieux du bâillement chez des enfants autistes, dont l'atteinte était plus ou moins profonde, en les comparant à des enfants non autistes.
 
Nous avons également évalué la fréquence et la distribution journalière de bâillements spontanés et comparé entre elles les données recueillies des trois groupes.
 
Chez les enfants autistes, l'effet contagieux du bâillement est profondément altéré, alors que la fréquence des bâillements spontanés et leur distribution journalière ne sont pas modifiées. Ces résultats tendent à confirmer l'hypothèse d'un lien phénoménologique entre contagion du bâillement et aptitude à lier un lien social apparenté à l'empathie. Il en résulte qu'il est probable que les bâillements spontanés et les bâillements contagieux font intervenir des processus neuropsychologiques différentes.

-Giganti F, Hayes MJ, Akilesh MR, Salzarulo P. Yawning and behavioral states in premature infants. Dev Psychobiol. 2002;41(3):289-96.
-Giganti F, Hayes MJ Cioni G, Salzarulo P Yawning frequency and distribution in preterm and near term infants assessed throughout 24-h recordings Infant Behav & Development 2007;30(4):641-647
-Giganti F, Ziello ME Contagious and spontaneous yawning in autistic and typically developing children CPL 2009
-Giganti F, Zilli I. The daily time course of contagious and spontaneous yawning among humans. J Ethol 2011;29(2):215-216
-Giganti F, Zilli I, Aboudan S, Salzarulo P. Sleep, sleepiness and yawning. Front Neurol Neurosci. 2010;28:42-6.
-Giganti F, Salzarulo P. Yawning throughout life. Front Neurol Neurosci. 2010;28:26-31
-Giganti F, Toselli M, Ramat S. Developmental trends in a social behaviour: contagious yawning in the elderly. Giornale di Psicologia dello Sviluppo. 2012;101:111-117
-Giganti F, Guidi S, Ramat S, Zilli I, Raglione LM, Sorbi S, Salzarulo P. Yawning: A behavioural marker of sleepiness in de novo PD patients. Parkinsonism Relat Disord 2013
-Zilli I, Giganti F, Salzarulo P. Yawning in morning and evening types. Physiol Behav 2007;91(2-3):218-222
-Zilli I, Giganti F, Uga V. Yawning and subjective sleepiness in the ederly. J Sleep Res 2008;17:3003-308
INTRODUCTION
Yawning is a widespread spontaneous behaviour observed not only in humans but also in several animal species (Baenninger, 1997; Walusinski & Deputte, 2004). The role and function of the yawn vary according to the animal's place on the phylogenetic scale (Ficca & Salzarulo, 2002). In low evolutive species, yawning seems to be involved in homeostatic processes, whereas in high evolutive ones (mammals and primates) yawning could be linked to environmental needs (increased vigilance level; danger; hunting prey), or even communicative ones (sign of aggressiveness, hierarchic dominance, frustration, sexual excitement, means of synchronised activities within the group).
 
In humans, besides being a spontaneous event, yawning can be "contagious" (Provine, 1986), that is it can be elicited by viewing or hearing another person who yawns. Differently from spontaneous yawning, contagious yawning is observed only in humans (Provine, 1986), chimpanzees (Anderson, Myowa-Yamakoshi, & Matsuzawa,, 2004) and macaques (Paukner & Anderson, 2006). During human development the "contagious" effect of yawning is found starting from four to five years of age and on (Anderson & Meno, 2003), differently from the precocious occurrence of spontaneous yawning observed from the second to third trimester of pregnancy in the foetus (de Vries, Visser, & Prechtl, 1982; Walusinski, Kurjak, Andonotopo, & Azumendi,. 2005), and between 30 to 40 weeks of postconceptional age in preterm newborn infants (Giganti, Hayes, Akilesh, & Salzarulo, 2002; Giganti, Hayes, Cioni, & Salzarulo, 2007).
 
The phase-shift between the emergence of spontaneous and "contagious" yawning could suggest separate processes underlying the two kinds of yawning, apparently similar, but probably different in their meaning. Previous studies on anencephalous newborns able to yawn proposed that the brain's archaic structures were involved in spontaneous yawning occurrence (Price Heusner, 1949). More recently (Daquin, Micallef, & Blin, 2001), clinical and pharmacological studies indicated that several anatomical structures are implicated in the control of yawning, such as the hypothalamus (mainly the paraventricular nucleus), bulbus, pontic regions, with frontal region connections in primates and to the cervical medulla.
 
Neuroimaging studies on contagious yawning found that viewing people yawn involves the activity of the posterior cingulate cortex (Platek, Mohamed, & Gallup, 2005) and superior temporal sulcus (Schürmann, Hesse, Stephan, Saarela, Zilles, Hari, & Fink, 2005): both are known to be associated with empathic processes of mental state attribution (Gallagher & Frith, 2003). Taking into account the link between contagious yawning and the capacity for empathy, some authors (Platek, Critton, Myers, & Gallup, 2003; Schurmann et al., 2005; Senju, Maeda, Kikuchi, Hasegawa, Tojo, & Osanai, 2007) propose that the contagious effect of yawning could be impaired in "empathy disorders".
 
In particular, Senju and colleagues (2007) report the absence of a contagious effect when autistic children view others yawn. The absence of contagious yawning in autistic children reported by Senju's study could be due to the their difficulty in establishing reciprocal gaze behaviour with human partners (Volkmar & Mayes, 1990). Indeed, autistic children look at others less frequently (Swettenham, Baron-Cohen, Charman, Cox, Baird, & Drew, 1998) and show deviant use of reciprocal gaze (Willemsen-Swinkels, Buitelaar, Weijnen, & van Engeland, 1998). Furthermore, the presence of a contagious effect of yawning in autistic children could depend on their degree of functioning and low-functioning autistic children could show a greater impairment in yawning contagiousness with respect to high-functioning autistic children.
 
The aim of this study was to evaluate the contagious effect of yawning in autistic children with different degrees of functioning (high vs low functioning) and in typically developing children using two different modalities: the viewing and hearing of another person yawning. Furthermore, in order to avoid a bias arising from possible differences among groups in spontaneous yawning production, the frequency and the daily distribution of spontaneous yawning were evaluated and compared among three groups.
 
 
DISCUSSION
Our results showed that spontaneous yawning was not impaired in autistic children. In both HFA and LFA children the daily yawn frequency was similar to that observed in TD children. In addition, daily yawn distribution in autistic children corresponded closely to the daily distribution not only of TD children but also of adult people (Provine, Hamernik, & Curchack, 1987; Baenninger, Binkley, & Baenninger, 1996). Indeed the number of yawns was high during the morning, decreased in the afternoon and increased in the evening approaching onset of sleep. Different from spontaneous yawning, contagious yawning seems to be impaired in autistic children. Indeed, typically developing children yawned more watching or hearing others yawn than both HFA children (only one of them yawned observing others yawn) and LFA children (none of them yawned either observing or hearing others yawn).
 
This result does not depend either on the differences of spontaneous yawning among the three groups or the differences of spontaneous yawn distribution during the daytime. Consistent with previous data (Senju et al., 2007), our results showed the absence of contagious yawning in autistic children when they view others yawning. The contagious effect of yawning during the listening to of others yawning was also impaired in these subjects. This result is contradictory to our hypothesis that autistic children's difficulty of establishing a reciprocal gaze behaviour with their caregivers and other people (Volkmar & Mayes, 1990) could affect the contagious effect during the observation, but not during the listening to of others yawns.
 
Therefore, our data pointed out that a specific disorder such as ASD can selectively affect some behaviours such as yawning. Indeed, whereas the spontaneous production of yawning in autistic children appeared to be preserved, yawning in response to the observation or to the listening to of others yawning was largely impaired. This result together with the phase-shift between the emergence of spontaneous and that of "contagious" yawning, contribute to bear out the hypothesis of separate processes underlying the two kinds of yawning. The absence of contagious yawning in autistic children and the impaired capacity for empathy reported in these subjects (Baron-Cohen, Knickmeyer, & Belmonte, 2005) support the widespread proposal (Anderson et al., 2004; Platek et al., 2005; Schurmann et al., 2005) of a link between contagious yawning and social abilities such as self-awareness and mental state attribution that show an atypical development in ASD (Leslie & Frith 1988; Baron-Choen, Leslie, & Frith,1985).
 
It is unlikely that the absence of contagious yawning in autistic children could be due to impairments of imitative abilities or of the mirror neuron systems involved in action and intention understanding found in these subjects (Dapretto, Davies, Pfeifer, Scott, Sigman, Bookheimer, & Iacoboni, 2006). In this regard, it is noteworthy to observe that autistic children are able to mimic behaviours such as smiles and laughter in our "control" conditions. Indeed, even if the evaluation of the contagious effect of laughing was not our main aim, we observed that in the control condition high functioning autistic children tend to smile more watching others smile than watching others yawn (z= -1.84; p=. 06) and laughed more listening to others laugh than listening to others yawn (z=-2.03; p= .04). These results could be interpreted also taking into account the proposal to consider empathy a "collection of partially dissociable neurocognitive systems" (Blair, 2005, pag. 698).
 
In particular three different levels were described: cognitive, motor and emotional empathy. Cognitive empathy refers to the ability to represent the mental state of others; motor empathy refers to the capacity to automatically mirror vocalizations, facial expressions and motor behaviours of another person and finally emotional empathy refers to the recognition and response to emotional expressions of other people, as well as various other emotional stimuli. Autistic subjects were found to be impaired with respect to both cognitive and motor empathy, whereas they seemed to show less difficulties with respect to emotional empathy (see Blair, 2005 for a review).
 
The sensitivity to the contagiousness of yawning could reflect cognitive empathy and the absence of contagious yawning in our sample could confirm the impairment in cognitive empathy previously reported in autistic subjects. Moreover, the response to others laughing and smiling (probably reflecting emotional empathy) observed in high functioning autistic children, but not in low functioning ones, not only supports data about the presence of emotional empathy in autistic subjects, but also suggests different levels of empathic capacities according to the degree of functioning.
 
Finally, the contagious effect of yawning was confirmed in typically developing children in agreement with previous results showing this effect in younger children (Anderson & Meno, 2003). Furthermore, this is the first study to show the contagious effect of yawning in children listening to others yawn. It is interesting to observe that the percentage of contagious yawning found in typically developing children was higher than the percentage reported by Provine (2005) in the young adult. Indeed, whereas in our study 70 % of children yawned watching others yawn, only 55% of young adults yawned (Provine, 2005) while observing yawns. Maybe children are less subject to the social inhibition of yawning than young adults. Indeed, Provine (2005, p.539) reported that "even highly motivated and prolific yawners [...] stopped yawning when placed before the camera" of a national television.
 
In conclusion, our study showed that ASD can selectively affect some behaviours. In autistic children the response to yawning, both viewed and listened to, is largely impaired, whereas the spontaneous production and daily distribution of yawns is not. These results support the hypothesis of a link between contagious yawning and social abilities and the existence of different processes underlying spontaneous and contagious yawning.
 
 
Ficca G, Salzarulo P Yawning: a facial signal Kos 2003;(212):22-25.