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Le bâillement foetal
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
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mystery of yawning 

 

 

 

 

mise à jour du
29 octobre 2017
Iperception
2017;8(4):1-22
Yawning Detection Sensitivity and Yawning Contagion
 
Chan MHM, Tseng CH.

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Tous les articles sur la contagion du bâillement
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Abstract
Contagious yawning-the urge to yawn when thinking about, listening to, or viewing yawning-is a well-documented phenomenon in humans and animals. The reduced yawn contagion observed in the autistic population suggested that it might be empathy related; however, it is unknown whether such a connection applies to nonclinical populations. We examined influences from both empathy (i.e., autistic traits) and nonempathy factors (i.e., individuals' perceptual detection sensitivity to yawning, happy, and angry faces) on 41 nonclinical adults. We induced contagious yawning with a 5-minute video and 20 yawning photo stimuli. In addition, we measured participants' autistic traits (with the autism-spectrum quotient questionnaire), eye gaze patterns, and their perceptual thresholds to detect yawning and emotion in human face photos. We found two factors associated with yawning contagion: (a) those more sensitive to detect yawning, but not other emotional expressions, displayed more contagious yawning than those less sensitive to yawning expressions, and (b) female participants exhibited significantly more contagious yawning than male participants. We did not find an association between autistic trait and contagious yawning. Our study offers a working hypothesis for future studies, in that perceptual encoding of yawning interacts with susceptibility to contagious yawning.
 
 
Introduction
 
Contagious yawning, the urge to yawn when thinking about, listening to, or viewing yawning (Baenninger, 1987), is a well-documented phenomenon observed in human beings, primates (Anderson, Myowa-Yamakoshi, & Matsuzawa, 2004), and dogs (Harr, Gilbert, & Phillips, 2009). Despite research e_orts across more than three decades, the underlying mechanism of contagious yawning remains unclear. However, an expanding range of hypotheses have been proposed, including an innate releasing mechanism (Provine, 1986, 1989), respiratory or circulatory, thermoregulation, the arousal hypothesis, and the social communication view (for a review, see Guggisberg, Mathis, Schnider, & Hess, 2010). Among them, the most intriguing hypothesis that has aroused many researchers' interest is the link between empathy and contagious yawning. For instance, Platek, Critton, Myers, and Gallup (2003) found that contagious yawning could be understood as a social behavior that involves mental attribution (i.e., the propensity to understand another's mental state). They found that individuals with higher susceptibility to contagious yawning are better at recognizing their own faces (i.e., self- face recognition) and theory of mind tasks that capture one's social understanding.
 
If contagious yawning is indeed a social behavior, what is its purpose? Guggisberg and coworkers (2010) attempted to explain the social function of contagious yawning by proposing yawning as a communication signal that spread to other people for survival purposes (i.e., the social or communication hypothesis of yawning). While the biological foundation of yawning might be a change in physiological state (e.g., lung oxygen levels decrease or brain temperature increases) in response to our environment, they proposed that the contagious e_ect of yawning allowed us to communicate with our social group and promotes behavioral synchronization for facing potential threat. Indeed, this idea is not entirely novel&emdash;in an earlier study, Provine (1989) stated that ''the chain reaction of contagious yawning synchronizes the physiological as well as behavioral state of the group'' (p. 213). Similarly, Brothers (1990) introduced the idea that yawning could be a form of social signaling akin to laughter that is contagious. Although speculative, the social or communication hypothesis helps explain the social function of contagious yawning and suggests an account for the relationship between contagious yawning and social understanding.
 
Neuroimaging studies have found that brain regions associated with contagious yawning are also related to social understanding and empathy. Activation in the ventromedial prefrontal cortex, which is known for the processing of social cues and recognition of complex emotional expression (Eslinger & Damasio, 1985; Wager, Phan, Liberzon, & Taylor, 2003), increased during free viewing of a yawning video but not when the video stimuli displayed gaping, coughing, or expressionless faces (Nahab, Hattori, Saad, & Hallet, 2009). Schu¨ rmann et al. (2005) showed that BOLD response signals in the superior temporal sulcus, a region known for being involved in facial expression recognition and empathy (see Narumoto, Okada, Sadato, Fukui, & Yonekura, 2001; Calder & Young, 2005, for a review), increased signiÞcantly when participants watched yawning videos, but not mouth opening videos, and was positively associated with the urge to yawn. Platek, Mohamed, and Gallup (2005) also revealed that watching yawning videos evoked unique activation in the posterior cingulate cortex and precuneus, which play important roles in theory of mind and social processing (Blakemore, Rees, & Frith, 1998; Fletcher et al., 1995). These studies together suggest that brain regions involved in social processing may be heavily involved in contagious yawning.
 
Clinical reports also suggest that individuals' social understanding may relate to their susceptibility to contagious yawning. Children aged 7 to 15 years who had been diagnosed with an autism spectrum disorder (ASD)&emdash;a range of developmental disorders characterized by deÞcits in social interaction&emdash;showed reduced contagious yawning compared with typically developing (TD) individuals when watching a yawning video but not when watching a smiling video (Senju et al., 2007). Helt, Eigsti, Snyder, and Fein (2010) matched mental ages between ASD and TD children aged 5 to 12 years and replicated the Þnding that children with ASD were signiÞcantly less likely than TD children to yawn after being exposed to the experimenter's yawn. In addition, Giganti and Esposito Ziello (2009) compared the frequency of contagious yawning between ASD children with varied severity (characterized by the Childhood Autism Rating Scale) and found that children with low autistic severity elicited more contagious yawning than those with high autistic severity. The clinical reports signiÞed a possible relationship between autistic characteristics and susceptibility to contagious yawning (Baron-Cohen, Leslie, & Frith, 1985; Platek et al., 2003). Nonetheless, it is unclear whether this connection applies to a nonautistic population that can be viewed as a continuous spectrum or exists only in the autistic population.
Previous studies have indicated that even among nonautistic populations, not all individuals were susceptible to contagious yawning. Only 40% to 60% of the nonautistic population display contagious yawning in response to a yawn stimulus (Hoogenhout, van der Straaten, Pileggi, & Malcolm-Smith, 2013; Platek et al., 2003), indicating individual variability in susceptibility to contagious yawning. However, little is known about factors that determine such individual di_erences. To our best knowledge, only one recent study assessed a comprehensive range of factors in explaining individual variation in susceptibility to contagious yawning (Bartholomew & Cirulli, 2014). Among all variables (i.e., basic demographics, empathy, sleep, cognitive performance, testing conditions, and time of day), age, not empathy, was the only factor that could signiÞcantly predict individual variation in susceptibility to contagious yawning: Older participants yawned less than younger participants. Yet, age only explained 8% of the variation, which leaves a huge amount of variation unexplained. Therefore, studies of other variables beyond the commonly studied social factors (e.g., empathy) are warranted.
 
Apart from social di_culties, one well-known characteristic of autistic people is their atypical eye-gazing pattern during face processing, that is, looking at the mouth more than the eyes (Blair, 2005; Gepner, Gelder, & Schonen, 1996; Golarai, Grill-Spector, & Reiss, 2006). This perceptual distinction was proposed as an alternative account for the notable social deÞcits in the ASD population: Their proclivity for not attending to regions containing the most social information (e.g., eyes) might create a perceptual bottleneck for the subsequent processing of social interactions (Baron-Cohen, Wheelwright, & Jolli_e, 1997; Dawson et al., 2004).
Interestingly, two recent Þndings indicated that directing attention to the eyes could e_ectively restore susceptibility to contagious yawning in autistic individuals to the same extent as nonautistic individuals. Senju et al. (2009) instructed both participants with and without autism to Þxate on a location where the eyes of face stimuli would appear. The participants were asked to count the number of female faces while watching video clips of yawning or control mouth movements. When autistic individuals directed their attention to the eyes, they displayed equally frequent yawning responses toward yawning stimuli as did nonautistic individuals. Yet, this study lacked objective measurement (e.g., an eye tracker) of the actual eye gaze to validate whether the e_ect was truly from gaze redirection. With the assistance of an eye tracker, Usui et al. (2013) initiated yawning or control videos only after participating ASD children had continuously Þxated on the eye region of the actor for 500 ms. In the task, participating children counted the number of actors wearing glasses, and Usui et al. (2013) replicated the results from Senju et al.'s (2009) study. The importance of access to the eye region of an inducing stimulus was reported in nonclinical participants (Provine, 1989). When participants viewed a variety of yawning stimuli including a complete-face yawn, no-mouth yawn, no-eyes yawn, and a control stimulus (smile), complete-face yawns evoked signiÞcantly more yawners than a control smiling face (Provine, 1989). The ''no-mouth'' yawn was the only stimuli with deleted facial features that generated as many yawners as the complete-face yawn. Conceivably, removing facial features of a yawn increases the detection di_culty. This in turn diminishes the contagion e_ect of yawning and evokes fewer yawners. This Þnding also suggests that the eye region may contain more fundamental information to evoke contagious yawning than the mouth region.
Other than experimental manipulation to increase detection di_culty by reducing accessibility of facial parts to viewers, does an individual's inherent detection sensitivity to a yawning expression preclude his or her susceptibility to contagious yawning? This question is currently unanswered. Similar to contagious yawning, emotional contagion is well documented as a highly unconscious and automatic behavior of mimicking others' emotional expression. Studies have shown that individuals especially susceptible to emotional contagion are those who can read others' emotional expressions and are sensitive to others' emotions (Doherty, 1997), and that those who mimic others' expressions are better at recognizing others' emotions (Oberman, Winkielman, & Ramachandran, 2007; Stel & van Knippenberg, 2008). Although yawning is not considered an emotion and contagious yawning is not understood as an example of emotional contagion, it is possible that a similar mechanism contributes to the individual variation of both contagion phenomena.
 
The contagion e_ect occurs not only unintentionally in higher level imitation such as action or emotional contagion but also in lower level nonemotional responses such as heart rate (Dimascio, Boyd, & Greenblatt, 1957), pupil size (del Valle Loarte & Garcia Ruiz, 2009; Harrison, Singer, Rotshtein, Dolan, & Critchley, 2006), and temperature contagion (Cooper et al., 2014). The temperature of a participant's hand has been found to decrease signiÞcantly after s/he observed and rated the perceived temperature of actors whose hands were immersed in ice-cold water. Since one possible function of yawning is to lower our body temperature to protect us from critical brain temperature rises, it is possible that both contagious yawning and temperature contagion are important for temperature regulation (Gallup & Eldakar, 2013; Gallup & Gallup, 2008). Notably, the link between sensitivity to temperature contagion and empathy is not clear. A negative correlation between sensitivity to temperature contagion and the Mehrabian balanced emotional empathy scale (a 30-item questionnaire, including items such as ''It upsets me to see someone being mistreated'' rated on a 9-point agree&endash;disagree scale that assess individual's emotional empathy) was found. However, a positive correlation was found with the empathy concern subscale of the Davis interpersonal reactivity scale rated on a 5-point scale (7-item Empathy Concern subscale e.g., ''I often have tender, concerned feelings for people less fortunate than me''). This suggests that the relationship between individual di_erences in empathy and low-level contagion phenomena may not be a simple one.
 
In this study, we contributed to the little-investigated area of individual di_erences in contagious yawning in a nonclinical population by observing individuals' autistic traits, and perceptual detection sensitivity to yawning expressions. We aimed to investigate the interplay between one's yawning detection sensitivity and contagious yawning. We Þrst attempted to extend the clinical Þndings of the link between autistic traits and contagious yawning to a nonclinical sample by examining the association between autism-spectrum quotient (AQ) scores and contagious yawning. Then, we tested the association between sensitivity to emotional/yawning expressions and contagious yawning. The study of individuals' susceptibility to contagious yawning could provide insight into psychiatric disorders such as schizophrenia and autism, as well as general human functioning related to yawning and the contagion e_ect. Our hypotheses are as follows:
 
1°) Individuals with higher autistic tendency will display less contagious yawning.
2°) Individuals with higher sensitivity to yawning expressions will display more contagious yawning.
 
 
Discussion
 
This study revealed that an individual's susceptibility to contagious yawning was associated with his or her yawning detection sensitivity. More speciÞcally, people with higher perceptual detection sensitivity to yawning are especially susceptible to contagious yawning. We did not Þnd that autistic tendencies in this nonclinical population were associated with contagious yawning. We found an unexpected gender e_ect: Females displayed more contagious yawning than males. In summary, gender and yawning detection sensitivity were the two variables associated with individuals' susceptibility for contagious yawning.
 
Our hypothesis that perceptual detection sensitivity to yawning expression contributes to the susceptibility of contagious yawning was supported. Although the underlying mechanism remained unclear, sensitivity to yawning could be a possible precursor of contagious yawning and might be facilitated by gazing at the eye region of the inducer. This is in line with the view from the perceptual perspective that sensitivity to others' expressions (Provine, 1989) and proclivity to look at the eyes (Senju et al., 2009; Usui et al., 2013) play a role in determining the individual's susceptibility to contagious yawning. These intriguing Þndings directed the study of contagious yawning from exploring a higher level of processing (e.g., empathy) to a lower level of processing (e.g., eye scanning patterns and perceptual detection sensitivity). Our Þndings add to the body of research showing that perceptual detection sensitivity to facial expression may alter one's social processing. For example, Kuusikko et al. (2009) used a computer-based emotional recognition test and asked participants with autism to select the correct upper facial basic emotion for each picture. They found that autistic girls scored lower in recognizing happiness and anger than nonautistic girls. This implies a lower sensitivity to emotional expressions and that more cues may be required to detect an emotion. This impedes their social processing and might lead to inappropriate responses in social interactions. Past studies found that patients with depression also exhibit biased emotion perception in emotional recognition tasks, in which they demonstrated lower sensitivity than controls when asked to distinguish happy from neutral expression (Gur et al., 1992; Mikhailova, Vladimirova, Iznak, Tsusulkovskaya, & Sushko, 1996; Surguladze et al., 2004). This reduced ability could have a signiÞcant impact on a person's social processing, which in turn could a_ect their own emotion experiences. While earlier research on contagious yawning highlighted its social and empathetic components by showing that poorer social understanding (e.g., in autism, Senju et al., 2007; and schizophrenia, Platek et al., 2003) depleted one's susceptibility to contagious yawning, here we o_ered another possible early perceptual origin. Hence, our Þnding implied that the later processing of the social information delivered by a yawn may be precluded by low sensitivity to yawning and results in a lower susceptibility to contagious yawning.
 
In addition, our hypothesis that gaze to eye regions enhanced one's perceptual detection sensitivity to expressions including yawning was partly supported by the positive association between Þxation duration to the eye region and perceptual detection sensitivity to yawning. This Þnding is consistent with a study in which eye-gazing patterns of autistic and nonautistic children were recorded when they viewed morphing facial expressions of six di_erent emotions and labeled the emotions (Bal et al., 2010). Results showed that looking more at the eyes was associated with fewer errors in recognition of disgust and surprise and faster reaction times for recognizing fear but not other emotions. This suggested that attention to the eye region increased sensitivity to emotion recognition, at least for fear, surprise, and disgust. Our study extends this Þnding beyond emotion recognition to the recognition of yawning.
 
Our study also reported a female advantage in susceptibility to contagious yawning, which could originate from several possible sources. First, a female advantage in yawning susceptibility could come from a female bias in empathetic ability (for a review, see Christov- Moore et al., 2014), which is known to be related to contagious yawning (Helt et al., 2010; Nahab et al., 2009; Platek et al., 2005; Schu¨ rmann et al., 2005; Senju et al., 2007). Females score higher on self-reported empathy questionnaires than males (Rueckert & Naybar, 2008) and show stronger neural activation in empathy-related brain regions such as the amygdala (Schulte-Ru¨ ther, Markowitsch, Shah, Fink, & Piefke, 2008). However, in our sample, autistic tendency measured by the AQ did not di_er between the two genders. Second, females were reported to excel in emotion recognition tasks (Hall & Matsumoto, 2004; McClure, 2000; Montagne, Kessels, Frigerio, de Haan, & Perrett, 2005; Thompson & Voyer, 2014) and were identiÞed as being better at expressing their own emotions than men. Neuroimaging studies also Þnd that females, but not males, show increased activation of the right inferior frontal cortex, which is known for being involved in emotional contagion (Derntl et al., 2010). In our sampled population, our female participants had marginally signiÞcant higher sensitivity than men in detecting happy faces (p _ .063), but not in angry or yawning faces. Therefore, there was no direct evidence to connect this possibility to our Þnding. Finally, females are more sensitive to nonverbal cues in social communication than men (Hall & Matsumoto, 2004; McClure, 2000; Montagne et al., 2005; Thompson & Voyer, 2014). It is possible that females are more susceptible to contagious yawning than males due to their higher abilities in understanding others' intention through nonverbal cues like yawning. We have no direct measurements to test this hypothesis, and this will be a direction for future studies. Norscia and coworkers (2016a) observed the natural occurrence of contagious yawning among 92 nonstranger dyads and found that female participants yawned more frequently than men in response to others' yawning. As the understanding of gender di_erence in the contagion e_ect is still at its infancy, future studies are warranted.
 
There are at least 15 negative reports on gender di_erences in contagious yawning, and it is worth noting the di_erences between them and our study. First, 3 of the 15 studies investigated children with autism (Helt et al., 2010; Senju et al., 2007, 2009; Usui et al., 2013), a population known to have a low yawning frequency (Senju et al., 2007). This may limit any detectable gender e_ect. Studies with nonclinical populations (e.g., the current study and Norscia et al., 2016a) might o_er a bigger observable range. Moreover, a sexually immature group like children is not a good sample group for studying gender di_erences (Norscia, Demuru, & Palagi, 2016b). Second, 5 of the 15 studies did not include a baseline condition to control for spontaneous yawning (Bartholomew & Cirulli, 2014; Eldakar et al., 2015; Gallup, Church, Miller, Risko, & Kingstone, 2016; Gallup & Eldakar, 2011; Massen, Dusc, Eldakar, & Gallup, 2014). A control condition (i.e., in our case, a smiling video) or a baseline measurement (e.g., spontaneous yawning in Norscia et al., 2016a) o_ers an assurance that the recorded yawning was not predominantly spontaneous yawning, which is known to have no gender di_erence (Schino & Aureli, 1989), but contagious yawning which was our central research interest. Lastly, contagious yawning could be signiÞcantly diminished by social presence (Gallup et al., 2016), and females are more sensitive to social etiquette (Baron-Cohen, O'Riordan, Jones, & Plaisted, 1999). It is possible that the initial female advantage to yawning susceptibility was counterbalanced by the higher inhibition of yawning behavior in females. Participants in 4 of the 15 studies were aware of experimenters' observation of their yawning behavior as they viewed the yawning photos directly in front of the experimenter (Eldakar et al., 2015; Gallup & Eldakar, 2011; Gallup & Gallup, 2007; Massen et al., 2014). This makes it possible that the gender di_erence was absent due to the pressure to inhibit yawning behavior, especially in females, due to the social presence of the experimenters. To reduce participants' awareness of having their yawning behavior observed, our cover story disguised the real study purpose and a hidden webcam was installed to record their yawning for later analysis. In summary, our control baseline, cover story, and experimental design may o_er a more suitable combination to observe a female advantage in susceptibility to contagious yawning.
 
While a previous study reported that age is the only variable contributing to individual susceptibility to contagious yawning (Bartholomew & Cirulli, 2014), we did not Þnd similar evidence for older individuals being less susceptible to yawning when they watched yawning video clips and still images. Our sample had a relatively narrow age range (i.e., 19&endash;26 years old) compared with Bartholomew and Cirulli's study (i.e., 18&endash;83 years old), hence, it may not be large enough to reþect similar age e_ect.
 
Our Þnding that participants with more autistic traits have a lower tendency to gaze at eyes adds to recent reports of an association between autistic traits and eye gazing in nonclinical populations. Individuals with more autistic traits (assessed using the Broad Autism Phenotype Questionnaire) tended to look less at the faces of experimenters who asked participants questions (Vabalas & Freeth, 2016) and had shorter and less frequent saccades on the face during a face-to-face interaction with the experimenters (Freeth, Foulsham, & Kingstone, 2013) compared with participants lower in autistic traits. In a recognition task of artiÞcial faces, Davis et al. (2017) discovered that those who had higher AQ scores on the AQ-social subscale tended to look less at eye regions of the facial stimuli. Our results extend the Þndings to human face photos and videos and indicate that nonclinical individuals lower in autistic traits tend to gaze more at the eyes. This is supplementary to the well-established report of individuals with autism looking less at the eyes (Blair, 2005; Gepner et al., 1996; Golarai et al., 2006).
 
However, we did not Þnd an association between eye-gaze patterns and contagious yawning. This is possibly because the face studying patterns among the nonclinical population were consistently concentrated on the key features. The aforementioned studies revealed the connection with contagious yawning through comparisons between autistic and nonautistic children (Senju et al., 2009; Usui et al., 2013), which might cover a bigger range of di_erences.
 
There are several possible directions for future studies. Despite our e_orts in disguising the main purpose of our study and minimizing participants' awareness of their own yawning, some participants still reported that they suppressed their yawning due to social etiquette. This could potentially a_ect subjects' yawning frequency in response to the yawning stimuli. We included a question on the subjective urge to yawn as a supplementary tool for measuring yawning tendency. In addition, a more objective method, such as myography that measures muscle activity, could be helpful to measure subjects' yawning tendency, including those that are suppressed and undetectable to observation. Moreover, it is worth noting that our yawning stimuli produced a þatter psychometric curve than happy and angry stimuli. All stimuli selected to construct psychometric curves for the three expressions were based on the same intensity rating method, so it is unclear what constituted this di_erence. While the faces considered as the happiest or angriest in the rating task were always considered as ''YES-presence'' in the detection ask, and the neutral faces are always considered as ''NO-presence'' in the detection ask, such connection was less clear in yawning. One possibility is that participants have adopted a di_erent criterion in the Yes-No detection task for yawning from that for happy or angry faces, possibly due to the lack of experience on yawning presence judgment. It is still an unsolved puzzle to us why this occurs, and it may be a possible direction for future study. Lastly, a more extensive screening to exclude participants with clinical conditions and trait-like alexithymia (the lack of own emotion understanding) could be applied in future studies. Individuals with psychiatric disorders such as autism and schizophrenia could have lower susceptibility to contagious yawning, and individuals with alexithymia (which could be measured with the Toronto Alexithymia Scale, Bagby, Parker, & Taylor, 1994; Bird, Press, & Richardson, 2011) may be limited to report accurately on their urge to yawn. Our postexperiment questionnaire showed that our participants were not diagnosed with any psychiatric disorders, and it may be desirable to employ a more extensive pretest screening to rule out factors that could a_ect sensitivity and susceptibility to yawning in future studies.
 
Conclusion
 
Our study revealed that participants with higher yawning sensitivity (but not emotional sensitivity) are more susceptible to contagious yawning, which adds to the growing literature that suggests perceptual deÞcits, such as atypical eye-gaze patterns, might contribute to reduced behavioral contagion. In addition, females were found to display more contagious yawning than males, and the underlying mechanism awaits elucidation by future studies. These Þndings have important theoretical implications for understanding the mechanism of contagious yawning for a nonautistic population. It will be interesting to see whether similar associations exist in a clinical population such as people with autism.
 
In conclusion, our study offers a working hypothesis for future studies to investigate how the perceptual encoding of yawning interacts with susceptibility to contagious yawning.