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
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

mystery of yawning 



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mise à jour du
18 juuillet 2021
Hum Nat
 Yawning Is More Contagious in Pregnant
Than Nulliparous Women:
Naturalistic and Experimental Evidence
Norscia I, Agostini L, Moroni A, Caselli M,
Micheletti-Cremasco M, Vardé C, Palagi E.  


 Tous les articles sur la contagion du bâillement
All articles about contagious yawning
Contrary to spontaneous yawning, which is widespread in vertebrates and probably evolutionary ancient, contagious yawning-yawning triggered by others' yawns-is considered an evolutionarily recent phenomenon, found in species characterized by complex sociality. Whether the social asymmetry observed in the occurrence of contagious yawning is related to social and emotional attachment and may therefore reflect emotional contagion is a subject of debate. In this study the authors assessed whether yawn contagion was enhanced in pregnant women, a cohort of subjects who develop prenatal emotional attachment in preparation for parental care, via hormonal and neurobiological changes. They predicted that if yawn contagion underlies social and emotional attachment, pregnant women would be more likely to contagiously yawn than nonpregnant, nulliparous women of reproductive age. They gathered data in two different settings.
In the experimental setting, 49 women were exposed to video stimuli of newborns either yawning or moving their mouth (control) and we video-recorded the women during repeated trials to measure their yawning response. In the naturalistic setting, 131 women were observed in a social environment and their yawning response was recorded. They tested the factors influencing the yawning response, including the reproductive status (pregnant vs. not pregnant). In both settings, yawn contagion occurred significantly more in pregnant than nonpregnant women. By showing that pregnant women were most likely to respond to others' yawns, these results support the hypothesis that the social variation observed in yawn contagion may be influenced by emotional attachment and that yawning in highly social species might have been coopted for emotional contagion during evolution.
Contrairement au bâillement spontané, qui est répandu chez tous les vertébrés donc probablement ancien, le bâillement contagieux - le bâillement déclenché par les bâillements des autres - est considéré comme un phénomène évolutif récent, trouvé chez les espèces caractérisées par une socialité complexe. La question de savoir si l'asymétrie sociale observée dans la survenue du bâillement contagieux est liée à l'attachement social et émotionnel et peut donc refléter une contagion émotionnelle est un sujet de débat. Dans cette étude, les auteurs ont évalué si la contagion du bâillement était augmentée chez les femmes enceintes, c'est à dire des sujets qui développent un attachement émotionnel prénatal en préparation aux soins parentaux, via des changements hormonaux et neurobiologiques.
Ils ont prédit que si la contagion du bâillement sous-tend l'attachement social et émotionnel, les femmes enceintes seraient plus susceptibles de bâiller de manière contagieuse que les femmes nullipares non enceintes et en âge de procréer. Ils ont collecté des données dans deux contextes différents. Dans le cadre expérimental, 49 femmes ont été exposées à des stimuli vidéo de nouveau-nés bâillant ou bougeant la bouche (témoin) et ils ont enregistré les femmes lors d'essais répétés pour mesurer leur réponse au bâillement. Dans le cadre naturaliste, 131 femmes ont été observées dans un environnement social et leur réponse de bâillement a été enregistrée. Nous avons testé les facteurs influençant la réponse au bâillement, y compris le statut reproducteur (enceinte vs non enceinte). Dans les deux cas, la contagion du bâillement s'est produite significativement plus chez les femmes enceintes que chez les femmes non enceintes. En montrant que les femmes enceintes étaient les plus susceptibles de réagir aux bâillements des autres, nos résultats soutiennent l'hypothèse que la variation sociale observée dans la contagion du bâillement peut être influencée par l'attachement émotionnel et que le bâillement chez les espèces hautement sociales pourrait avoir favorisé la contagion émotionnelle au cours de l'évolution.
Whereas spontaneous yawning is independent from the perception of others' yawns, contagious yawning occurs when the yawn emitted by a subject (trigger) acts as a releasing stimulus (sensu Tinbergen and Perdeck 1951) and elicits yawning in another subject (responder) (Provine 1989). Although morphological variants are present in yawns, especially in primates (e.g., chimpanzees, Pan troglodytes, Vick and Paukner 2010; geladas, Theropithecus gelada, Palagi et al. 2009; Tonkean macaques, Macaca tonkeana, and Japanese macaque, M. fuscata, Zannella et al. 2017; humans, Homo sapiens, Provine 1986, 2012), spontaneous yawning is probably a plesiomorphic (ancestral) trait because it has been recorded in a wide array of vertebrates (Baenninger 1987).
To the contrary, contagious yawning between conspecifics has been observed thus far in a relatively small number of species (Palagi et al. 2020) and may be an apomorphic trait, which appeared more recently in vertebrate evolution. With one exception (Pongo pygmaeus; van Berlo et al. 2020), the species exhibiting yawn contagion between conspecifics usually live in highly social groups: namely, all the extant hominine species (chimpanzees: Anderson et al. 2004; Campbell and Cox 2019; Campbell and de Waal 2011; bonobo, Pan paniscus: Demuru and Palagi 2012; Tan et al. 2017; but see Amici et al. 2014 on a very small sample size; humans: Provine 1986, 1989), two species of cercopithecines (geladas and Tonkean macaques; Palagi et al. 2009; Palagi and Norscia 2019), non primate mammals (lions, Panthera leo: Casetta et al. 2021; wolves, Canis lupus lupus: Romero et al. 2014; sheep, Ovis aries: Yonezawa et al. 2017; elephant seals, Mirounga leonina: Wojczulanis-Jakubas et al. 2019; domestic pigs, Sus scrofa: Norscia et al. 2021), and one social bird species (budgerigar, Melopsittacus undulates: Gallup et al. 2015).
One of the most remarkable aspects of intra-specific yawn contagion is that it shows social asymmetry in all the species where this aspect has been investigated (Campbell and de Waal 2011, 2014; Demuru and Palagi 2012; Massen et al. 2012; Norscia and Palagi 2011; Palagi et al. 2009; Romero et al. 2014). The yawning response is most likely or precisely triggered by yawns coming from individuals that are "socially relevant" to the potential responders, even though the communicative value of the triggering yawns (e.g., threat, tiredness) can vary. For example, in humans the yawning response is highest between familiar subjects (Norscia and Palagi 2011). In chimpanzees, living in social groups characterized by male dominance, males seem to respond more when the triggering yawn comes from the dominant males (Massen et al. 2012), whereas in bonobos, living in groups with female dominance, females seem to be more effective in eliciting others' yawns (Demuru and Palagi 2012). Indeed, bonobos and chimpanzees preferentially attend familiar subjects of the dominant sex (Lewis et al. 2021). In geladas, the female dyads, which are responsible for maintaining group cohesion, showed the most precise matching of different yawning types (Palagi et al. 2009).
The social attachment between individuals seems also to affect the rates of yawn contagion. In dogs (Canis lupus familiaris), the evidence of interspecific yawn contagion (dog/human) and its modulation is mixed (for review: Neilands et al. 2020; Palagi and Cordoni 2020); in wolves, top rates of intraspecific yawn contagion were found between strongly bonded subjects (with bonding being measured by assessing the level of affinitive behavior; Romero et al. 2014). Adult chimpanzees (but not immature chimpanzees, Madsen and Persson 2013) yawn more in response to the yawns of ingroup than outgroup members (Campbell and de Waal 2011). Bonobos (in vivo but not when exposed to video stimuli; cf. Tan et al. 2017) show the highest yawning response between closely bonded individuals (Demuru and Palagi 2012; Palagi et al. 2014). A similar situation occurs in geladas, with yawn contagion being greatest between individuals that affiliate the most (Palagi et al. 2009). In humans, yawn contagion is higher in kin and friends than in acquaintances and strangers (Norscia and Palagi 2011; Norscia et al. 2016), and the familiarity bias remains when the yawns are heard but not seen (Norscia et al. 2020).
Based on neuroethological evidence, it has been hypothesized that in highly social species yawning may have been coopted during evolution for emotional contagion, a basic building block of empathy (de Waal and Preston 2017; Palagi et al. 2020). However, at present, it is highly debated for both human and nonhuman animals whether the social asymmetry observed in yawn contagion depends on interindividual bonding, possibly reflecting emotional attachment, as postulated by the Emotional Bias Hypothesis (EBH), and/or on other factors, such as attentional levels, social dominance, or as-yet undefined aspects of the social setting (Adriaense et al. 2020; Kapita_ny and Nielsen 2017; Massen and Gallup 2017; Palagi et al. 2020).
Emotional contagion and empathic processes are assumed to have evolved from mother&endash;offspring bond (for review: Preston 2013). Pregnant women are particularly suitable to investigate the link between yawn contagion and bonding because they undergo heavy psychological, physiological, and neurobiological changes leading to the development of maternal attachment and caregiving (Barba-Mu_ller et al. 2019; Napso et al. 2018; Tichelman et al. 2019). These changes often alter body systems so that pregnant women perform and act differently (e.g., with respect to dietary choice, motor activity, sensitivity to emotional stimuli) than nonpregnant women in the general population (Crozier et al. 2009; Gradmark et al. 2011; Moya et al. 2014; Oso_rio et al. 2018).
Although proposing different underlying mechanisms, definitions, and measures, (Brandon et al. 2009), the psychological literature addressing attachment theory (originally introduced for the postpartum period; Bowlby 1969) converges in indicating that mother-infant bonding starts long before birth, during pregnancy (Ferrari et al. 2016; Sadeghi and Mazaheri 2007; Salehi and Kohan 2017; Sedgmen et al. 2006). During gestation, women develop what Rubin (1975:149) called a sense of "we-ness," later defined as prenatal attachment, the emotional and psychological bond between the mother and her unborn child (Brandon et al. 2009; Rossen et al. 2017). The mother-infant bonding quality developed in pregnancy is important because it is positively associated with the mother-infant bonding quality after birth (Tichelman et al. 2019).
Psychobiological changes during pregnancy, involving hormonal and maternal brain adaptations, occur in both human and nonhuman mammalian females to support the transition to parenthood (Kim 2016; Lonstein et al. 2015). In women, the establishment of prenatal attachment is sustained by recent neurobiological evidence. Via magnetic resonance imaging (MRI), Hoekzema et al., (2017) found that during pregnancy women's brains undergo dramatic, long-lasting changes in areas that significantly overlap with areas involved in the Theory of Mind (ToM) (i.e., anterior and posterior cortical midline and specific sections of the bilateral lateral prefrontal and temporal cortex; Hoekzema et al. 2017). ToM, among other aspects, is related to the ability to read others' emotions (affective ToM; Abu-Akel and Shamay-Tsoory 2011). Brain changes are also linked to the development of maternal attachment and can significantly predict the quality of future mother-infant attach- ment (Hoekzema et al. 2017).
Psychological and neurobiological changes are interconnected with the massive hormonal variations that occur in women during gestation (Barba-Mu_ller et al. 2019; Glynn and Sandman 2011). Changes in the so-called maternal brain (including areas especially involved in maternal caregiving) are mediated by glucocorticoids, prolactin, and oxytocin, whose levels increase across pregnancy (Kim and Strathearn 2016; Napso et al. 2018; Prevost et al. 2014; Slattery and Hillerer 2016). Moreover, prolactin&endash;Growth Hormone (GH) family and neuroactive hormones, including melatonin and its precursor serotonin, prepare pregnant women to adequately care for their offspring by impacting on different physiological functions (Le_vy 2016; Napso et al. 2018). Oxytocin is the neuroactive hormone that is thought to play a major role in the development of maternal attachment and, more generally, social bonding in humans and other animals (Decety et al. 2016). Although contextual and interindividual factors can mitigate or even reverse the effects of oxytocin (Beery 2015; Olff et al. 2013), during pregnancy oxytocin is involved in the emergence of mother-infant emotional bonding and, in humans, also in the mental representations typical of such bonding (Decety et al. 2016; Feldman et al. 2007).
In summary, yawn contagion may be related to emotional attachment (as predicted by EBH), and pregnant women represent a cohort of subjects that is bio- logically and psychologically "equipped" for mother-infant emotional attachment (Barba-Mu_ller et al. 2019; Brandon et al. 2009; Palagi et al. 2020; Tichelman et al. 2019). Hence, to check for further evidence of the association between yawn contagion and social attachment, possibly reflecting emotional attachment (de Waal and Preston 2017), we focused on the yawning response in pregnant women. In particular, we predicted that if social asymmetry in contagious yawning is also driven by interindividual attachment, a proxy of emotional attachment, contagious yawning would occur at higher rates in pregnant compared to nulliparous women.
The results from both the experimental and the naturalistic data converge in indicating that women's reproductive status had an effect on contagious yawning, which was more likely to occur in pregnant than in nulliparous women (here defined as women who were not pregnant and had no children). As a matter of fact, pregnant women were more likely to respond than nulliparous women to both video yawns of unknown infants in the experimental trials and live yawns from adults in the naturalistic setting (Tables 2 and 3; Figs. 3 and 5). This finding, presented for the first time with this study, provides support to the Emotional Bias Hypothesis (EBH) because yawn contagion was highest in the category of women characterized by enhanced social attachment predisposition, owing to the biological and psychological changes typical of the gestation period (Barba-Mu_ller et al. 2019; Brandon et al. 2009; Tichelman et al. 2019).
Since yawn contagion has been found to vary across the day (Giganti and Zilli 2011), we checked whether our yawning response sampling could be biased by the time periods during which the data were collected, depending on the availability of the study subjects. In neither setting did we find a significant effect (Tables 1 and 3), probably because the majority of the data was collected in the morning and in the afternoon (with little data collected at the very extremes of the day).
The use of a twofold approach, involving both experimental and naturalistic data collection, allowed the verification of the possible effect of different variables on yawn contagion. The results of the experimental trials show that the yawning response was significantly higher in the yawning than in the control video condi- tion (Table 1; Fig. 2). This finding confirms that yawn contagion was present in the cohort of human subjects considered in this study (nulliparous and pregnant women) since it has been found in other segments of the population (Arnott et al. 2009; Pro- vine 1989, 2005).
Yawn contagion may be affected by selective, top-down attentional biases (Massen and Gallup 2017), in addition to bottom-up, stimulus-driven attention (Attentional Bias Hypothesis, ABH; Palagi et al. 2020). Therefore, in the experimental setting we checked for selective attention to the stimulus and we found no significant influence of the time of attention to the stimulus source (video screen) on yawning (Table 1), which was high overall in both yawning and control video conditions, as well as in pregnant and nulliparous women. This finding reduces the probability that in our sample a selective attention bias may have accounted for the differences between stimulus (yawning/control) and reproductive status (pregnant/nulliparous) conditions. This is line with evidence indicating, directly or indirectly, that contagious yawning in humans may depend on bottom-up more than top-down selective attention (Norscia et al. 2020; for a review see Palagi et al. 2020). Age is another variable known to possibly affect yawn contagion rates (Bartholomew and Cirulli 2014). In our case, in the experimental setting there was a nonsignificant trend of the influence of age in the yawning response, possibly because the women under study fell within the relatively short reproductive age.
In the naturalistic setting we could verify the effect of a social bond between the trigger and the potential responder on the yawning response. Although the bond was restricted to two categories (strangers and acquaintances) owing to data constraints, and despite showing an inverse correlation with reproductive status, the bond had a significant effect on yawn contagion, which was more likely between subjects who knew each other than between strangers. This finding is in agreement with previous literature showing that relationship quality has an influence on yawn contagion, whose likelihood increases as the strength of the social bond increases (from strangers to acquaintances, friends, and lastly to family members; Norscia and Palagi 2011; Norscia et al. 2016). Norscia et al., (2020) found no difference between strangers and acquaintances when the yawns were heard but not seen, although friends and family responded at significantly higher rates than did those in the other categories. In the absence of the visual cue, it is probably more difficult for the potential responders to discern between subjects with whom they have reduced or no familiarity.
Importantly, our results from the experimental trials show that reproductive status (pregnant/nulliparous) had a significant effect on the yawning response in the yawning video condition but not in the control video condition (cf. Tables 2 and 3). Therefore, only yawning resulting from contagion, and not spontaneous yawning, was affected by pregnancy in our sample. Historical accounts report an increase of spontaneous yawning in the case of certain diseases (e.g., puerperal fever or hemorrhage; Walusinski 2010), and excessive yawning has indeed been indicated as a possible marker of disease in humans (Thompson and Simonsen 2015). Progesterone increases daytime drowsiness and sleeping time (Won 2015) and so it may increase spontaneous yawning rate during pregnancy. In this respect, we cannot exclude that the yawning stimulus might have preferentially primed the yawning motor response in pregnant women also because they experienced increased fatigue (despite showing similar levels of sleep to those of nulliparous women). An investigation on how spontaneous rates vary within subjects across pregnancy, possibly in relation to fatigue and tiredness, and how contagious yawning varies depending on the stimulus (e.g., babies/adults), with hormonal and neurobiological correlates, could better clarify the above issues.
Overall, the different yawning response of pregnant women relative to women with no children can fall within the broad range of the behavioral changes that start occurring during pregnancy, such as motor activity and dietary choice variations (Crozier et al. 2009; Gradmark et al. 2011). Compared with childless women, pregnant women show increased sensitivity to emotional signals and facial expressions. For example, pregnant women were found to perceive infant cries in more differentiated ways than women with no offspring (Bleichfeld and Moely 1984; Yoshiaki 1985). As gestation progresses, pregnant women also show enhanced ability to encode and process emotional faces, especially related to distress (an emotional state; Keltner et al. 2019) as an evolutionary adaptation to motherhood, which requires hypersensitivity to emotional threat signals and contagion (Oso_rio et al. 2018; Pearson et al. 2009). Our results fit with this scenario because they indicate enhanced responsiveness of pregnant women to yawning, which has been linked (with various degrees of evidence) to anxiety and distress in human and nonhuman primates (from lemurs to apes: e.g., Baker and Aureli 1997; Coleman and Pierre 2014; Leone et al. 2014; Palagi et al. 2019; Thompson 2014, 2017; Thompson and Bishop 2012; Zannella et al. 2015). Thompson (2014) has posited that cortisol (involved in the stress response) may be involved in yawn contagion, at least under certain situations. Another hypothesis, not mutually exclusive to the cortisol hypothesis, may be that yawn contagion is, to a certain extent, under the influence of oxytocin, considering that enhanced emotional recognition is one of the effects of oxytocin, whose levels largely increase during pregnancy (Domes et al. 2007; Preston 2013). In particular, oxytocin appears to increase the accuracy of the recognition of faces displaying angry and happy emotions, especially in women (Yue et al. 2018). Mariscal et al., (2019) found that yawn contagion in autism spectrum disorder (ASD) children was positively related to the blood concentration of oxytocin. The possible relationship between oxytocin and yawn contagion is supported by evidence that yawn contagion in humans follows the empathic gradient (sensu Preston and de Waal 2002), being highest between closely bonded subjects (Norscia and Palagi 2011; Norscia et al. 2020). Some features typical of mother-infant attachment, such as social recognition, bonding, and affiliation, are maintained in adult- hood and promoted by oxytocin, which has been found to increase trust (Kosfeld et al. 2005), generosity (Zak et al. 2007), altruism (de Dreu et al. 2010), and both cognitive and affective empathy (Rodrigues et al. 2009; Shamay-Tsoory et al. 2013; Smith et al. 2014; Uzefovsky et al. 2015). One of the future steps is to evaluate the possible covariation between oxytocin and yawn contagion in both pregnant and nulliparous women. Beyond incorporating hormones, further studies could involve postmenopausal versus pregnant women and check how mothers react when they see their own fetus yawning on the echograph screen.
The possible connection between yawn contagion and increased social and emotional bonding is also suggested by the fact that some of the areas that seem to be involved in yawn contagion (such as the ventromedial-prefrontal cortex, superior temporal sulcus, amygdala, insula, posterior cingulate, and precuneus; Nahab et al. 2009; Platek et al. 2005; Schu_rmann et al. 2005) are also involved in mother-infant care, in mother's enhanced sensitivity to the baby, and maternal brain changes occurring during pregnancy (Barba-Mu_ller et al. 2019; Hoekzema et al. 2017; Kikuchi and Noriuchi 2015; Preston 2013; Rifkin-Graboi et al. 2015).
In summary, by showing increased occurrence of yawn contagion in pregnant women, a cohort of subjects that is specifically "programmed" to recognize and respond to others' emotions, this study provides support for the hypothesis that yawn contagion may, at least under certain circumstances, underlie emotional contagion (EBH; Palagi et al. 2020). This process is considered by some scholars a basic form of empathy and occurs when an emotion is transferred from one individual to another, possibly via a motor perception&endash;action mechanism, involving the matching of facial expressions and the resonance of the emotions that underlie such expressions (de Waal and Preston 2017).
The perception&endash;action and the offspring care model both predict that subjects can preferentially attend the stimuli coming from closely bonded others, particularly car- egiving individuals such as pregnant women toward babies (Preston 2013; Preston and de Waal 2002). Visual, top-down attention has limited effect on yawn contagion and does not follow a consistent familiarity trend in hominines because other fac- tors, such as dominance, can come into play (Lewis et al. 2021; Norscia et al. 2020; Palagi et al. 2020). Hence, a possible bonding hypothesis between EBH and ABH is that yawn contagion can be influenced by emotional bonding and attention, mainly directed through bottom-up mechanisms.
Importantly, not all contagious yawning is triggered by emotional resonance, and that is not the point in question here. Contagious yawning also occurs between strangers (Norscia and Palagi 2011), and some people are consistently not susceptible to others' yawns (Bartholomew and Cirulli 2014; Platek et al. 2003; Provine 1986, 1989). Contagious yawning is a form of yawning and, as such, can be related to non-emotional, individual and/or environmental factors, such as time of the day (Giganti and Zilli 2011), age (Bartholomew and Cirulli 2014), and possibly temperature (Gallup and Eldakar 2011). The perception&endash;action mechanism itself is based on a theory in motor control that assumes that our physical motor acts are primed in the brain by observation of those in others, even if they do not bear emotional cues (Preston and de Waal 2002). Thus, contagious yawning can also be a non-emotional motoric response. The pivot around which this study revolves is the possible mechanism leading to the social variations observed in the occurrence of contagious yawning. Although still under debate (Adriaense et al. 2020; Massen and Gallup 2017), various physiological, neuroethological, and psychological studies sustain the possible connection between the social asymmetry of yawn contagion and emotional bonding. Some of the brain areas that appear to be involved in yawn contagion (Nahab et al. 2009; Platek et al. 2005; Schu_rmann et al. 2005) seem to overlap with those involved in emotional processing of internal and external stimuli and empathy (Palagi et al. 2020) and, importantly, with the maternal brain (Barba-Mu_ller et al. 2019; Hoekzema et al. 2017; Kikuchi and Noriuchi 2015; Rifkin-Graboi et al. 2015). Highest levels of yawn contagion are associated with increased oxytocin lev- els (i.e., ASD children; Mariscal et al. 2019), enhanced social bonding (i.e., between friends and family; Norscia and Palagi 2011), and maternal prenatal bonding (i.e., in pregnant women; present study). Lower yawn contagion rates in association with levels of autistic traits were found to be related to attentive rather than background emotional empathy deficits (Helt et al. 2021). Finally, another study found that sub- jects who yawned in response to observing others' yawns exhibited significantly higher empathy scores (Franzen et al. 2018).
Hence, although we cannot discard the possibility that other priming and motor mechanisms may also underlie the social asymmetry of yawn contagion, the hypothesis that this behavior has been coopted during evolution for emotional contagion still stands and gains further support.