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
http://www.baillement.com

mystery of yawning 

 

 

mise à jour du
8 janvier 2021
Animal Cognition
Seeing others yawn selectively enhances vigilance:
an eye-tracking study of snake detection
Andrew C. Gallup, Kaitlyn Meyers
 
Evolutionary Behavioral Sciences Program, Department
of Social and Behavioral Sciences, State University of New York Polytechnic Institute, Utica, NY 13502, USA

Chat-logomini

 
Abstract
While the origin of yawning appears to be physiologic, yawns may also hold a derived communicative function in social species. In particular, the arousal reduction hypothesis states that yawning signals to others that the actor is experiencing a down regulation of arousal and vigilance. If true, seeing another individual yawn might enhance the vigilance of observers to compensate for the reduced mental processing of the yawner. This was tested in humans by assessing how exposure to yawning stimuli alters performance on visual search tasks for detecting snakes (a threatening stimulus) and frogs (a neu- tral stimulus). In a repeated-measures design, 38 participants completed these tasks separately after viewing yawning and control videos. Eye-tracking was used to measure detection latency and distractor fixation frequency. Replicating previous evolutionary-based research, snakes were detected more rapidly than frogs across trials. Moreover, consistent with the view that yawning holds a distinct signaling function, there were significant interactions for both detection latency and distractor fixation frequency showing that vigilance was selectively enhanced following exposure to yawns. That is, after viewing videos of other people yawning, participants detected snakes more rapidly and were less likely to fixate on distractor frogs during trials. These findings provide the first experimental evidence for a social function to yawning in any species, and imply the presence of a previously unidentified psychological adaptation for preserving group vigilance.
 
Résumé
A côté des bâillements physiologiques, certains bâillements peuvent également avoir une fonction dérive, par exemple de communication au sein des espèces à vie sociale. En particulier, l'hypothèse de réduction de la vigilance stipule que le bâillement signale aux autres que l'effecteur subit une régulation à la baisse de la vigilance. Si cela est vrai, voir un autre individu bâiller pourrait renforcer la vigilance des observateurs pour compenser l'altération de la vigilance du bâilleur.
 
Ceci est ici testé chez l'homme en évaluant comment l'exposition à des stimuli de bâillements modifie les performances au cours de tâches de détection visuelle de serpents (un stimulus de menace) et les grenouilles (un stimulus neutre). Cette conception a été testée de façons répétées chez 38 participants après avoir visionné des vidéos de bâillements et de contrôle. Le suivi oculaire a été utilisé pour mesurer la latence de détection et la fréquence de fixation du distracteur. Reproduisant les résultats de recherches antérieures en lien avec l'Évolution, les serpents ont été détectés plus rapidement que les grenouilles au cours de ces essais.
 
De plus, conformément à la conception selon laquelle le bâillement a aussi une fonction de signalisation distincte, il y a eu des modifications significatives à la fois sur la latence de détection et sur la fréquence de fixation du distracteur montrant que la vigilance était sélectivement augmentée après l'exposition aux bâillements. Autrement dit, après avoir visionné des vidéos d'autres personnes en train de bâiller, les participants ont détecté des serpents plus rapidement et étaient moins susceptibles de se fixer sur les grenouilles pendant les essais. Ces résultats fournissent la première preuve expérimentale d'une fonction sociale du bâillement chez n'importe quelle espèce, et impliquent la présence d'une adaptation psychologique non identifiée auparavant pour préserver la vigilance de groupe.
 
Introduction
Yawning is characterized by an involuntary and powerful stretching of the jaw with deep inspiration, followed by a temporary period of peak muscular contraction and a passive closure of the jaw with expiration (Barbizet 1958). Yawns, or at least similar patterns of mandibular gaping, have been observed across vertebrate classes (Baenninger 1987) and emerge early on during intrauterine development (De Vries et al. 1982). These phylogenetic and ontological findings suggest yawning has been conserved throughout vertebrate evolution. Moreover, several additional lines of evidence indicate that yawning is an adaptation rather than a byproduct. For example, yawning is an overt response that conflicts with other movement (Miller et al. 2010) and in rare cases can entail extreme costs resulting in subluxation or locking of the jaw (Tesfaye and Lal 1990). In addition, psychological research shows hedonic properties to yawning (Provine and Hamernik 1986) where the inability to achieve full yawns is often perceived as frustrating (Walusinski 2018).
 
Numerous functional hypotheses of yawning have been developed over the last 80 years, with most proposing either (1) individual physiological benefits or (2) communication to others (Guggisberg et al. 2010; Smith 1999). Yawns are known to have two distinct causes: spontaneous yawns appear physiologically driven (Baenninger 1997), and contagious yawns are triggered by sensing yawns in others (Provine 1986). Yawning may therefore be multifunctional, including underlying physiologic actions shared across vertebrates, and derived communicative roles among social species (Gallup 2011).
 
Physiologically, comparative and neurological research suggests that yawns act to modify cortical arousal (Baenninger 1997) and promote state change (Provine and Hamernik 1986; Provine 2005) through enhanced intracranial circulation (Walusinski 2014) and brain cooling (e.g., Gallup et al. 2011; Eldakar et al. 2015; Ramirez et al. 2019). However, aside from being contagious among humans (Pro- vine 1986) and some non-human animals (Anderson et al. 2004; Palagi et al. 2009; Gallup et al. 2015), direct tests of any communicative value to yawning are lacking and no functional outcomes to contagious yawning have been observed (Massen and Gallup 2017). Observational studies of non-human primates report that yawns of differing intensity or morphology (e.g., covered teeth versus uncovered gum yawns) occur more often during certain social contexts, but no clear social functions have been identified for these yawn-types (see Leone et al. 2014; Zannella et al. 2017). Although "threat yawns" have been described as a signal among some primate species, as first noted by Darwin (1872), these gaping behaviors represent directed canine displays with focused visual attention on the target. Therefore, "threat yawns" differ fundamentally from the stereotyped motor action pattern that defines yawning across vertebrate classes, which includes a distinct spatiotemporal organization and disparate physiologic activation with head tilting, eye closure, tearing, and salivating (Anderson 2010; Barbizet 1958; Provine 2012).
 
As a potential signal, one of the most well documented features of spontaneous yawning pertains to its circadian pattern; i.e., yawns are not randomly triggered across the day, but rather occur with greatest frequency before sleeping and/or after waking across diverse species (Ania et al. 1984; Baenninger et al. 1996; Miller et al. 2012a; Provine et al. 1987; Zilli et al. 2007). As a result, yawn frequency in humans is positively correlated with subjective ratings of sleepiness (Giganti et al. 2010). Moreover, yawning occurs naturally among people during states of diminished mental processing and boredom (Provine and Hamernik 1986), as well as during reduced awareness from anesthesia (Kasuya et al. 2005). Due to these connections, the development of computer vision systems for detecting yawning, as a primary indicator of drowsiness and fatigue, has expanded rapidly within the last decade (for a partial sampling, see Abtahi et al. 2011; Yang et al. 2020; Zhang et al. 2015).
 
Consistent with the view that yawns serve to communicate one's internal state (Guggisberg et al. 2010), Dourish and Cooper (1990) proposed that yawning could signal the end of sustained concentration or from the experience of a stressful event. More recently, Liang et al. (2015) coined this the arousal reduction hypothesis, proposing that yawns signal to others that an individual is experiencing a down regulation of arousal and vigilance. In a study of stressful encounters in wild Nazca boobies (Sula granti), these authors showed that, similar to research on budgerigars (Melopsittacus undulatus) (Miller et al. 2010, 2012b) and humans (Eldakar et al. 2017), yawning is absent during exposure to stressors but then becomes potentiated thereafter. These findings were interpreted by Liang et al. as support for the arousal reduction hypothesis, with yawning "communicating to others the transition from a state of physiological and/or psychological arousal (for example, due to action of a stressor) to a more relaxed state" (p. 38; Liang et al. 2015).
 
While the conclusions of Liang et al. (2015) have been critiqued with regards to the inference of communication in the context studied, in particular as it relates to nocturnal yawning by adult boobies and yawning by nestlings in the absence of parents or response from nearby nestlings (see Gallup and Clark 2015), yawns could still hold a signaling function in this and other species within social settings where signals could be readily detected. Yawning is an overt motor action pattern that is reliably identified in others. Recent research shows that even human infants can discriminate yawning from other types of mouth movements (as measured by brain activity) (Tsurumi et al. 2019), suggesting that the detection of yawns in others is biologically important.
 
Here, we propose a novel extension of the arousal reduction hypothesis termed the group vigilance hypothesis. In particular, we posit that the detection of yawns in others functions to increase vigilance in the observer as a means of compensating for any reductions in these processes experienced by the yawner. Consistent with the view that spontaneous yawns are triggered during reduced states of vigilance (Dourish and Cooper 1990; Liang et al. 2015) and arousal (Baenninger 1997) tied to circadian fluctuations in sleep ness (Giganti et al. 2010) and diminished mental processing (Provine and Hamernik 1986; Gallup and Gallup 2007), yawning occurs during major shifts in brain and skull temperature across diverse species (Gallup and Gallup 2010; Shoup-Knox et al. 2010; Eguibar et al. 2017; Gallup et al. 2017).
 
Accordingly, in terms of social functionality, yawns may not only serve to signal the internal state of the actor, but the detection of yawns in others is predicted to initiate neurophysiological changes to modify the mental state of observers that would function to maintain or improve group vigilance. In support of this hypothesis, imaging studies on humans show distinct patterns of neural activation indicative of enhanced vigilance and threat detection following exposure to yawns. For example, visual and auditory yawning stimuli have been shown to activate regions of the prefrontal cortex (PFC) (Nahab et al. 2009; Arnott et al. 2009) and the superior temporal sulcus (STS) (Schu_rmann et al. 2005; Tsurumi et al. 2019), and these very same brain areas have been implicated in attentional allocation to biologically relevant and threatening stimuli (Mobbs et al. 2007; Dinh et al. 2018), vigilance (Parasuraman et al. 1998; Nelson et al. 2014), and visual search tasks (Ellison et al. 2004; Bichot et al. 2015). Together, this neurological coupling suggests that merely sensing yawns from others could enhance processing in these domains. If true, this would represent the first evidence for a social function to yawning, which could provide critical insight into the evolution of yawn contagion, as the partial spreading of socially-triggered yawns within a group would help propagate this signal to nearby conspecifics.
 
We tested the group vigilance hypothesis in an experiment designed to examine how exposure to video clips of people yawning altered performance on visual search tasks for detecting threatening and neutral stimuli (snakes and frogs). Based on the group vigilance hypothesis, which extends upon the view that yawns signal a reduction in vigilance by the actor (i.e., Liang et al. 2015), we hypothesized that observing other people yawn would selectively enhance the detection of snakes. Specifically, we predicted that participants would (1) detect target snakes more rapidly, (2) show fewer fixations towards distractor frogs, and (3) show more fixations towards distractor snakes after viewing other people yawn. Snakes represent an ecologically valid stimulus since they have been a recurring survival threat to mammals during evolutionary history (O_hman and Mineka 2003), and estimates suggest that even now snake bites claim the lives of approximately 100,000 people each year (Cheng and Currie 2004). While there is evidence that a specific fear of snakes is developed through learning (Mineka et al. 1984), snakes are nonetheless rapidly prioritized in the visual system even among children without prior experience with these dangerous animals (LoBue and DeLoache 2008). Moreover, research indicates that both humans and non-human primates possess neurological adaptations designed for detecting snakes (i.e., Snake Detection Theory) (e.g., Isbell 2006; 2009; O_hman et al. 2001; O_hman, 2009; Shibasaki and Kawai 2009; Van Le et al. 2013), including regions activated when sensing yawns (Dinh et al. 2018). Therefore, if yawning serves as a signal that increases an observer's vigilance to threats, this should be present for the detection of snakes.
  
Discussion
Although yawning is widespread across vertebrate classes (Baenninger 1987), and contagious yawning has been well-documented in humans and other group-living species (Massen and Gallup 2017), a social function to yawning has not been established. The arousal reduction hypothesis (Dourish and Cooper 1990; Liang et al. 2015) states that yawns signal to others that the individual is experiencing a down regulation of arousal and vigilance. As an extension of this hypothesis, we predicted that viewing other people yawn would improve vigilance.
 
In a high-powered repeated-measures design, we found strong support for the group vigilance hypothesis, showing that exposure to yawning stimuli selectively enhanced the detection of snakes. As predicted, participants detected snakes more rapidly and showed fewer fixations on distractor frogs after viewing vid- eos of people yawning. In addition, the fixation frequency on snake distractors was higher during frog-target searches, albeit marginally, following exposure to yawning stimuli. These effects occurred independent of whether participants reported yawning contagiously as a result of the stimuli, and are consistent with past research showing that merely sensing yawns in others activates neural substrates (i.e., PFC and STS) involved in threat detection, sustained attention, and visual search (Bichot et al. 2015; Dinh et al. 2018; Ellison et al. 2004; Mobbs et al., 2007; Nelson et al. 2014; Parasuraman et al. 1998). The fact that exposure to people yawning improves the detection of snakes, but not frogs, implies that the neurological effects of observing yawns are domain specific to threaten stimuli.
 
A similar, yet distinct connection between yawning and vigilance has previously been suggested in the literature, though this relied on the transmission of yawn contagion (Gallup and Gallup 2007). According to the brain cooling hypothesis, the physiological consequences of yawning serve to counteract intermittent rises in brain temperature and enhance mental processing, and thus the transmission of yawns across group members through contagion is predicted to improve collective vigilance and facilitate adaptive responses to external stimuli (Miller et al. 2012b). However, psychological experiments show that contagious yawning is highly variable and occurs in less than 50% of participants even following exposure to repeated yawning stimuli (Platek et al. 2003; see Anderson et a, 2004 for similar findings in chimpanzees), suggesting an even lower rate of contagion under natural conditions (Anderson 2020; Kapita_ny and Nielsen 2017). In addition, research measuring brain activity through electroencephalography has cast doubt on whether the motor action pattern of yawning alters vigilance levels (Guggisberg et al. 2007), though these particular findings may not generalize to the larger population since the sample studied experienced excessive daytime sleepiness (Gal- lup 2011). Conversely, if merely sensing yawns in others is sufficient to improve vigilance, as shown here, then even partial spreading of this response through contagion could effectively modify the collective detection of threats among groups in real-world settings. Research examining the spatial and temporal factors driving the acquisition of visual information in human crowds suggests that signals from just a small proportion of contagious yawners could propagate among natural aggregates (Gallup et al. 2012). Therefore, the current findings are consistent with the hypothesis that contagious yawning enhances group vigilance (Gallup and Gallup 2007), but indicate that this follows at least in part, if not primarily, from a signaling function of yawning.
 
These findings offer novel insights into the multifunctionality of yawning in social species, and improve our understanding of some previously documented factors that influence yawn contagion. In light of the effects observed here, the high spontaneous yawning frequency experienced in the evening (e.g., Zilli et al. 2007), for example, appears to not only function in triggering neurophysiological changes at the end of the waking hours (Gallup and Gallup 2007; Provine et al. 1987), but may also serve as a signal to enhance the detection of threats during this vulnerable period of the night prior to sleep onset. For example, previous research has shown that snake bites are most common in the evening (Rahman et al. 2010), when the incidence of contagious yawning is highest (Giganti and Zilli 2011). From an evolutionary perspective, the higher rate of contagious yawning between kin and in-group members reported in Hominidae (Campbell and De Waal 2011; Norscia and Palagi 2011; Norscia et al. 2020; Palagi and Norscia 2013; Palagi et al. 2014) is consistent with the proposed signaling function to yawning as this could promote inclusive fitness.
 
Some limitations to this study should be acknowledged. For one, although we demonstrate a robust effect on vigilance following exposure to yawning, the video stimuli used as a control did not include a comparable, non-yawning, gaping of the jaw. Therefore, in addition to the presence or absence of yawning, there were differences between these conditions in terms of a wide mouth opening. However, there are strong grounds to expect that the results here are specific to yawning and not from other gaping movements. In particular, there is clear neurological evidence that humans begin to discriminate yawning from other mouth movements in infancy (Tsurumi et al. 2019). Moreover, studies demonstrating an enhanced activation of brain regions involved in threat detection after viewing yawns previously controlled for gaping and wide mouth openings, showing that these neurologic effects are tied to the distinct motor action pattern of yawns (Nahab et al. 2009; Schu_rmann et al. 2005; Tsurumi et al. 2019). In other words, simply viewing non-yawning gaping movements fails to induce comparable neural changes in the PFC and STS that are proposed to explain these observed effects.
 
Another limitation to this study was the use of just one type of threatening and neutral animal within the search tasks, i.e., snakes and frogs. Although snakes represent a recurrent survival threat to humans during evolutionary history, and there is evidence for specialized neurobiological adaptations in primates for detecting snakes (Isbell 2006, 2009; O_hman et al. 2001; O_hman, 2009; Shibasaki and Kawai 2009; Van Le et al. 2013), it remains unknown whether exposure to yawning would improve the detection of other types of threatening stimuli.
 
Further research should therefore expand upon these initial findings using a variety of threatening and non-threatening stimuli. For example, to assess whether the neurological effects of observing yawns are specific to ancestral threats, future research could investigate whether seeing others yawn similarly enhances the detection of novel threats that are learned within modern environments (e.g., guns and hypodermic needles).
 
The experimenter presence during testing was also a limitation to this study, as it likely reduced the rate of yawn contagion (Gallup et al. 2016; 2019). While we were able to show that the enhanced vigilance from viewing yawns was independent of whether participants reported yawning contagiously, the small number of yawning participants did not permit statistical comparisons to participants that did not yawn. However, descriptive data in Table 1 indicate a Data presented as mean ± standard deviation greater improvement in detection latency during snake trials for participants that yawned, suggesting that the combination of visual exposure to yawns and subsequent yawn contagion may produce an even greater effect on vigilance (as suggested by the brain cooling hypothesis, Gallup and Gallup 2007). Further research is needed to examine this possibility, as well as whether merely sensing yawns in others induces changes in arousal similar to when individuals experience yawning themselves (Baenninger 1997).
 
In summary, the findings from this study provide the first experimental evidence for a social function to yawning in any species, and imply the presence of a previously unidentified psychological adaptation for preserving group vigilance. We hope this work spurs future research examining the relationship between yawning and vigilance in both humans and non-human animals. In addition to replicating and extending upon the visual search tasks performed here in the laboratory, future studies could test for similar effects using auditory stimuli (Massen et al., 2015). Moreover, follow-up studies should investigate how sensing others yawn alters scanning rates and other indicators of vigilance under natural conditions. If attempts to replicate and expand upon the group vigilance hypothesis are successful, this theoretical insight into the signaling function of yawning could provide a major advance in our understanding of the evolution and elaboration of yawning via contagion and distinct yawn- types among social vertebrates.