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Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
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La parakinésie brachiale oscitante
Yawning: its cycle, its role
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Fetal yawning assessed by 3D and 4D sonography
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mise à jour du
28 mai 2023
Animals (Basel)
2023;13(10):1700
 The Role of Empathic Concern and Gender
on Interspecific Contagious Yawning in Humans
 
 Gallup AC, Wozny SM  

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-Gallup A, Wozny S. Interspecific Contagious Yawning in Humans. Animals (Basel) 2022;12(15):1908.
 
Abstract
Interspecific contagious yawning (CY), whereby yawns from one species trigger yawning in different species, has now been reported across various taxa. This response to human yawning appears common among animals in captivity and has been interpreted as an empathic response towards human handlers/caregivers. A recent study found that humans also display interspecific CY, though this response was not modulated by proxies of empathic processing (i.e., phylogenetic relatedness or social closeness to the animals).
 
Here, the authors explored this relationship more explicitly by assessing how interspecific CY to yawns from common household pets relates to self-reported empathic concern. Participants (N = 103) completed a survey measuring empathic concern and then reported on their yawning behavior following exposure to a control condition or yawning images either from domesticated cats or domesticated dogs.
 
The results provide further evidence for interspecific CY in humans, but empathic concern was negatively predictive of this response. There was also no sex difference in interspecific CY, though when comparing the sexes across CY conditions, women reported a higher frequency of yawning in response to dog yawns, and men reported a higher frequency of yawning in response to cat yawns. Overall, these findings do not support a strong connection between interspecific CY and empathy or emotional contagion.
 
Résumé
La contagion interspécifique des bâillements (CY), par lequel les bâillements d'une espèce déclenchent des bâillements d'autres espèces, a été signalé dans divers taxons. Cette réaction aux bâillements humains semble commune chez les animaux en captivité et a été interprétée comme une réponse empathique envers les humains qui les manipulent ou les soignent. Une étude récente a montré que les humains présentent également un CY interspécifique, bien que cette réponse ne soit pas modulée par des indicateurs de traitement empathique (c'est-à-dire la parenté phylogénétique ou la proximité sociale avec les animaux).
 
Ici, les auteurs ont exploré cette relation de manière plus explicite en évaluant comment le CY interspécifique aux bâillements des animaux domestiques est lié à la préoccupation empathique auto-déclarée. Les participants (N = 103) ont répondu à une enquête mesurant la préoccupation empathique et ont ensuite rapporté leur comportement de bâillements après avoir été exposés à une condition de contrôle ou à des images de bâillements provenant soit de chats domestiques, soit de chiens domestiques.
 
Les résultats fournissent des preuves supplémentaires de l'existence d'un CY interspécifique chez l'homme, mais la préoccupation empathique était un facteur prédictif négatif de cette réponse. Il n'y avait pas non plus de différence entre les sexes dans le CY interspécifique, bien que lorsque l'on compare les sexes entre les conditions du CY, les femmes ont rapporté une fréquence plus élevée de bâillements en réponse aux bâillements de chiens, et les hommes ont rapporté une fréquence plus élevée de bâillements en réponse aux bâillements de chats. Dans l'ensemble, ces résultats ne confirment pas l'existence d'un lien étroit entre le CY interspécifique et l'empathie ou la contagion émotionnelle.
Introduction
Contagious yawning (CY) is a distinctive pattern of behavioral coupling that occurs when the mere detection of yawns by others elicits the automatic and reflexive tendency for an observer to yawn. Yawning can be reliably elicited in this way in humans using images, videos, or audio clips of yawning [1&endash;5], though there is considerable variability in this response [6,7]. While the first experimental demonstration of CY in a nonhuman animal was published less than two decades ago [8], evidence for CY is now present for a growing number of social vertebrates (for a review, see [9]). Various theories have been proposed pertaining to the biological significance of CY [10], with recent evidence indicating a role in facilitating motor synchrony and enhancing vigilance in groups [11,12].
 
Independent of its ultimate function, one view that has gained considerable traction in the scientific community is that CY represents a primitive form of empathic processing, i.e., the tendency to yawn after detecting this action in another could reflect a form of emotional contagion. This idea, which could explain the distinctive individual differences in CY across studies, was initially proposed in a monograph by Lehmann [13] and further elaborated within the perception&endash;action model of empathy [14,15]. Empirical support for a connection between empathy and CY was first published by Platek et al. [6], and this continues to be a prevailing view in the current literature [16]. However, systematic reviews of the studies examining the linkage between CY and empathy have shown that the totality of evidence is rather mixed and inconsistent [17]. Alternatively, CY could instead represent a simple feature of behavioral contagion or facial mimicry [18,19] that would show a statistical correlation to markers of empathy or emotional contagion without a causal relation. For example, one key issue in this debate is that at a proximate level CY requires the detection of yawns in others, and social attention and empathy are often difficult to disentangle [20,21]. Thus, while the use of CY as a potential indicator of empathy or emotional contagion is intriguing, a direct linkage remains unclear.
 
Recently, interspecific CY, whereby yawns from one species trigger a member of a different species to yawn, has been examined in relation to empathy. The first evidence for interspecific CY came 15 years ago from a study showing that the overt display of human yawning was sufficient to induce a similar response among domesticated dogs [22]. This initial report garnered considerable attention and led to numerous follow-up studies designed to explore the interspecific CY/empathy connection. If this cross-species facial mimicry was enhanced by empathy, it had been predicted that dogs should respond more strongly to yawns from caregivers/owners where there was an existing social bond or attachment. This view was based largely on a 2011 study of chimpanzees, whereby an ingroup bias for CY was observed and interpreted as a sign of empathy [23]. The authors of this work suggested that since humans show ingroup biases for empathy for pain [24&endash;26], similar biases in CY could be used as a measure of affective empathy. Overall, the evidence in support of this effect among dogs is mixed [27&endash;29], and a recent study, including a meta-analysis of this literature, concluded that human-initiated CY in dogs was, in fact, not a signal of empathy [30].
 
Studies on other captive species, however, have reported more consistent familiar- ity/ingroup biases when it comes to interspecific CY. In line with the view that CY may reflect a form of empathy or emotional contagion, familiarity has been shown to enhance both intra- and interspecific CY among nonhuman primates [23,31,32]. In one study on chimpanzees, subjects responded with CY to stimuli from familiar humans (i.e., researchers and husbandry staff) and ingroup conspecifics but not to outgroup chimps or unfamil- iar members from other species [31]. A more recent and very similar study on captive red-capped mangabeys produced the same basic findings: subjects showed a higher CY response to familiar human caretakers and conspecifics compared to unfamiliar individuals from across three species [32]. In addition, one study on African elephants found that individuals responded with CY to yawns from familiar human handlers [33], though no comparisons were made with unfamiliar humans.
 
To further examine this relationship, Gallup and Wozny [5] investigated whether humans also display interspecific CY. Using an online format, participants were shown a series of yawning stimuli from one of the following categories: fish, amphibians, reptiles, birds, non-primate mammals, great apes, and a compilation of common household pets (including an equal representation of domesticated cats and dogs). Given that prior studies have shown that people display greater empathy and attachment towards both more closely related species [34&endash;36] and domesticated animals that are commonly kept as pets [37&endash;39], it was predicted that interspecific CY would be enhanced by phylogenetic proximity and domestication/social closeness. The findings provided clear evidence for interspecific CY when compared to the control images, with 69% of participants reporting interspecific CY. Yet, while it was expected that yawns from great apes (chimpanzees, gorillas, and orangutans) and common pets (cats and dogs) would elicit the greatest response, this was not the case. Consequently, these findings did not support the purported connection between interspecific CY and empathy or emotional contagion in humans and instead suggest that the mechanisms governing CY are generalized. Importantly, Gallup and Wozny [5] included a task that ensured attention towards the yawning stimuli during testing. Given CY is a reflexive and automatic response, it seems that the detection of yawns, independent of the taxa represented, may be sufficient to generate this response. However, like previous works, overt measures of empathy or attitudes towards animals were not obtained in this experiment. In addition, subsequent exploratory analyses from this open-access dataset indicated that women may be more likely to yawn in response to yawns from a compilation of CY stimuli from domesticated cats and dogs. While sex differences in CY are rarely observed (for a review, see [40]), and an overall effect of gender was not found. In general, it has been argued that a female bias in CY would be consistent with links to empathy and/or emotional contagion [41]. Thus, future research could help clarify this picture by assessing whether this interaction is reproducible.
 
The current study served as a direct follow-up to Gallup and Wozny [5], providing a more explicit examination of the relationship between interspecific CY and empathy in humans. We sought to examine whether validated measures of empathic concern and animal attitudes predicted interspecific CY to common household pets while controlling for attention. Empathic concern was selected because it has previously been shown to correlate with animal attitudes [42,43] and intraspecific CY in humans [44], while measures of cognitive empathy (i.e., reading emotions and perspective-taking) tend to be less correlated with animal attitudes and have more often failed to predict CY in humans [45&endash;47]. Given that dogs have undergone a long period of domestication that involved distinct forms of social communication and cooperation with humans [48] and that people tend to perceive both human and dog facial expressions in a similar manner [49], we examined interspecific CY separately to domesticated cats and dogs. Moreover, based on exploratory analyses showing a potential female bias in interspecific CY to common household pets, we aimed to replicate this effect of participant gender. If empathy was related to interspecific CY, empathic concern should positively predict this behavior, and perhaps women would show a greater response [41]. If interspecific CY is generalized, due to it being more of an automatic and reflexive response, merely attending to the animal stimuli should elicit yawns independent of empathic concern or gender.
 
Discussion
The current findings provide further evidence of interspecific CY in humans, repli- cating previous research [5]. While the magnitude of this effect was relatively limited for yawning images of domesticated dogs, showing up only when examining CY frequency, there was a larger and significant effect observed within the cat yawning condition across both the binary and frequency models. This difference in interspecific CY when viewing images of cat and dog yawns was not expected given the coevolution of human&endash;dog bonding and social communication [48,49,61]. Nonetheless, these results, coupled with the report of Gallup and Wozny [5], provide strong support that, in general, yawns from common household pets can reliably elicit CY among humans.
 
A primary objective of the current study, outside of replicating interspecific CY in humans, was to more explicitly assess how this response varied as a function of individual differences in a self-reported measure of affective empathy. To date, prior studies in this area have only used proxies for empathy, focusing on features pertaining to the familiarity (e.g., human handlers/caregivers) or phylogenetic closeness of the interspecific stimuli. Here, we had participants complete the empathic concern subscale of the IRI [54] as well as the five-item version of the Animal Attitude Scale (AAS-5) [55] to assess how this predicted interspecific CY. Although the reliability of the AAS-5 was poor, the internal consistency of the empathic concern scale was acceptable and included in the analysis. Moreover, this measure of affective empathy towards humans has previously been shown to predict attitudes towards animals [42,43]. Despite people generally showing high levels of empathy towards domesticated cats and dogs [37&endash;39], this measure was not a positive predictor of interspecific CY. In fact, participants with greater empathic concern were less likely to yawn during testing, casting doubt on the view that interspecific CY is strongly linked to features of empathy or emotional contagion [16,23,31,32]. Together, these results add to a growing number of psychological studies providing mixed support for a connection between CY and empathy when using self-reported trait measures (reviewed by [17]).
 
Based on exploratory analyses of the dataset from Gallup and Wozny [5], a secondary objective of the current study was to further examine the role of gender in interspecific CY among humans. Consistent with most studies in the literature, the current results revealed no overall gender bias in interspecific CY. However, a significant gender _ stimulus condition interaction emerged whereby women reported a higher frequency of CY to dog yawns, and men reported a higher frequency of CY to cat yawns. Given that this particular result was not anticipated, we can only speculate as to the mechanisms governing this effect. Prior work has shown, for example, that interactions with pet dogs tend to enhance oxytocin (OT) among female owners, while they lead to no change or decreases in OT among men [62,63]. Moreover, in contrast to human interfaces with dogs, a recent study including only women found no overall increase in OT following interactions with pet cats [64]. Thus, one potential explanation for the female bias in CY to dog stimuli could be differences in OT among participants. However, we are skeptical of this possibility for at least two reasons. First, while OT has been implicated in CY [65,66], studies that have manipulated OT via intranasal administration have failed to yield support for this connection [57,67]. Second, the studies measuring changes in human OT levels were undertaken following real-world interactions with bonded cats and dogs (i.e., pets and their owners), and it seems unlikely that the current procedures of merely viewing static images of unknown animals would elicit similar neurochemical changes. Nevertheless, this represents a potentially fruitful area for future research to explore.
 
Consistent with similar online studies examining both intra- and interspecific CY in humans [5,7], indices of arousal/fatigue were the strongest predictors of self-reported yawning in the current sample. As expected, sleep duration the night before was nega- tively correlated with interspecific CY, while tiredness during the study was positively correlated with this response. These findings align with a large body of comparative evi- dence suggesting that circadian rhythms and internal temperature drive yawning behavior (reviewed by [9]).
 
While the current research serves as a replication of interspecific CY in humans and furthers our understanding of the factors contributing to this response, this study has several limitations. First, no measure of pet ownership was captured from the participants. Prior studies suggest that just over half of US households have a pet, with the majority reporting dog and/or cat ownership [68], and thus further work could assess how living and bonding with a pet cat or dog contributes to interspecific CY in these conditions. Another limitation to this study was the relatively small sample of participants, which was reduced primarily due to attentional checks. However, the attentional measures obtained during testing remains a strength of this study, as they ensured (1) high quality data and (2) that visual attention was directed towards the yawning stimuli. That said, the manipulation was not robust, particularly for the binomial outcome. Though common in the literature, the use of one-time measures of yawning to assess the relationship to psychological traits could be considered a further limitation. While we included a self- report measure of affective empathy, we did assess the ability to engage in empathy. Follow- up studies in this area could explore this further while also examining the relationship between interspecific CY and cognitive measures of empathy (i.e., emotion reading and perspective-taking). In addition, further work in this area could attempt to improve the ecological validity of this online experiment, perhaps including live demonstrations of yawning in the laboratory or the use of dynamic (i.e., video) yawn stimuli to enhance the participant response. While self-report CY has proven to be a valid measure of this behavior in psychology [3,56,57], future studies could attempt to capture a combination of both self-report and objective measures of CY.
 
Conclusions
In summary, this study replicates recent findings providing evidence for interspecific CY in humans. By comparing separate conditions for common household pets, we were able to show a slightly greater CY response to yawns of domesticated cats compared to domesticated dogs. Furthermore, when explicitly examining how individual differences in empathic concern and gender influence this response, our findings do not support a strong connection between interspecific CY and empathy or emotional contagion.