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Yawning: its cycle, its role
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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
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mise à jour du
21 juin 2013
Anim Cogn. 2013
 Contagious yawning, social cognition, and arousal:
an investigation of the processes underlying
shelter dogs' responses to human yawns
Buttner AP, Strasser R.
 
 
Department of Psychology, University of Nebraska. Omaha, USA
 

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Tous les articles sur la contagion du bâillement
All articles about contagious yawning
 
Abstract
 
Studies of contagious yawning have reported inconsistent findings regarding whether dogs exhibit this behavior and whether it is mediated by social-cognitive processes or the result of physiological arousal. We investigated why some dogs yawn in response to human yawns; particularly, whether these dogs are exceptional in their ability to understand human social cues or whether they were more physiologically aroused. Sixty shelter dogs were exposed to yawning and nonyawning control stimuli demonstrated by an unfamiliar human. We took salivary cortisol samples before and after testing to determine the role of arousal in yawn contagion. Dogs were tested on the object-choice task to assess their sensitivity for interpreting human social cues. We found that 12 dogs yawned only in response to human yawns (i.e., appeared to exhibit yawn contagion), though contagious yawning at the population level was not observed. Dogs that exhibited yawn contagion did not perform better on the object-choice task than other dogs, but their cortisol levels remained elevated after exposure to human yawning, whereas other dogs had reduced cortisol levels following yawning stimuli relative to their baseline levels. We interpret these findings as showing that human yawning, when presented in a stressful context, can further influence arousal in dogs, which then causes some to yawn. Although the precise social-cognitive mechanisms that underlie contagious yawning in dogs are still unclear, yawning between humans and dogs may involve some communicative function that is modulated by context and arousal.
 
Introduction
 
Over the last decade, there has been renewed interest in understanding the mechanisms that control contagious yawning (i.e., yawning in response to perceiving another individual yawn). It has been suggested that yawning functions to increase arousal in situations in which environmental stimulation is low and wakefulness and vigilance are important (Baenninger 1997). This behavior may have evolved a communicative mechanism when exhibited within group contexts, serving to synchronize group activities by communicating sleepiness or stress (Deputte 1994; Guggisberg et al. 2010). Although it has been argued that contagious yawning is nothing more than a behavioral fixed action pattern (Provine 1986), more recent studies have indicated that a social-cognitive mechanism (i.e., empathy) is involved in contagious yawning. Humans who score higher on empathy scales (Arnott et al. 2009) and faux pas theory of mind and self-recognition tasks (Platek et al. 2003) have been reported to be more susceptible to yawn contagion than individuals who score low in those abilities. Consistent with other empathic behaviors, Norscia and Palagi (2011) found contagious yawning was more likely to be elicited in response to the yawning of more familiar individuals rather than less familiar individuals. Researchers have shown particular interest in how the emergence of contagious yawning across development and phylogeny can inform us of the underlying mechanisms of this behavior. Contagious yawning emerges in children around the same time as more complex forms of empathy (i.e., 5&endash;6 years of age, Anderson and Meno 2003; Millen and Anderson 2011) and is disrupted in children with autism (Giganti and Esposito Ziello 2009; Senju et al. 2007), unless instructed to fixate on the eyes of the yawner (Senju et al. 2009). Studies with nonhuman primates further support a possible association between contagious yawning and empathy. Chimpanzees (Pan troglodytes) have been shown to yawn in response to viewing an ingroup member yawn as opposed to an outgroup member (Campbell and de Waal 2011), bonobos (Pan paniscus) exhibit yawn contagion particularly in response to socially close individuals (Demuru and Palagi 2012), and gelada baboons (Theropithecus gelada) exhibit yawn contagion at higher levels when individuals are socially close (Palagi et al. 2009). However, yawning in response to a conspecific's yawn in stumptail macaques (Macaca arctoides) may be a function of stress as opposed to empathy, as researchers observed elevated levels of self-directed scratching during yawning but not control stimuli (Paukner and Anderson 2006).
 
Although it was originally proposed that complex cognitive abilities (i.e., theory of mind and self-awareness) are required for the emergence of contagious yawning (Platek et al. 2003), evidence of contagious yawning in animals that do not demonstrate these advanced abilities (e.g., domestic dogs, Canis familiaris) contradicts this stance. While there are no data to suggest that dogs possess 'theory of mind,' dogs are outstanding in their ability to interpret human social cues. For example, when given the choice of two containers, one of which is hiding a piece of food, dogs choose the correct container at above chance levels after viewing a human point or gaze at the container (see review by Reid 2009), outperforming chimpanzees at this 'objectchoice' task (Hare et al. 2002). It is possible that through domestication and coevolution with humans (Hare et al. 2010), socialization with humans during a critical period (Udell et al. 2010), or, more likely, this gene&endash;environment interaction (Miklo´si and Topa´l 2011), dogs have developed ways of communicating and coordinating their behaviors with humans. One means by which they synchronize their interactions may be through contagious yawning. However, studies of yawn contagion in dogs up to this point have reported variable findings. Although some have found high levels of contagious yawning in dogs at the individual level (72 % in Joly-Mascheroni et al. 2008; 69 % in Madsen and Persson 2012), others have reported much lower proportions (6 % in Harr et al. 2009; 26 % in O'Hara and Reeve 2011; 28 % in Silva et al. 2012), possibly stemming from the considerably different methodologies employed by each study.
 
Joly-Mascheroni et al. (2008) suggested two possible underlying mechanisms for contagious yawning in dogs. First, dogs may yawn as a means of coordinating their behavior with humans' behavior, which may involve an empathic component. Several studies now have tested the social modulation of contagious yawning in dogs (i.e., whether it is biased toward more familiar individuals, as with other empathic behaviors). Although Silva et al. (2012) found that dogs yawned more in response to just the sound of their owner's yawn than an unfamiliar individual's, studies with live models have shown no such relationship (Madsen and Persson 2012; O'Hara and Reeve 2011). In fact, O'Hara and Reeve found that contactdeprived shelter dogs yawned more than human-bonded owned dogs, particularly in response to an unfamiliar human, supporting Yoon and Tennie's (2010) nonconscious mimicry hypothesis that contagious yawning may serve as a means of affiliating with an unknown human and does not require a 'theory of mind.' Given the discrepancies in the findings of previous studies that have tested the social modulation of contagious yawning, it may be necessary to use measures that do not rely on the relationship between the dog and human to assess the social-cognitive mechanisms that underlie this behavior.
 
Alternatively, Joly-Mascheroni et al. (2008) suggested that contagious yawning in dogs could be mediated by stress. Mildly stressful situations may elicit 'tension' yawns in animals (Maestripieri et al. 1992), particularly dogs (Beerda et al. 1998). Although tension yawns resemble 'sleepy' yawns, they often occur with other stress behaviors such as panting, trembling, body shaking, lip licking, or whimpering (Madsen and Persson 2012). Thus, situations that increase arousal (e.g., the sound of an owner's yawn in their absence as in Silva et al. 2012; see Madsen and Persson 2012 for critique) may elicit tension yawns that are mistaken for contagious yawns. When a live model is used, the human yawn itself may be responsible for this increased arousal, which triggers tension yawns. Joly-Mascheroni and colleagues proposed that human yawning may be perceived as a threat behavior to dogs, thereby causing them to yawn as a means of alleviating tension, much like what was observed by Paukner and Anderson (2006) in stumptail macaques. Although yawning is frequently observed during agonistic interactions between numerous primate species (see Baenninger 1997), there is no scientific evidence that we are aware of to suggest that human yawning is perceived as a threat to dogs. Rather, arousal may play an important role in modulating the meaning of a yawn, and when displayed in 'situations of uncertainty' (Madsen and Persson 2012), human yawning may communicate stress as opposed to sleepiness to dogs, which leads to an increase in arousal and subsequent yawning by the dog. This may also explain O'Hara and Reeve's finding that contagious yawning was most common in shelter dogs with unfamiliar humans, since shelter dogs were more physiological aroused (measured via heart rate) than owned dogs throughout testing.
 
Many of the inconsistencies in the number of dogs that exhibit yawn contagion presented in previous studies may be due to the fact that different methodologies produce varying levels of arousal in dogs (Madsen and Persson 2012). Most studies attempt to control for tension yawns through methodological procedures (e.g., testing in a familiar environment) and excluding yawns that occur in the presence of other stress behaviors. Although some have presented convincing evidence for contagious yawning in dogs by taking these measures (e.g., Madsen and Persson 2012), it is still unclear how these methodologies influence arousal (O'Hara and Reeve 2011; Silva et al. 2012). Because there is great individual variation in dogs' behavioral coping strategies in response to stressors (Beerda et al. 1998), physiological measures are needed to determine the role arousal is playing in contagious yawning in dogs. Many have recognized the need for physiological measures when assessing contagious yawning in dogs (Joly-Mascheroni et al. 2008; Madsen and Persson 2012), but only one study up to this point has used a physiological measure to quantify stress responses in their subjects (i.e., heart rate: O'Hara and Reeve 2011), and the impact that testing had on individual dogs' physiological responses and subsequent yawning was unclear.
 
The purpose of the present study was to test the two explanations put forth by Joly-Mascheroni et al. (2008) in order to determine why some dogs exhibit yawn contagion in response to human yawns while others do not. We examined the role of arousal in contagious yawning using a physiological measure that has not yet been used in yawn contagion studies. Specifically, we assessed whether dogs that exhibited yawn contagion had elevated levels of arousal via salivary cortisol measures. We also included a measure to assess whether social-cognitive processes play a role in contagious yawning in dogs as in some primates (Platek et al. 2003; Campbell and de Waal 2011). We propose that if yawning serves as a means of coordinating interactions between dogs and humans, perhaps dogs that exhibit yawn contagion are also more perceptive to human social cues in general. Based on previous studies that have shown that social-cognitive performance (i.e., faux pas theory of mind and self-face recognition tasks) correlates with contagious yawning in humans (Platek et al. 2003), we expected that dogs that exhibited yawn contagion would also perform better on a social-cognitive task. We chose to test these two mechanisms using shelter dogs in order to elaborate on O'Hara and Reeve (2011) study in which they unexpectedly found that shelter dogs exhibited yawn contagion at much higher levels than owned dogs.
 
yawning contagiosiness by dogs
 
Discussion
 
This study is the first to present evidence to suggest that human yawning, when presented in a stressful context, influences physiological arousal and yawning in some dogs. Although we did not observe contagious yawning among shelter dogs overall, we identified 12 dogs that yawned only in the yawning condition (henceforth referred to as dogs that appeared to exhibit yawn contagion). This subgroup of dogs was distinct from the other dogs in this study in their levels of physiological arousal following exposure to human yawns. Specifically, their cortisol levels remained elevated following exposure to human yawning, whereas other dogs had reduced levels relative to their baseline levels. We must caution that we did not observe notable differences between the number of dogs that yawned only in the yawning condition versus the control condition and that it is possible that some dogs may have fallen into this category by chance. However, if a significant number of these dogs were in this subgroup by chance, it is unlikely that we would have observed these different cortisol patterns. Further, this effect did not appear to be the result of some dogs being more inherently nervous, causing them to yawn more, because there was no relationship between baseline cortisol levels and yawning rates.
 
In addition to different cortisol patterns, 83 % of dogs that yawned contagiously had received the yawning stimuli rather than control stimuli first. Previous studies would support that levels of arousal were probably elevated in the first trial regardless of condition as a result of the novelty of the situation (Tuber et al. 1996; Hennessy et al. 1998). One possibility is that when yawning is presented in the first trial, when arousal is high, these dogs are more likely to yawn and their cortisol levels remain elevated, but when yawning stimuli are presented later on, after dogs have acclimated and arousal is lower, they are less likely to yawn. It is also possible that dogs that received control stimuli first habituated to mouth movements, which decreased their responsiveness in the second trial when yawning stimuli were presented and therefore showed lower levels of yawning. However, since our findings suggest that elevated arousal may facilitate yawning, and yawning has been directly associated with glucocorticoids in previous studies (Anő´as-Caldero´n et al. 2004), we tend to agree with the first interpretation.
 
These findings suggest that context and arousal could both play a role in modulating the meaning of a yawn. Previous studies have shown that shelter dogs have elevated cortisol levels relative to pet dogs in their homes, especially during the first few days in the shelter (Hennessy et al. 1997). We suggest that when a yawn is presented in situations of uncertainty, when arousal is high (e.g., in a shelter environment), it may be nonconsciously perceived as a signal for stress, but when presented in a comfortable situation, when arousal is low (e.g., in a home environment), it may be nonconsciously perceived as a signal for sleepiness. The perception of the yawn then influences the arousal state of the perceiver (i.e., the dog) and the type of yawn that is exhibited (tension yawn or true contagious yawn). However, the direction of the relationship between arousal and a yawning response is unclear. It has been suggested that in true, 'sleepy' contagious yawning, the yawning response serves as a low-level form of mimicry (Yoon and Tennie 2010) that is then internalized and produces a reduction in arousal (Madsen and Persson 2012; Fig. 4a). This suggestion has been supported by anecdotal evidence of diminished arousal in dogs following yawning, but not control stimuli presented in a naturalistic, comfortable setting (Madsen and Persson 2012). It is possible that the yawns we observed in this study follow this process (i.e., dogs mimic the yawn of the actor, and given the heightened arousal of the dog and the uncertain context, dogs show an increase in arousal). Like true contagious yawning, this would also serve to synchronize their behavior with humans' (Joly-Mascheroni et al. 2008). However, since nearly an equal number of dogs yawned only in the control condition as in the yawning condition, our data do not suggest that dogs were mimicking the human's behavior. On the other hand, it may be more plausible that a human yawn could trigger a physiological response (i.e., elevated arousal), which then elicits tension yawns. Rather than functioning to coordinate behaviors, these yawns would serve to displace internal anxiety arising from a tense social situation (Maestripieri et al. 1992; Fig. 4b). Whether this is in fact the case could be determined in future studies by blocking physiological arousal and observing whether dogs in high stress contexts continue to yawn.
 
Even though the evoked yawns that occur in high arousal situations, like those observed in this study, may differ from true contagious yawns, they could potentially still involve a social-cognitive mechanism. Human yawning influenced dogs' levels of arousal, which suggests that the perception of a human yawn contains a communicative component, perhaps conveying their emotional state. This may also be related to dogs' ability to empathize with humans. However, recent studies have reported variable findings as to whether contagious yawning in dogs is biased toward familiar individuals (Madsen and Persson 2012; O'Hara and Reeve 2011; Silva et al. 2012). Unlike primates, which have demonstrated social modulation of contagious yawning (e.g., bonobos: Demuru and Palagi 2012; chimpanzees: Campbell and de Waal 2011, but see Massen et al. 2012; humans: Norscia and Palagi 2011; gelada baboons: Palagi et al. 2009), dogs may not, possibly because of their frequent positive interactions with unfamiliar humans (Campbell and de Waal 2011), or perhaps the emotional bond between human and dog is only unidirectional (O'Hara and Reeve 2011). Before concluding that this lack of social modulation suggests that contagious yawning operates on a low-level form of nonconscious mimicry or affective empathy (Madsen and Persson 2012), we should generate alternative means of assessing the underlying social-cognitive mechanisms of contagious yawning.
 
Rather than exploring a familiarity bias to determine the role of social cognition in yawn contagion, we explored whether dogs that exhibited yawn contagion were exceptional in their social-cognitive abilities, similar to the premise of Platek et al. (2003) study with humans. The objectchoice task involves a basic level of perspective-taking (Emery and Clayton 2009), which is an important skill for coordinating group behavior. The object-choice task was chosen to assess the social-cognitive skills of the dogs in this study because it encompasses the basic components of more complex abilities that have been suggested to be involved in yawn contagion (Platek et al. 2003). However, we found that dogs that exhibited yawn contagion in this study performed similarly on the object-choice task to dogs that did not yawn uniquely at the yawning stimuli. There are several ways to interpret our finding that social-cognitive performance was not different among dogs that did and did not yawn contagiously. First, this may suggest that yawn contagion may not require the high level of cognitive complexity (i.e., theory of mind) that had been proposed by Platek et al. (2003). This would support Madsen and Persson's (2012) suggestion that lower-level affective empathy underlies contagious yawning in dogs rather than more complex cognitive empathy. However, we also must acknowledge that the seemingly 'contagious' yawns we observed in this study may operate on some different mechanism than the contagious yawns observed in other studies (e.g., Madsen and Persson 2012), given our subjects' heightened arousal compared to owned dogs (Hennessy et al. 1997). This could also explain why dogs that exhibited yawn contagion performed the same as other dogs on the object-choice task. Further, dogs that yawned in response to human yawns had elevated levels of physiological arousal, and heightened arousal was associated with poorer performance on the object-choice task. Thus, our measure of social-cognitive abilities may have been confounded by high levels of arousal. It may be necessary to test owned dogs in their homes under more comfortable conditions (as in Madsen and Persson 2012) in order to determine whether dogs that exhibit yawn contagion in comfortable settings are in fact more perceptive to human social cues. If we still fail to observe an association between performance on the object-choice task and yawn contagion when tested in a comfortable setting, this would not necessarily imply that social cognition does not underlie contagious yawning in dogs. Rather, it may indicate that this type of social-cognitive task is assessing a process unrelated to contagious yawning. Still, researchers should strive to develop other ways of testing the relationship between yawn contagion and social cognition (including empathy) aside from familiarity biases.
 
Though some studies have provided convincing evidence that dogs engage in yawn contagion with humans (e.g., Joly-Mascheroni et al. 2008; Madsen and Persson 2012), other studies have found only a small percentage of dogs exhibits this behavior (Harr et al. 2009; O'Hara and Reeve 2011). The discrepancies between these studies may be the result of the fact that yawn contagion in dogs, though present, is influenced by contextual factors more so than in other species (i.e., primates, Demuru and Palagi 2012). Our findings indicate that in a stressful context, dogs that yawn in response to human yawns remained aroused following exposure to stimuli. Though these yawns appear contagious, they may be based on different underlying mechanisms than what would be observed in a low-stress situation. It is possible that the methods utilized in this and other studies (e.g., requiring eye contact, long periods of silence with little if any petting, testing in an unfamiliar setting) may have influenced arousal levels and therefore could contribute to the variable findings between studies. This emphasizes the importance of assessing arousal in such studies. Potential stressors (e.g., unfamiliar humans, novel environment), including stimuli that may trigger physiological arousal that may not typically be considered a 'stressor' (e.g., food, exercise, eye contact), should be considered in their contribution to dogs' state of arousal.
 
Further, as there is no standardized behavioral measure of stress in dogs given the individual variation in behavioral manifestations of stress (Rooney et al. 2007), physiological measures can provide valuable information regarding the role of physiological arousal in contagious yawning. In fact, physiological measures may be necessary in situations in which it is not clear whether the contagious yawning being observed is the result of arousal and tension yawns.
 
Conclusions
 
Our findings are consistent with several previous studies that reported low levels of contagious yawning in dogs. However, these results may be explained by the arousal states of our subjects. Dogs that exhibited yawn contagion remained physiologically aroused following observing human yawns, and most of them had received the yawning stimuli first. These findings may suggest that arousal levels and context have a substantial effect on the perception of a human yawn by dogs. When presented in conjunction with other environmental stressors, human yawning may be perceived as a signal for stress, leading to increased arousal levels, which then elicit tension yawns. Although these yawns resemble true contagious yawning, they probably operate on some other mechanism. Investigating the socialcognitive mechanisms that underlie this phenomenon can reveal whether this type of yawning is functionally distinct from contagious yawning observed in other studies when arousal is low. Although we did not find that the type of contagious yawning we observed in this study was linked to dogs' social-cognitive abilities, it is important to explore alternative means of assessing social cognition and empathy when attempting to understand the processes that give rise to contagious yawning in dogs.