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

 

 

 

 

 

 

 

 

 

 

 

 

  

 

 

 

 

 

 

mise à jour du
1 septmebre 2014
Animal Cognition
2014
Smell facilitates auditory contagious yawning
in stranger rats
Moyaho A, Rivas-Zamudio X, Ugarte A, Eguibar JR, Valencia J.
Instituto de Fisiología, Benemérita Universidad Autónoma de Puebla, Apdo. Mexico
 
Tous les travaux de MR Melis & A Argiolas 
Tous les travaux de JR Eguibar & G Holmgren

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Most vertebrates yawn in situations ranging from relaxation to tension, but only humans and other primate species that show mental state attribution skills have been convincingly shown to display yawn contagion. Whether complex forms of empathy are necessary for yawn contagion to occur is still unclear. As empathy is a phylogenetically continuous trait, simple forms of empathy, such as emotional contagion, might be sufficient for non-primate species to show contagious yawning. In this study, we exposed pairs of male rats, which were selected for high yawning, with each other through a perforated wall and found that olfactory cues stimulated yawning, whereas visual cues inhibited it. Unexpectedly, cage-mate rats failed to show yawn contagion, although they did show correlated emotional reactivity. In contrast, stranger rats showed auditory contagious yawning and greater rates of smell-facilitated auditory contagious yawning, although they did not show correlated emotional reactivity. Strikingly, they did not show contagious yawning to rats from a low-yawning strain. These findings indicate that contagious yawning may be a widespread trait amongst vertebrates and that mechanisms other than empathy may be involved. We suggest that a communicatory function of yawning may be the mechanism responsible for yawn contagion in rats, as contagiousness was strain-specific and increased with olfactory cues, which are involved in mutual recognition.
-Moyaho A et al Induced grooming transitions and open field behaviour differ in high- and low-yawning sublines of Sprague-Dawley rats Animal Behavior 1995;50:61-72
-Moyaho A, Valencia J Grooming and yawning trace adjustment to unfamiliar environments in laboratory Sprague-Dawley rats J Comparative Psychology 2002;116;(3):263-269
-Moyaho A et al. Genetic and littermate influences on yawning in two selectively bred strains of rats Dev Psychobiol. 2009;51(3):243-248
 
General introduction
 
Yawning is a readily observable behaviour that has been described in many vertebrate species, including fish (Baenninger 1987), rats (Anias et al. 1984), birds (Delius 1967) and primates (Baenninger 1987). Many of these species, especially mammals, may yawn concurrently with stretching and spontaneous penile erections (Holmgren et al. 1985), and some of them show yawn contagion (Provine 1986; Anderson et al. 2004). Despite having this taxonomic information about yawning and the increasing number of studies addressing its immediate mechanisms (Collins and Eguibar 2010), the literature still ignores other important aspects, such as its biological meaning (Guggisberg et al. 2010) and whether a wider range of species are capable of showing yawn contagion. Animals typically yawn in situations that vary from calm (Provine et al. 1987) to mild stress (Voigt and von Helversen 1999; Voigt-Heucke et al. 2010) to conflict or tension (Deputte 1994). Such a broad range of situations suggests, according to the dimensional view of emotion (Mendl et al. 2010), that yawning manifests itself in the punishment avoidance system, from low-arousal positive pleasant states to high-arousal negative unpleasant states. This association of yawning with apparently contrasting emotional states might explain the diversity of hypotheses about its function (Smith 1999; Gallup and Gallup 2008; Guggisberg et al. 2010). Overall, one can distinguish two classes of hypotheses. One class considers yawning as a physiological response associated with the recovery of homeostasis (for a review see Guggisberg et al. 2010). For example, yawning may enhance physiological arousal (Greco et al. 1993) or assist thermoregulation (Gallup and Gallup 2008). The second class, which has arisen from studies with primates, suggests that yawning is a communicative act (Deputte 1994). Accordingly, yawning can be a displacement behaviour (Delius 1967), a threat display (Redican 1982) or a way of synchronising a group's behaviour (Sauer and Sauer 1967). Although there are some correlative studies that have provided evidence for some of these hypotheses, none of them have been conclusively supported.
 
Contagious yawning&emdash;an increase in the probability of yawning by a subject perceiving another subject yawning&emdash; is a rare trait shown by the few primate species that presumably exhibit cognitive empathy (Provine 1986; Anderson et al. 2004). However, according to the perception&endash; action model (Preston and de Waal 2002), empathy, which refers to an individual's sensitivity to the emotional state of others (Preston and de Waal 2002), is a phylogenetically continuous phenomenon, and therefore, even small mammals should show some form of it. In fact, cagemate mice (Mus musculus) showed emotional contagion&emdash; the tendency to automatically mimic and synchronise expressions, vocalizations, postures and movements with those of another subject's and, consequently, to converge emotionally&emdash;by intensifying their response to pain when perceiving other mice in pain (Langford et al. 2006). Additionally, rats (Rattus norvegicus) showed empathic concern by liberating a cage mate trapped in a restrainer (Ben-Ami Bartal et al. 2011), although the interpretation of this finding has recently been challenged (Silberberg et al. 2014). Therefore, it is not surprising that other species such as dogs (Canis familiaris) and budgerigars (Melopsittacus undulatus) may also show yawn contagion (Joly-Mascheroni et al. 2008; Miller et al. 2012), although the evidence is still controversial (Harr et al. 2009; O'Hara and Reeve 2011).
 
Yawn contagion has generally been elicited through the use of visual cues. For example, human subjects (Homo sapiens) yawn when they watch other subjects yawning on a TV screen (Provine 1986) and chimpanzees (Pan troglodytes) yawn when they watch animated chimpanzee yawns (Campbell et al. 2009). Nonetheless, other sensory cues, such as sounds, may make human individuals feel an urge to yawn (Arnott et al. 2009), and because animal species vary in their ecology, yawn contagion may use species-specific senses. The present paper will examine three aspects of yawn contagion using male rats that were obtained from two populations of rats that were selected for high yawning (HY) and low yawning (LY) (Urba´-Holmgren et al. 1990). First, we expose dyads of HY rats to different sensory cues to determine whether they have a differential effect on yawn contagion susceptibility. Second, we further analyse which sensory cues are involved in yawn contagion. Finally, we assess whether the high-yawning rats contagiously yawn to the low-yawning strain, taking advantage of their genetic difference in yawning rates.
 
General discussion
 
This study provides evidence for yawn contagion in rats and suggests that it most likely arises from a mechanism other than empathy. Yawn contagion in HY rats may not be the result of synchronised activity, as has been claimed to happen, for instance, in lions (McKenzie 1994). Circadian rhythms, such as feeding and the sleep/wake cycle that are associated with yawning (Holmgren et al. 1991), remained unaltered throughout the test situations. Stress-related yawning did not account for yawn contagion because the results persisted after we statistically controlled for variation in defecation rates in the rats. Therefore, we can confidently conclude that rats did indeed demonstrate yawn contagion.
 
The stimulating role of olfaction on auditory contagious yawning reflects the importance of olfactory cues in social interactions in most mammals (Johnston 2003). The variety of chemicals that are released with bodily secretions and urine during such interactions provides information about individual identity, sex and strain (Brennan and Zufall 2006), and rats use this information to distinguish between group members (Bradbury and Vehrencamp 1998). In contrast, visual contact seems not to convey such information, perhaps owing to the impairment of albino rats from seeing as pigmented rats normally do (Prusky et al. 2002). This impairment may explain the slight effect of visual cues on the yawning of the rats in this study, which contrasts with the function in primates, in which they undoubtedly play a stimulating role (Provine 1986; Platek et al. 2003; Anderson et al. 2004). Alternatively, an evolutionary divergence in the type of sensory modalities used in social interactions may explain the opposite effect of visual cues on yawning between primates and rodents (Bradbury and Vehrencamp 2011). Both groups of species share, however, the use of auditory cues in contagious yawning, which suggests that this sensory modality may have been involved in contagious yawning earlier than vision.
 
The finding that stranger NVOC and OC rats, rather than cage-mate rats, showed yawn contagion contrasts with the prediction that empathic processes are more likely to occur in familiar animals (Preston and de Waal 2002; Langford et al. 2006). Therefore, mechanisms other than empathy are most likely involved in contagious yawning in rats. Imitation cannot be suggested as a valid process of yawn spreading because yawning cannot be considered as a novel or improbable response in the repertoire of the rats, which is a necessary condition for imitative behaviour (Byrne 1994; Zentall 2011). Our results suggest the existence of a social interaction effect that is more specific than an indiscriminate influence on yawning. A social facilitation mechanism, such as contagious behaviour (Byrne 1994), may suffice for contagiousness to occur. In such a case, yawning would be released if the releasing stimulus (e.g. the sound of a yawn) happened to be another rat behaving in the same manner (Yoon and Tennie 2010). However, this mechanism ought to produce yawn contagion in both cage-mate and stranger HY rats. Because stranger NVOC- and OC-HY rats yawned at each other, contagion seems to have simply occurred as a consequence of using yawning as a form of communication. This mechanism does not rely on empathy based on the fact that only stranger NVOC- and OC-HY rats showed contagious yawning.
 
Why did cage-mate and stranger HY rats differ in their ability to show yawn communication? The difference may be because of the way in which they coped with the test situations. Individual recognition based on familiarity made cage-mate OC-HY rats, although not NVOC-HY rats, empathise emotionally (Hatfield et al. 1993) because their defecation rates positively correlated. Nonetheless, the yawn they showed was unlikely to influence each other's behaviour; it possibly served for monitoring their internal state. In contrast, individual recognition based on familiarity failed in stranger NVOC- and OC-HY rats. The encounter between them could lead to a conflict situation because they were placed next to each other in a limited area in which they very likely simultaneously attempted to gain control (Hurst and Beynon 2004; Bradbury and Vehrencamp 2011). The conflict most likely led the rats to gather information about the opponents' fighting ability and motivation using cues and signals. The rats could benefit if the conflict could be settled without a fight, and therefore, they would somehow signal their fighting ability to convince each other to retreat. Yawning of HY rats might be correlated with dominance status through its ability to encode physiological condition. The positive association between spontaneous penile erections and yawning underpins this suggestion because there is a physiological link between the two traits that depends on steroid hormones, such as testosterone (Huston 1971; Holmgren et al. 1980; Phoenix and Chambers 1982; Melis et al. 1994). Androgen hormones, like testosterone, facilitate aggressive behaviour, which is expected to characterise dominant rats. Therefore, yawn rate would be a reliable signal for indicating physiological capacity&emdash;an animal's overall quality in terms of acquired endurance, due to circulating levels of testosterone, necessary for prolonged displays and agonistic interactions (Sinervo et al. 2000)&emdash; which only dominant rats could attain. Male&endash;male conflicts might explain the finding that the yawning of littermates in HY male rats increased with male-biased sex ratios (Moyaho et al. 2009) and support a connection between yawning and dominance status. This evidence agrees with the observation that dominant males out-yawn subordinate males in stump-tailed macaques (Macaca arctoides) (Adams and Schoel 1982) and is consistent with the increase in yawning rate in male&endash;male encounters in Siamese fighting fish (Betta splendens) (Baenninger 1987). The finding that HY rats possibly inhibited LY's yawning might also be because of a male&endash;male conflict in which a HY dominant male out-yawns a subordinate LY one. However, further experiments will be necessary for supporting this hypothesis.
 
In summary, the findings of this study suggest that yawn contagion is more common than was previously thought and that it may result from a communicatory function of yawning. We believe that this function may advertise greater physiological capacity during male&endash;male conflicts.