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 



mise à jour du
8 février 2020
Intraspecific Motor and Emotional Alignment
in Dogs and Wolves:
The Basic Building Blocks of Dog&endash;Human
Affective Connectedness
Elisabetta Palagi, Giada Cordoni
Ethology Unit, Department of Biology, University of Pisa


Involuntary synchronization occurs when individuals perform the same motor action patterns during a very short time lapse. This phenomenon serves an important adaptive value for animals permitting them to socially align with group fellows thus increasing integration and fitness benefits. Rapid mimicry (RM) and yawn contagion (YC) are two behavioral processes intermingled in the animal synchronization domain.
Several studies demonstrated that RM and YC are socially modulated being more frequently performed by individuals sharing close relationships. This evidence highlights the relation between RM/YC and emotional contagion that is the capacity of two or more individuals to share the same affective state.
In this review, the authors try to delineate a possible developmental trajectory of emotional sharing phenomena by using, as a model species, the domestic dog (Canis lupus familiaris), a valid example of empathic predisposition towards individuals belonging both to the same and the different species. They contrast available findings on RM and YC in dog&endash;dog and dog&endash;human dyads with those in wolf&endash;wolf dyads, in order to investigate if the ability to emotionally engage with conspecifics (wolf&endash;wolf and dog&endash;dog) is evolutionary rooted in canids and if provides the basis for the development of inter-specific emotional sharing (dog&endash;human).
La synchronisation involontaire se produit lorsque les individus exécutent les mêmes schémas moteurs pendant un laps de temps très court. Ce phénomène a une valeur adaptative importante pour les animaux leur permettant de s'intégrer socialement avec les membres du groupe, augmentant ainsi les bénéfices de cette intégration et de bien-être.
Le mimétisme rapide (RM) et la contagion du bâillement (YC) sont deux processus comportementaux entremêlés dans le domaine de la synchronisation animale. Plusieurs études ont démontré que la RM et la YC sont socialement modulées, étant plus fréquemment effectuées par des individus partageant des relations étroites. Ces preuves mettent en évidence la relation entre RM / YC et la contagion émotionnelle qui est la capacité de deux personnes ou plus à partager le même état affectif. Dans cet article les auteurs essaient de montrer l'évolution du développement des phénomènes de partage émotionnel en utilisant, comme espèce modèle, le chien domestique (Canis lupus familiaris), un exemple valide de prédisposition empathique envers les individus appartenant à la même espèce et aussi à d'autres espèces.
Ils comparent les résultats disponibles sur la RM et la YC dans les dyades chien &endash; chien et chien &endash; humain avec ceux dans les dyades loup &endash; loup, afin d'étudier si la capacité de s'engager émotionnellement avec des conspécifiques (loup &endash; loup et chien &endash; chien) est enracinée dans l'évolution canidés et si cela fournit une base pour le développement du partage émotionnel interspécifique (chien &endash; humain).
Les zones cérébrales impliqués dans les systèmes de récompense, de stress, d'imitation et prosociaux ont été conservés au cours de l'évolution des mammifères

 Tous les articles sur la contagion du bâillement
All articles about contagious yawning
-Palagi E, Leone A, Mancini G, Ferrari PF. Contagious yawning in gelada baboons as a possible expression of empathy. Proc Natl Acad Sci USA. 2009;106(46):19262-19267
-Palagi E, Norscia I, Demuru E. Yawn contagion in humans and bonobos: emotional affinity matters more than species Peer J 2:e519
-Palagi E, Norscia I, Cordoni G. Lowland gorillas (Gorilla gorilla gorilla) failed to respond to others' yawn: Experimental and naturalistic evidence. J Comp Psychol. 2019
-Palagi E, Guillén-Salazar F, Llamazares-Martín C. Spontaneous Yawning and its Potential Functions in South American Sea Lions (Otaria flavescens). Sci Rep. 2019;9(1):17226.
-Palagi E, Cordoni G. Intraspecific Motor and Emotional Alignment in Dogs and Wolves: The Basic Building Blocks of Dog&endash;Human Affective Connectedness. Animals 2020;10(2):241
-Norscia I, Zanoli A, Gamba M, Palagi E. Auditory Contagious Yawning Is Highest Between Friends and Family Members: Support to the Emotional Bias Hypothesis. Front Psychol. 2020 Apr 3;11:442

1. Introduction
Behavioral non-conscious synchronization is widespread among animals, including humans. It occurs when individuals engage in the same motor action during a very tight time window and when they are spatially close [1,2]. Synchronizing with others has a highly adaptive value and produces many different benefits as a function of the type of synchronization. For example, the synchronization in reproduction, movements, and vigilance of group living animals can increase their effectiveness in the defense from predators [1]. Synchronization can occur not only at group level but also at dyadic level [3]. During their dyadic social interactions, human and non-human animals can synchronize their motor actions such as facial expressions and body postures [4]. For example, it has been recently demonstrated that dogs synchronized their resting and locomotor activity with that of their owners when they were freely acting in an open area [2].
The behavioral synchronization domain includes two phenomena that are still debated topics in human and non-human animal studies: Rapid Mimicry (RM) and Yawn Contagion (YC) [5]. Even though they are often considered as different processes, they seem to share similar neural and social mechanisms [6&endash;8]. It has been proposed that these motor resonance behaviors are grounded in the automatic perception&endash;action coupling in the sensorimotor areas [5,9] The mirror neurons, discovered in monkeys and humans, provided neurophysiological support to the perception&endash;action model, because they fire when the motor action is both observed and perceived. For this reason, a large array of studies indicates that RM and YC may be automatic, fast, reflex-like mechanisms which go beyond the intentional control [10].
RM and YC seem to intermingle with emotional contagion which is defined as "the tendency to automatically mimic and synchronize expressions, vocalizations, postures, and movements with those of another person's and, consequently, to converge emotionally" [11]. Emotional contagion is a well-known basic building-block of empathy [5] and implies that two (or more) subjects share the same affective state [12]. The perception of others' action leads the observer to automatically reproduce the same action. Through this unconscious mirroring response, the observer can experience the same affective emotional state underpinning such action [13]. The expression and perception of emotions in non-human animals seem to be adaptive because these skills allow them to respond quickly and appropriately to unpredictable situations thus increasing their survival and fitness [14,15]. According to the perception&endash;action coupling, the capacity to mirror others' behaviors acquires an even more adaptive value in animals whose relationships are not inhibited by rank rules and that build and maintain their bonds through cooperation and social affiliation [16].
Beyond primates, cohesive and cooperative societies also characterize several social carnivores such as wolves (Canis lupus lupus) and dogs (Canis lupus familiaris) [17,18]. Compared to wolves, dogs have expanded towards humans their propensity to synchronize and affiliate [2]. Dogs develop strong affinitive bonds with owners, which represent their favorite social partners [19]. One of the aspects of this preferred affectional bond seems to be the empathically predisposition of dogs towards humans' emotions [20]. The capacity of dogs to understand and experience humans' emotions (i.e., empathy) [5,12]can be evidenced by their (1) preferential responses to the cry of humans compared to their humming or talking [21], (2) ability to discriminate emotions that are more positive for owners [22] and (3) high propensity to be infected by humans' yawns [23&endash;25]. The question arising from these evidence deals with the origin of the human&endash;dog emotional sharing: is it a phenomenon shaped by artificial selection or evolutionarily rooted in the line of social carnivores? Trying to answer the question, we focus on rapid mimicry (RM) and yawn contagion (YC) in wolf and dog groups to investigate if the ability to emotionally engage with conspecifics can provide the basis for the development of inter-specific emotional sharing.
2.2. Yawn Contagion in Dogs and Wolves: When the Partner Matters
Spontaneous yawning is a primitive stereotyped motor action pattern, that once triggered, is uncontainable and unstoppable [54]. It cannot be considered as a facial expression because it recruits facial, oral, laryngeal, pharyngeal, thoracic and abdominal muscles. Indeed, depending on the species, yawning may be also accompanied by eye closing, vocalizations, body stretching, pandiculation and even tongue protrusion [63]. Yawning is a widespread phenomenon in mammals and birds [64,65]. In humans, the new ultrasound technologies evidenced the presence of spontaneous yawning just starting from the fetal phase [66]. The occurrence of fetal yawning seems to contribute in assessing the correct development of brainstem and understanding the neural underpinnings of sleep and arousal systems [66]. Several hypotheses on the functions of spontaneous yawning in non-human animals have been formulated and these involved both physiological and social explanations. Indeed, yawning could act as a homeostatic restoring and brain cooling mechanism, an anxiety and drowsiness signal, and it has also a role in the social communicative system (e.g., threat or alertness yawn) [63].
Contagious yawning, a behavioral act involuntarily induced by viewing or listening other's yawns [64], is considered as a different phenomenon which has been widely demonstrated in human and non-human primates [67&endash;71]. In primates, yawn contagion can be considered as a proxy of emotional contagion and it can be associated with the level of social attachment between partners [5]. Even though in human and non-human primates the social modulation of contagious yawning is supported by ethological [68&endash;71], neurological [72,73], and psychological evidence [74], contradictory results about proximate mechanisms of contagion emerged from the studies on domestic dogs. In 2008, Joly-Mascheroni and co-authors [23] evidenced that dogs responded to humans' yawns in the 72% of experimental cases. This first evidence of contagious yawning between two different species led to hypothesize a possible association between the phenomenon and empathic involvement between partners. Later, two studies found neither evidence of yawn contagion in dogs nor its linkage with empathy [75,76]. In 2013, Madsen and Persson [77] demonstrated the occurrence of dog&endash;human yawn contagion. However, the empathic interpretation of the phenomenon was not supported because the relationship quality shared by the interacting subjects (dog-owner vs dogunfamiliar human) did not affect the level of contagion [77]. Silva and colleagues [25] provided evidence in favor of the empathic hypothesis of contagious yawning in dogs by using auditory instead of visual stimuli. During the experiment, dogs yawned more frequently when the auditory stimulus came from familiar (the owner) rather than unfamiliar humans. This first evidence of social modulation of yawn contagion was quickly challenged. In many species, including dogs, spontaneous yawning can emerge in response to environmental or social stressors [63, 78&endash;80]. In this light, it has been suggested that the finding obtained by Silva and colleagues [25] could be simply ascribed to a distress response by dogs. When dogs heard, but not saw, their owner, they experienced high anxiety levels that determined an increase in their yawning response.
In order to discriminate between the two possible proximate causes (empathy vs anxiety) of yawn contagion in dogs, Romero and co-workers [24] carried out an elegant study integrating ethological and physiological approaches. During the research, dogs observed familiar (the owner) and unfamiliar humans while yawning (experimental condition) or simply making mouth movements (control condition). Concomitantly, the heart rate and heart rate variability, two reliable physiological indicators of stress and well-being in animals [81], were monitored. The authors demonstrated that dogs yawned more frequently in experimental than in control condition and they were more infected by the yawns of familiar than unfamiliar humans. Intriguingly, the physiological parameters did not differ between experimental and control condition, thus suggesting that yawn contagion was not related to environmental or social stressors, but it was modulated by the affinitive attachment between dogs and their owners.
Recently, by investigating the possible relation between yawn contagion and the empathic gradient Kis and colleagues [82] provided contrasting results. The authors tested 33 dogs in both yawning and control condition by previously treating them with intranasal oxytocin or placebo. Contagious yawning did not occur at all and the number of yawns performed by dogs were not related to the degree of social closeness with owners but rather with the levels of anxiety measured by mouth licking. Moreover, the oxytocin pre-treatment significantly reduced the yawning events. Nevertheless, it is worth noting that intranasal administration of oxytocin can activate the endogenous hypothalamic oxytocin system, thus the still lack of information about the neural, physiological and behavioral consequences of this activation implies to interpret with caution the observed effects of exogenous oxytocin [83&endash;85]. Accordingly, Romero and colleagues [50] found that the effects of exogenous oxytocin in dogs were fine-tuned by the individual variability in endogenous oxytocin: the dogs showing high basal levels of oxytocin were less responsive to the effects of intranasal oxytocin. In order to clarify the "social role" of oxytocin in dog&endash;human emotional contagion, future studies should take into account the interaction between the applied hormone doses and endogenous secretion in modulating behavioral changes.
If the occurrence of contagious yawning and its proximate causes have been investigated in the dog&endash;human relationship, no studies are available on the phenomenon of yawn contagion between dogs. Is the phenomenon of yawn contagion exclusively linked to dog&endash;human interactions because of the domestication process or is this motor resonance phenomenon deeply rooted in social carnivores and simply transferred from conspecifics to human partners in the domestic dogs? A study carried out by Romero and colleagues [86] on captive wolves may answer the question. The authors observed the animals in their environmental and social setting without altering their ordinary habits. The wolves yawned more frequently when they were exposed to conspecific yawning and the propensity to be infected was positively linked to the strength of social relationship shared between the trigger (the initial yawner) and the observer. These findings suggest that contagious yawning is an ancestral phenomenon firstly naturally selected for intra-specific social communication and group synchronization and later artificially selected for inter-specific communication. To complete this framework, it is therefore crucial exploring the occurrence of the phenomenon of yawn contagion and its potential roles in groups of dogs characterized by a certain level of variance in the distribution of relationship quality.
3. Conclusions
Wolves, the ancestors of dogs, constitute cohesive family group whose members actively and cooperatively participate to the pack life creating a sort of "division of labor" system [87,88]. As humans, wolves engage in strong social and emotional bonds with conspecifics and these relations could be at the basis of the evolution of dog&endash;human affective attachment [62]. The brain areas involved in reward, stress, imitation, and prosocial systems have been evolutionary conserved along with the developmental pathway of mammals [89&endash;91].
This common neurological state could have permitted wolves and (ancient) humans to develop, during the progressive increase of their cohabitation, a shared representation of actions and emotions. Motor and emotional sharing probably promoted wolf&endash;human social interactions and improved interspecific empathic predisposition [92] that is at the basis of the long history of dog&endash;human affinitive relationship. In conclusion, to understand the role of the domestication process and artificial selection operated by humans in shaping the emotional contagion of dogs (rapid mimicry and yawn contagion), we should focus not on the possible presence and distribution of these phenomena between hand-reared wolves and humans but, instead, between the different wolf pack members [93]. Long-term studies should quantify (dyadic variance, seasonality, hormonal variations) and qualify (affiliation, agonistic support) the relationship quality shared by the subjects and verify whether the incidence of rapid mimicry and yawn contagion is socially modulated in wolves. A further important point is whether the occurrence and the distribution of rapid mimicry and yawn contagion covariate with some empathy-driven and prosocial behaviors such as consolation and helping. This could provide an indirect evidence of the potential empathic nature of these motor resonance phenomena.
As for dogs, we should focus on the different breeds. By selecting the most recent (less humanoriented) and ancient breeds (more human-oriented) as models we can evaluate to what extent the artificial selection has operated in shaping the mimicry phenomena. To reach the goal, observational studies on groups of dogs belonging to the same breed and experimental studies including dogs of different breeds and their owners are necessary.