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 



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mise à jour du
21 juillet 2019
Journal of Visualized Experiments
 A Laboratory Method to Measure
Contagious Yawning in Rats
Moyaho A, Díaz-Loyo AP, Juárez-Mora OE, Beristain-Castillo E.
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Communication is an essential aspect of animal social life. Animals may influence one another and come together in schools, flocks, and herds. Communication is also the way sexes interact during courtship and how rivals settle disputes without fighting. However, there are some behavioral patterns for which it is difficult to test the existence of a communicatory function, because several types of sensory modalities are likely involved. For example, contagious yawning is a communicatory act in mammals that potentially occurs through sight, hearing, smell, or a combination of these senses depending on whether the animals are familiar to one another. Therefore, to test hypotheses about the possible communicatory role of such behaviors, a suitable method is necessary to identify the participating sensory modalities. The method proposed here aims to obtain yawn contagion curves for familiar and unfamiliar rats and evaluate the relative participation of visual and olfactory sensory modalities. The method uses inexpensive materials, and with some minor changes, it can also be used with other rodent species such as mice. Overall, the method involves the substitution of clear dividers (with or without holes) with opaque dividers (with or without holes) that either allow or prevent communication between rats placed in adjacent cages with holes in adjoining sides. Accordingly, four conditions can be tested: olfactory communication, visual communication, both visual and olfactory communication, and neither visual nor olfactory communication. As social interaction occurs between the rats, these test conditions simulate what may occur in a natural environment. In this respect, the method proposed here is more effective than traditional methods that rely on video presentations whose biological validity can raise concerns. Nonetheless, it does not discriminate between the potential role of hearing and roles of smell and vision in yawn contagion.

La communication est un aspect essentiel de la vie sociale des animaux. Les animaux peuvent s'influencer et se réunir en troupeaux ou autres groupes sociaux. La communication est également le moyen par lequel les sexes interagissent pendant les parades et par laquelle les rivaux règlent leurs différends sans se battre. Cependant, il existe des schémas comportementaux pour lesquels il est difficile de tester l'existence d'une fonction de communication, car plusieurs types de modalités sensorielles sont probablement impliqués. Par exemple, le bâillement contagieux est un acte de communication chez les mammifères qui se produit potentiellement par la vue, l'ouïe, l'odorat ou une combinaison de ces sens, selon que les animaux se connaissent ou non. Par conséquent, pour tester des hypothèses sur le rôle communicatif possible de tels comportements, une méthode appropriée est nécessaire pour identifier les modalités sensorielles participantes. La méthode proposée ici vise à obtenir des courbes de contagion de bâillement pour des rats qui se connaissent et ou pas et à évaluer la participation relative des modalités sensorielles visuelles et olfactives.
La méthode utilise des moyens peu coûteux, et avec quelques modifications mineures, elle peut également être utilisée avec d'autres espèces de rongeurs telles que les souris. Globalement, la méthode implique la substitution de séparateurs clairs (avec ou sans trous) par des séparateurs opaques (avec ou sans trous) qui permettent ou empêchent la communication entre les rats placés dans des cages adjacentes avec des trous dans les côtés adjacents. En conséquence, quatre conditions peuvent être testées : la communication olfactive, la communication visuelle, la communication visuelle et olfactive, et la communication ni visuelle ni olfactive. Comme les interactions sociales se produisent entre les rats, ces conditions de test simulent ce qui peut se produire dans un environnement naturel. À cet égard, la méthode proposée ici est plus efficace que les méthodes traditionnelles qui reposent sur des présentations vidéo dont la validité biologique peut susciter des critiques.
Néanmoins, ce test ne fait pas de distinction entre le rôle potentiel de l'audition et celui de l'odorat et de la vision dans la contagion des bâillements.
Traditionally, communicatory behavior has been studied from two perspectives. From one perspective, ethologists observe and record the behavior of animals in natural settings and attempt to recognize its adaptive value1. The particular sense or senses involved have not been the primary interest of these studies. From another perspective, physiologists are more interested in unraveling the mechanisms by which animals communicate1; hence, laboratory studies have provided methods to address the role that sensory modalities play in communication2,3. These two perspectives are indeed complementary, because knowledge of both adaptive value and immediate mechanisms is necessary to gain a comprehensive understanding of communicatory behaviors in the social life of animals.
Yawning behavior is a conspicuous component of the behavioral repertoire in several species of vertebrates4, ranging from fish to primates5. It can be described as a slow opening of the mouth and maintenance of its open position, followed by a more rapid closure of the mouth5.
The duration of the whole sequence depends on the species; for example, primates yawn for longer durations than non-primate species6. In many species, with humans being the exception, males tend to yawn more frequently than females7. This feature might underpin the possible communicatory function of yawning, although regular patterns of yawning and its daily frequency may also suggest a physiological function. In rats, spontaneous yawning follows a circadian rhythm, with peaks of high frequency occurring in the morning and afternoon8,9.
One interesting feature of yawning behavior is that it can be a contagious act (when the releasing stimulus of a behavior happens to be another animal behaving in the same way10) in several species of vertebrates11,12,13,14,15,16, including birds17 and rodents18. Furthermore, recent evidence has indicated that contagious yawning may reflect a communicatory role, because the yawning of one rat can affect the physiological state of another when exposed to olfactory cues19. However, whether or not yawning has a communicatory role is still under debate20,21, and analyzing contagious yawning is an essential first step to solve this issue.
On the other hand, contagious yawning has been linked to an animal's ability to empathize with the perspectives of other animals; hence, closely related individuals are more likely to show contagion4. This hypothesis has been frequently tested in laboratory conditions in which animals are presented with yawn stimuli on video12,13; hence, contagion can only occur through visual cues. Other investigations have assessed yawn contagion in more natural conditions using groups of animals14,15. A major problem of this is that socially interacting animals often respond to cues and exchange signals that are conveyed through combinations of sensory modalities. Disentangling the actual senses involved in a given behavior from their combined effects is not always an easy task. Typically, researchers pharmacologically or surgically hinder an animal's use of a given sense, then infer the role of that sense in the relevant behavior2,3,18,22. Fortunately, there are other methods in which only physical barriers are used to either allow or impede communication between animals23,24,25, thereby achieving greater biological validity.
The method proposed here has been specifically designed to study contagious yawning in familiar and unfamiliar rats in a social setting. According to the empathetic hypothesis, the former group should be more susceptible to contagious yawning. The method does not require the animals to be surgically or pharmacologically deprived of any senses. Instead, it works by placing the rats in adjacent cages with holes and physically obstructing their communication using either clear or opaque dividers with or without holes. Thus, four test conditions can be examined: (1) olfactory communication (OC, perforated opaque divider), (2) visual communication (VC, nonperforated clear divider), (3) visual and olfactory communication (VOC, perforated clear divider), and (4) neither visual nor olfactory communication (NVOC, nonperforated opaque divider). Therefore, researchers can compare the relative contributions of olfactory, visual, and to some extent, auditory cues in yawn contagion. This approach is not new, as similar methods have been used to isolate the senses involved in certain communicatory behaviors in animals such as lizards23 and mice26. In fact, Gallup and colleagues27 have used a similar method to demonstrate the role of visual cues in contagious yawning in budgerigars. The main features of these methods are simulation of a social context and the minimal stress inflicted on the animals. Furthermore, the use of interacting animals increases the biological validity of the conclusions.
There are several ways to measure contagious yawning25,28. Dr. Stephen E. G. Lea (personal communication, 2015) helped us numerically adapt a method previously employed by primatologists13,14 for an earlier analysis of the data used here18. Presented in this protocol is an enhanced version of this method with a wider range of applications. It consists of weighting the total number of a rat's yawns, within and outside of a given time window, by the proportion of observation time corresponding to the yawns within and outside the time window.
For example, if it is assumed that rats A and B are observed for 12 min, their yawning is recorded to the nearest minute, and a 3 min time window is set to measure contagious yawning. Next, the following sequences of yawns for each of those rats are considered: rat A (0,0,0,1,0,0,2,0,0,0,2,1) and rat B (0,1,1,0,1,1,0,0,0,0,0,3). It should be noted that each number (0-3) corresponds to the number of yawns scored at each min. For rat A, during minutes 1, 10, and 11 (numbers in bold type), rat B does not yawn within the preceding 3 min (the chosen time window) or within that minute. In those minutes, rat A yawns a total of 2 times. Therefore, the yawn rate of rat A without any yawn stimulus (non-post-yawn yawn rate) is 2/3 (i.e., 0.67 yawns/min). In the remaining 9 min, rat B yawns at least one time in either the same minute or the 3 previous minutes. Rat A yawns a total of four times in those 9 min. Therefore, the yawn rate of rat A in response to a yawn stimulus (post-yawn yawn rate) is 4/9 (i.e., 0.44 yawns/min). The application of the same procedure to rat B yields a non-post-yawn yawn rate of 2/3 (i.e., 0.66) and post-yawn yawn rate of 5/9 (0.55).
On the other hand, if yawning is recorded to the nearest decimal of a minute, yawn contagion will result in an adjusted post-yawn time. For example, if the following yawn times are recorded over a 12 min observation period for rats A and B: rat A (2.3, 5.1, 5.8, 10.4, 10.8, 11.1) and rat B (1.2, 2.4, 4.5, 5.1, 11.2, 11.6, 11.8). For rat A, the time periods over which rat B does not yawn within the past 3 min range from 0 to 1.2
min and from 8.1 to 11.2 min (i.e., 3.1 min), which yields a total of 4.3 min of non-post-yawn time. The number of times that rat A yawns during those times is three (numbers in bold type), so the non-post-yawn yawn rate is 3/4.3 (i.e., 0.69), while the post-yawn yawn rate is 3/7.7 (i.e., 0.38; the denominator from 12-4.3 min). Similarly, for rat B, the time periods over which rat A does not yawn within the past 3 min range from 0 to 2.3 min and from 8.8 to 10.4 min, which yields a total of 3.9 min. The number of times rat B yawns within those periods is one, so the non-post-yawn yawn rate is 1/3.9 (i.e., 0.25). Accordingly, the post-yawn yawn rate is 6/8.1 (i.e., 0.74).
While a near-contemporaneous match in behavior is an ideal criterion to demonstrate the presence of a contagion, aspects such as the constraints on what an individual attends to, time of reaction to a stimulus, distribution of the behavior over time (e.g., yawning may occur in episodes), and time to acclimatize to the experimental setting all give rise to species differences, making it difficult to use a unique time window. This may be the reason why researchers have used time windows that vary from seconds5 to several minutes11, which creates problems when comparing results28. Because of this, it is proposed to repeat the procedure described above for a range of time windows to obtain yawn contagion curves and compare the yawn contagion curves between species.
Equivalent yawn contagion curves can be compared by randomly distributing the number of yawns observed for each rat over the observation period. Thus, the proposed method to measure yawn contagion offers two types of controls: the (1) yawn rate occurring outside of the time window (non-post-yawn time) and (2) artificial yawn contagion curve obtained from the random distribution of the number of yawns. Therefore, this approach to analyze yawn contagion is a step forward from other procedures, such as those comparing the percentage or frequency of yawning within a single time window to that occurring outside this window25, without taking into account the actual times frames. The method is complemented by an R-based program29 to conveniently and objectively calculate the probability of contagious yawning for one or more time windows.
To illustrate the usefulness of this method and advantages of the R-based program, a data set from a previously published study18 is used. The experimental condition consisted of 144 male rats allocated to either a familiar or unfamiliar condition. The rats in each experimental condition were subdivided into four subgroups of nine pairs and exposed to any of the four test situations described above. The yawning behaviors of the rats in each experimental condition and test situation were then recorded over a period of 60 min.


There are critical steps in the method that should be taken into account to obtain successful results. Familiar rats must share home cages for at least 1.5 months after weaning and before running the experiments. However, unfamiliar rats must live in separate home cages. In both cases, the pairs of rats must come from different litters but be as similar in age as possible. Regarding the observation cages, their holes should match those in the dividers, because this is the only way to guarantee olfactory contact between the rats. The dividers, on the other hand, should be clear enough to ensure visual contact or opaque enough to ensure no visual contact. The wooden partition between one pair of rats and the other must be sufficient to prevent the rats on one side from seeing those on the other side. Another crucial aspect is the appropriate design of the experiment. Whenever there is a suspicion that a process may be biased, a random procedure should be implemented30.
The method should not present serious problems to users. Making the holes in the glass was the main technical problem faced, and because
of that, acrylic was used instead. Nonetheless, glass may be used for making the entire observation cages, provided professional advice is obtained. It should be ensured that the edges of the holes are filed to avoid glass splinters that may injure the rats. However, modifying the main method is not recommended (e.g., making the holes larger). Additionally, use of a combined group of males and females may make it difficult to detect yawn contagion.
The dividers used here may be insufficient to prevent the rats from using auditory cues, because rats are able to produce and perceive sounds at frequencies at which the materials of the observation cages and dividers likely did not block. However, this situation itself makes it possible to infer that auditory cues caused yawn contagion18 and that olfactory cues only facilitated the recognition of the partner's degree of familiarity. Therefore, the method proposed here still provides reasonable evidence to identify the senses involved in contagious yawning and their intensities.
Earlier methods have been designed to study contagious yawning in laboratory conditions mainly by presenting videos to the experimental individuals12,13, but these were questionable approaches in terms of biological validity. The method presented here solves this concern by using socially interacting animals in conditions more similar to what occurs in the real world. Furthermore, it is possible to simultaneously explore the participation of several sensory modalities in a single experimental set-up. It is recognized that this method does not absolutely discriminate between the effects of auditory cues and other sensory cues. However, a well-designed further experiment may allow researchers to infer the most likely sensory modality involved18. One possible noninvasive solution is the use of white noise to mask sounds and eliminate auditory cues. Similarly, researchers may expose nai_ve rats to bedding from OC rats to determine the role of olfactory cues, which is a proven procedure in social facilitation studies32.
The use of this method can be extended to study yawn contagion in other species. For example, this set-up can be used after simple modifications with animals such as mice and hamsters to compare yawn contagion curves. Comparisons among different species may reveal unexpected patterns. The basic experimental plan can work with larger animals such as guinea pigs, cats, and rabbits. Likewise, the method can be used to study other potentially contagious behaviors such as grooming and scratching. The R-based program can reduce the time spent calculating yawn contagion for several time windows and can be used to measure yawn contagion in other vertebrate species, provided the user has previously collected relevant data.
In summary, the main advantages of this method are the leading to acquisition of yawn contagion curves and aiding in discrimination between the relative roles of sensory modalities involved. The acquisition of yawn contagion curves is, as far as we know, a novel approach that may be useful to measure the strength of a contagion and observe how this intensity varies among species. Accordingly, the method can also be used with some modifications in other animal species such as sheep16, wolves15, dogs33, snakes34, and fish5. In all these species except snakes, yawning has been previously documented. In fact, a method similar to the one presented here has been used successfully in budgerigars27. This method may also be used to study other types of behavior that are contagious. For example, behaviors such as emotional reactivity, grooming, and scratching in rodents may be contagious. In fact, the method proposed here showed contagious emotional reactivity in familiar rats18.
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