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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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mise à jour du
22 septembre 2015
PLoS One.
2015;10(9):e0136979
 Repeated Witnessing of Conspecifics in Pain:
Effects on Emotional Contagion
Carrillo M, Migliorati F, Bruls R, Han Y, Heinemans M,
Pruis I, Gazzola V, Keysers C.

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Abstract
 
Witnessing of conspecifics in pain has been shown to elicit socially triggered freezing in rodents. It is unknown how robust this response is to repeated exposure to a cage-mate experiencing painful stimulation. To address this question, shock-experienced Observer rats repeatedly witnessed familiar Demonstrators receive painful footshocks (six sessions). Results confirm that Observers freeze during the first testing session. The occurrence of this behaviour however gradually diminished as the experimental sessions progressed, reaching minimal freezing levels by the end of the experiments. In contrast, the appearance and continuous increase in the frequency of yawning, a behavior that was inhibited by metyrapone (i.e,. a glucocorticoid synthesis blocker), might represent an alternative coping strategy, suggesting that the observer's reduced freezing does not necessarily indicate a disappearance in the affective response to the Demonstrator's distress.

Il est démontré chez les rongeurs que si l'un d'entre eux observe un congénère sujet à une souffrance, il est lui-même comme « tétanisé ». On ne sait pas actuellement si cette réponse se maintient dans le temps en cas d'expositions répétées.
 
Pour répondre à cette question, des rats qui ont déjà vu la souffrance d'un autre congénère familier sont soumis à six séances de chocs électriques douloureux. Les résultats confirment que les observateurs sont « tétanisés » lors de la première séance d'essais. L'apparition de ce comportement diminue cependant progressivement à mesure que les sessions expérimentales se renouvellent jusqu'à disparaître en fin de série d'expériences.
 
En revanche, l'apparition et l'augmentation continue de la fréquence des bâillements, un comportement qui a été inhibée par la métyrapone (un bloqueur de la synthèse de glucocorticoïdes), pourraient représenter une stratégie alternative d'adaptation, ce qui suggère que réduit la tétanisation de l'observateur ne signifie pas nécessairement une disparition de la réponse à la détresse affective exprimée par le conspécifique.
 
Introduction
 
Empathy, the ability to understand and share the feelings of others, can be conceptualized as a hierarchically organized multi-level capacity such that higher-level processes are built on top of more primal ones, like emotional contagion [1;2]. Emotional contagion is an automatic tendency to converge with another individual's emotional state as a direct consequence of perception and without distinguishing the origin of the emotion (i.e., self vs other) [3;4]. An increasing amount of evidence suggests that at least the basic components of empathy, namely emotional contagion, are shared with non-human mammals.
 
Evidence of emotional state sharing in rodents originates from studies showing socially-induced hyperalgesia [5], social priming [6] and social buffering [7,8]. For example, mice and rats learn to fear a conditioned stimulus by simply observing or interacting with a conspecific in distress [6]. Sharing the distress of others has also been evidenced by the socially triggered freezing response exhibited by shock-experienced observers when witnessing demonstrators endure painful foot electroshocks [9&endash;13]. This phenomenon is modulated by the genetic characteristics of the rodent strain [14], context [12] the degree of familiarity between observer and demonstrator and by previous experience of the observers [11]. In addition, the expression of emotional contagion in both mice and humans is dependent on stress levels of the observer animal [15], as reduced affective responses can be restored by administration of a glucocorticoid synthesis inhibitor.
 
So far, all the studies investigating emotional contagion in rodents have examined the behavior of animals after a single exposure or interaction with another in distress. Despite the increasing characterization of emotional contagion in rodents, it is still unknown how animals would respond following repeated witnessing of a conspecific in pain. How would animals respond following repeated testing with a conspecific in pain? This question is of methodological interest, as many experiments would require repeated testing of an individual, be it to investigate, using repeated measures the effect of drugs or to record neural activity and behavior over multiple exposures. Here, leveraging our rodent model of empathy [9], we exposed shock experienced rats on multiple days to familiar Demonstrators undergoing footshocks to investigate whether and how behavior changed from day to day.
 
 
Results and Discussion
 
Shock-experienced Observer rats were exposed to familiar Demonstrators undergoing footshocks during six identical, semi-consecutive testing days. Each testing day contained a preshock baseline period and 5 shocks, during which the freezing of Demonstrators and Observers was scored.
 
Freezing of Demonstrators
 
A 6 Days x 6 Epochs (1 baseline + 5 shock periods) ANOVA revealed a significant Day x Epoch interaction (F25,100 = 3.96, p<0.0001). This interaction was driven by Day 1, as removing Day 1 rendered the interaction non-significant (p>0.05). A 6 Day repeated measures ANOVA on baselines showed differences between freezing levels of Demonstrators during the baseline period of Days 1 to 6 (F5,30 = 10.751, p<0.001; Fig 1B). Specifically, relative to the preshock-baseline of Day 1, Demonstrators displayed high freezing levels throughout (paired t-tests of baseline Day 1 compared to Days 2 to 6, all p<0.05). Further, planned comparisons using paired sample t-tests of each shock period to baseline, revealed that on Day 1, Demonstrators froze more following each one of the five shocks than baseline (all p<0.01; Fig 1B). In contrast, the same analysis showed that except for two data points, on Days 2 to 6, the Demonstrators' freezing levels during the shock periods was not higher than on baseline. This indicated that after the first test Day Demonstrators developed contextual freezing. Freezing of Observers
 
A 6 Days x 6 Epochs ANOVA on the freezing of Observers revealed main effects of Days (F5,20 = 9.45, p<0.0001) and Epoch (F5,20 = 4.1, p<0.01; Fig 1B) and a significant Day x Epoch interaction (F5,20 = 1.68, p<0.05). In contrast to Demonstrators, a 6 Day repeated measures ANOVA on baselines showed no significant differences between freezing levels during the baseline period of Days 1 to 6 (p>0.1). Planned paired sample t-tests comparing shock with baseline periods for each Day indicates diminished freezing after Day 4 (Fig 1B). Specifically, post-hoc t-tests revealed Observers froze significantly more during various shock- periods of Days 1, 2 and 3 (compared to those day's baseline, all p<0.05) while this was not the case on Days 4 to 6 (all p>0.4). This reduction in freezing of Observers, could suggest that their sensitivity to the distress of the Demonstrator diminishes following repeated exposure. Emergence of Yawning in Observers
 
Throughout the experiment, we however noticed the appearance of yawning, an unusual behaviour displayed only by the Observers (Fig 2, S1 Video). Yawning included extensive opening of the mouth and most of the times a full-body extension and upward pointing of the snout. A 6 day repeated measures Friedman test on normalized yawns (i.e., number of yawns during the first 10mins of shock period minus number of yawns during preshock period [first 10 minutes at start of test prior to 1st shock]) detected differences in yawning frequency between Days (É'2 (5) = 12.12, p = 0.033). Planned Wilcoxon posthoc tests comparing yawning frequency between Day 1 and Days 2 to 6 revealed that Observers yawned more during Day 6 compared to Day 1 (p = 0.017). The yawning response of Observers appeared to be specific to the distress of the Demonstrators, as a Wilcoxon signed rank test comparing the total number of yawns during the combined preshock periods of Days 1 to 6 to the total number of yawns during the shock periods of Days 1 to 6, showed that Observers yawned more during the shock periods (Z(6) = -2.2, p<0.05) (Fig 1B and 1C). Further, the percent of Observers yawning increased throughout the experiment, with more than 70% of animals yawning in the last two Days compared with 0% on Day 1 (Fig 1C). Moreover, by Day 6, all Observers had yawned at some point indicating a generalized behavioral response. The number of yawns depended on the time of day at which rats were tested. Three rats were tested in the morning (beginning of their dark phase), and showed on average a total of 9 yawns over the 6 days. Four rats were testing in the afternoon (second half of their dark phase) and showed on average a total of 19 yawns. To ensure that the increase of yawns across Days was not due to an inadvertent shift in testing time, the total number of yawns on each Day was compared with the average testing time on that day, but the relationship was clearly non-significant (r2<0.0067, p = 0.87). Importantly, the results of a separate experiment showing that yawning was significantly inhibited by pre-treatment with metyrapone (t(18) = 2.191, p = 0.042), suggests that yawning reflects heightened stress levels in the Observers.
 
Attention in Observers
 
To investigate whether the attention of Observers towards the Demonstrators changed throughout the experiment, the percent of time Observers spent in the window zone (i.e., 12cm x 25cm area closest to the divider from the Demonstrator' chamber) was quantified (Fig 1C). A repeated measures ANOVA with 6 Days x 2 Epochs (comparing the 10 minute preshock period prior to shock start and the 10 to 15 minute after the 1st shock) revealed a main effect of Epoch (F1,4 = 13.3, p<0.05). This indicated that Observers were drawn to spend a higher percent of time in the window zone following shock delivery. The absence of an interaction of Epoch and Day (p>0.05) however shows this effect to be constant across days, suggesting that the attention of Observers was captured by the Demonstrators receiving shocks in a way that was sustained throughout the experiment.
 
Discussion
 
Demonstrators submitted to repeated and unavoidable foot shocks exhibit elevated freezing levels. Confirming previous findings [9;11;12;16] in the first testing session (i.e., Day 1), shock-experienced Observers display freezing in response to familiar Demonstrators enduring painful footshocks. As to our core question of whether these effects can be measured over repeated days, as necessary for designs that require repeated testing, our results show that freezing gradually diminishes as a consequence of repeatedly witnessing the Demonstrator receive painful stimulations. Results of a separate pilot experiment revealed that this reduction of freezing occurs even if a number of experimental factors are manipulated to reduce such habituation (S1 Fig). Alternating between different testing contexts, increasing the length of time between testing sessions, pairing two Demonstrators to each Observer and adding a reminder shock session for the Observers, failed to avoid a progressive reduction of the Observer's freezing. From an experimental design point of view, our findings thus indicate that socially triggered freezing, as an assay of social sensitivity in rodents may be more suited for between-subject designs (that do not require multiple testing of a given rodent) than for within-subject designs. In addition, at first glance, our findings could suggest that the affective response of Observers to the distress of Demonstrators is progressively reduced throughout the testing sessions. The appearance of yawning however complicates this interpretation.
 
Yawning is a phylogenetically old behavior, ubiquitously present across vertebrates [17&endash;21]. It is characterized by an extensive and involuntary opening of the mouth with deep, prolonged inspirations and short expirations lasting approximately 10 seconds and commonly accompanied by stretching. Yawning has been observed in stressful situations in different species like monkeys [22&endash;25], rats [26] and birds [27]. Thus, the emergence of yawning as freezing becomes infrequent could mean that animals change the way they manifest their affective response to the distress of others, but that animals are still responsive to the distress of the other. Yawning as a possible indicator of elevated stress levels in the Observers was confirmed by the reduction of this behavior following administration of an anti-stress drug (i.e., metyrapone) on test days 5 and 6. This is in agreement, with results showing that administration of anxiogenic drugs to monkeys induces both anxiety-like behavior and yawning [25], suggesting that indeed yawning is indicative of elevated stress levels. It has been hypothesized that in addition to being a marker of arousal, yawning marks the transition between different types of arousal or levels of arousal [28]. Perhaps then, yawning in Observers indicates a change in the type of arousal the Observers experience during the first testing days compared to the arousal in the last testing days. In contrast, the repeated daily shock exposure the Demonstrators undergo maintains a highly elevated but similar arousal type throughout the experiment, thus preventing yawning form emerging. However, this is highly speculative and further testing such as corticosterone measurements throughout the experiment would be necessary to confirm this hypothesis. In addition to the postulated role in stress, yawning has been linked to a variety of other functions, such as a thermoregulation [20,29]. Here though all sessions were conducted in conditions of constant room temperature. That yawning appeared following repeated testing, was specific to the shock periods and only present in Observers suggests that the most parsimonious explanation for its emergence is that it is indicative of changes in autonomic regulation and reflects an affective response in the Observer to the distress of the Demonstrator. Together, these findings and the results showing that the Observers attention towards the Demonstrators is unaltered indicate that although the freezing response to witnessed distress changes over time, the affective response of the Observers may outlast socially triggered freezing and invite yawning as a coping mechanism. However, more data will be needed to fully understand the relationship between freezing, yawning and other stress related manifestations.