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Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
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mystery of yawning 

 

 

 

 

mise à jour du
19 décembre 2016
rsos.royalsocietypublishing.org
R. Soc. open sci.
2016;3:150459
She more than he:
gender bias supports the empathic nature
of yawn contagion in Homo sapiens
Ivan Norscia, Elisa Demuru, Elisabetta Palagi
 
Museo di Storia Naturale, Università di Pisa
Unità di Primatologia Cognitiva, Roma, Italy

Chat-logomini

-Demuru E, Palagi E. In Bonobos Yawn Contagion Is Higher among Kin and Friends. PLoS One. 2012; 7(11): e49613
-Leone A, Mignini M, Mancini G, Palagi E. Aggression does not increase friendly contacts among bystanders in geladas (Theropithecus gelada) Primates. 2010;51(4):299-305
-Leone A, Ferrari PF, Palagi E. Different yawns, different functions? Testing social hypotheses on spontaneous yawning in Theropithecus gelada. Scientific Reports 2014;4;4010
-Norscia I, Palagi E. Yawn Contagion and Empathy in Homo sapiens. PLoS ONE. 2011;6(12): e28472
-Norscia I, Demuru E, Palagi E. She more than he: gender bias supports the empathic nature of yawn contagion in Homo sapiens. R. Soc. open sci. 2016:3:150459. http://dx.doi.org/10.1098/rsos.150459
-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 PeerJ 2:e519
-Zannella A, Stanyon R, Palagi E. Yawning and Social Styles: Different Functions in Tolerant and Despotic Macaques (Macaca tonkeana and Macaca fuscata). J Comp Psychol. 2017
-Zannella A, Norscia I, Stanyon R, Palagi E. Testing Yawning Hypotheses in Wild Populations of Two Strepsirrhine Species: Propithecus Verreauxi and Lemur Catta. Am J Primatol. 2015;77(11):1207-1215
 
 
Psychological, clinical and neurobiological findings endorse that empathic abilities are more developed in women than in men. Because there is growing evidence that yawn contagion is an empathy-based phenomenon, we expect that the female bias in the empathic abilities reflects on a gender skew in the responsiveness to others' yawns. We verified this assumption by applying a linear model on a dataset gathered during a 5 year period of naturalistic observations on humans. Gender, age and social bond were included in the analysis as fixed factors. The social bond and the receiver's gender remained in the best model.
 
The rates of contagion were significantly lower between acquaintances than between friends and family members, and significantly higher in women than in men. These results not only confirm that yawn contagion is sensitive to social closeness, but also that the phenomenon is affected by the same gender bias affecting empathy. The sex skew, also found in other non-human species, fits with the female social roles which are likely to require higher empathic abilities (e.g. parental care, group cohesion maintenance, social mediation). The fact that female influence in social dynamics also relies on face-to-face emotional exchange raises concerns on the negative repercussions of having women's facial expressions forcibly concealed.
 
1. Introduction
 
Empathy is defined as the ability to understand and share the internal states of others [1]. This ability is vital to engage in successful relationships within complex social networks and, consequently, to increase individual fitness [2]. Possibly, because women are hard-wired for maternity and parental care, they have been classically considered as more empathic than men (for an extensive review, see [3]). Psychological studies indeed report that women score higher than men on different self-reported measures of empathy in childhood [4], adolescence [5,6] and adulthood [7&endash;9] with differences growing with age during the puberty period [5,10&endash;13].
 
The higher empathic capacity of women is also strongly suggested by neurobiological studies focusing on the mirror neuron system. Through the recruitment of this system, an observer can preconsciously activate shared emotional representations during the perception of an action or of a facial expression of others [14&endash;16]. This activation response, known as perception&endash;action mechanism [14], is a basic requirement of empathy because it allows individuals to automatically experience others' affective states [3,14,17].
 
Empathy is considered to be the result of the interactions between mirror neuron areas and emotional-processing brain centres [3,18]. Through a study of functional magnetic resonance imaging, Schulte-Rüther et al. [19] found that women activated more than men the inferior frontal cortex when asked to focus on either their own feelings or the feelings of another person while seeing facial emotional expressions. Such brain area was found to include mirror neurons, as it had been previously hypothesized [20,21].
 
Moreover, within the same brain area (inferior frontal gyrus, pars opercularis) women seem to possess larger grey matter volume compared with men, with the larger grey matter volume being also coupled with higher self-reported scores in the emotional empathic propensity [22]. One of the outputs of the perception&endash;action coupling involving the mirror neuron system is facial mimicry which, in turn, is positively associated with empathy [23,24].
 
Measures of facial electromyography revealed greater facial muscle reactivity in women, compared with men, when exposed to facial expressions of anger and happiness [25,26]. Additionally, women rely more than men on facial feedback for recognizing facial expressions [27]. Hence, it is not surprising that one behavioural manifestation of empathy is facial mimicry, including contagious yawning [3,28,29].
 
Yawning is an involuntary sequence of mouth opening, deep inspiration, brief apnoea and slow expiration. In humans, yawns last on average 6s, and the individual yawn duration and frequency remains remarkably stable over weeks [30]. Yawning is an interesting topic for neurobehavioural research owing to its implications in several neuroendocrine and physiological activities including sleep&endash;awake rhythms, thermoregulation, vigilance and consequently, in the diagnostic of related disorders (for an extensive review, see Walusinski [31]).
 
Possibly because of its strict association with hormones and physiology, yawning performance can vary as a function of the degree of sexual dimorphism (sexual dimorphism hypothesis, [32]). For example, in rhesus macaques, yawning rates are strictly linked to testosterone levels, thus being more frequent in males than in females [33], the same occurs in geladas [34]. In humans, Schino & Aureli [35] noted that such androgen-driven dimorphism is not present, with men and women yawning equally often. Yawning is contagious in that it can be triggered by others' yawns [30].
 
A wide range of sensory modes are vectors of contagious yawning in humans, ranging from hearing [36], seeing [30,37], reading about [30] or even thinking about yawning [30]. Moreover, yawn contagion in humans can be affected by different variables, such as the time of the day [38], age [39] or familiarity between subjects [40].
 
As a physiological response, yawn contagion is expected to be sensitive to the interaction between individual, environmental and social factors. Despite few controversial results [39], there is growing evidence that yawn contagion is an empathy-based phenomenon. Contagious yawning recruits different neuronal networks involved in empathic processing, including the inferior frontal gyrus and other mirror neuron areas [36,41&endash;45].
 
Although some aspects of empathy may appear earlier than others [46], contagious yawning follows a similar ontogenetic trajectory as empathy. It increases with age starting at 4-5 years [47,48] when the ability to identify others' emotions is being acquired [2,49,50] and declines with old age [39] when empathic abilities also decline [51]. Contagion is significantly less likely in subjects suffering from empathy disorders, such as autism and psychopathy [52-55]. Contagious yawning follows an empathy gradient (sensu [14]) being more frequent in response to kin, then friends, then acquaintances, and lastly strangers [40].
 
Previous reports indicate that not all individuals are susceptible to others' yawns. Approximately 40-60% of healthy humans were never observed yawning in response to a yawn stimulus under laboratory conditions [28,30,37]. Moreover, susceptibility to others' yawns appears to be stable under different experimental contexts, and yawn susceptibility is not significantly different between men and women [39]. In their naturalistic study on yawn contagion, Norscia & Palagi [40] considered all the potential responders, which also included subjects showing no contagion.
 
The authors found that the probability to contagiously yawn was affected by social bond more than by any other tested variable, including gender. Therefore, social modulation more than individual features appeared to affect the probability to respond to others' yawns under natural settings. Yet, within the susceptible population, the level of yawn contagion may also vary according to different individual features. If yawn contagion is an empathy-based phenomenon, then we expect social bond to be confirmed as a variable that significantly affects yawn contagion frequencies (prediction 1a). Moreover, if women are more empathic than men, then we also expect that in the susceptible population women are infected at higher rates by others' yawns compared with men (prediction 1b). We verified these assumptions through an ethological, naturalistic approach based on a 5 year period (2010&endash;2015) of direct observation on humans.
4. Discussion
 
Our results show that in the individuals that are susceptible to yawn contagion, the rates of yawn responses are affected by both the social bond linking trigger and responder and by responder's gender. In particular, yawn contagion rates were significantly lower between acquaintances than between friends and family members (prediction 1a confirmed; figure 1) and women responded at higher rates than men (prediction 1b confirmed; figure 2) even though men and women have not been found to differ in their rates of spontaneous yawning ([35]; this study).
 
The former result is consistent with previous findings by Norscia & Palagi [40], who reported that in natural conditions the occurrence and frequency of yawn contagion correlated with the level of social closeness. The relationship quality (acquaintances, friends and kin) significantly explains the variation of yawn contagion in humans, either considering all the potential responders [40] or susceptible subjects only (present study). The increase of yawn contagion rates along with social attachment supports the hypothesis that this phenomenon has an empathic basis. In fact, one outcome of the perception&endash; action model [14] is that the more compatible and socially tied two subjects are, the easier interpartner identification is [59]. Yawn contagion is socially modulated also in non-human primates. Chimpanzees (Pan troglodytes) contagiously yawn more in response to in-group compared with out-group members [60]. In bonobos (Pan paniscus), yawn contagion peaks among closely bonded individuals, which are those who exchange more affinitive contacts [61]. A comparative study analysed the variation in yawn contagion in humans and bonobos and showed that its rates were affected by the social bond more than by the species, thus highlighting the salience of interindividual attachment to yawn contagion [57]. The relationship between yawn contagion and social bond is not limited to humans, bonobos and chimpanzees that share a close common ancestor (about 5&endash;7 Myr ago) [62]. In geladas (Theropithecus gelada), yawning is especially contagious between socially close individuals [63], thus suggesting that yawn infectiousness may be an empathy-based phenomenon also in monkeys. This is in line with the bottom-up perspective proposed by de Waal & Ferrari [64], who posit that a cognitive continuity bridges non-human to human primates.
 
Although at variable frequencies, yawn contagion has been also described between dogs, wolves and between dogs and humans [65&endash;70], O'Hara & Reeve [71] found no association between yawn response and the familiarity of the human models. Later Silva et al. [67] and Romero et al. [68] found that adult dogs yawned more in response to familiar than unfamiliar yawners, regardless of the sensory modality through which the animals perceived the stimulus (hearing or seeing). Therefore, there is evidence that yawn contagion between humans and dogs underlies some empathic abilities. In wolves, yawn contagion between conspecifics was also associated with the social closeness of group members [70]. Hence, in canids, familiarity or social bond can positively affect the frequency of yawning responses, suggesting that the susceptibility of yawn contagion might correlate with the level of emotional proximity [68,70]. The available data on social primates and canids are silent on whether the association between yawn contagion and emotional closeness found in these two mammalian taxa may have a common origin (homology) or be the outcome of convergent evolution related to social living (analogy). Whatever the case, empathy may be adaptive in highly cooperative and cognitively demanding social systems. In fact, empathy favours prosocial behaviour and dyadic closeness [3,72]. Through transitive emotional transmission [73], interindividual attachment can spread within the social network and increase group cohesion and cooperation.
 
The completely new finding of this study is that under natural conditions the women from our population sample contagiously yawned at significantly higher rates than men (figure 2). This result further supports the empathic ground of yawn contagion, in the light of the existing psychological, clinical and neurobiological evidence in favour of higher empathic abilities of women compared with men [4&endash;9,19,22,25,26,74]. A recent study on humans found no relationship between empathic abilities or gender and yawn contagion. Yet, this study was conducted in laboratory conditions on a population including an enriched cohort of university students (mean age = 32.0 ± 15.7 s.d., range = 18&endash;83 years) and was based on yawn video stimuli, self-reported contagion and self-reported scores for empathy [39]. It is not possible to make direct comparisons with our study, which is based on a different target population (with no prevalence of a specific cohort; mean age = 41.7 ± 11.3 s.d., range = 16&endash;72 years), direct observations of people in their natural settings, not aware of being under study and responding to real stimuli. Moreover, we used the social linkage as a proxy for empathy at dyadic level, because although the empathic sensitivity can vary from one subject to another, the individual expression of empathy is strongly affected by the emotional bond shared by the subjects [14].
 
The literature examining sex differences in empathy-based behaviours is scarce but still suggests that&emdash;compared with males&emdash;females are more sensitive to others' emotions and more inclined to behave prosocially [3]. For example, compared with males, female rats showed greater sensitivity to other's pain (measured via an increase of writhing; [75]) and were more likely to release a trapped cagemate [76]. In chimpanzees, female bystanders were more likely to console-distressed individuals [77] and in lowland gorillas, immature females offered more frequently consolatory contact than males [78]. The presence of a female skew in the phenomenon of yawn contagion was detected in different non- human mammals and can be interpreted in the light of the role of females according to species-specific social dynamics. Romero et al. [70] found that female wolves showed a shorter reaction time than males when observing yawns of close associates, suggesting that females are more responsive to emotional, social stimuli. This may be possibly related to the fact that wolf family packs possess a division-of- labour system in which the female predominates primarily in such activities as defence and pup care [79] requiring the ability to quickly detect the emotional state of the offspring (e.g. distress, danger) and react accordingly.
 
In bonobos, Demuru & Palagi [61] found that group members would respond more likely to a female than to a male model. Also in this case, the role of females is crucial to interpret the result. In bonobos, adult females represent the relational and decisional nucleus of the society [80&endash;84], thus playing a key role in affecting the emotional states of others [61,85].
 
In geladas, Palagi et al. [63] found a stronger and more specific matching of yawn types in female-female compared with female&endash;male dyads. In this species, females form coalitions and long-term relationships, support each other in infant rearing and remain together, regardless of whether a dominant male is present or not [86&endash;88]. According to these authors, the role of gelada females in cementing the group may rely on their capacity of being emotionally tuned to one another. The empathy gender bias suggested by yawn contagion provides biological and ethological support to some sociology studies that are revisiting the role of women in the mediation of social conflicts. For example, women as peace negotiators seem to be more generous and egalitarian than men in that they expect and ask for less. The propensity to fairness makes women potentially more successful to resolve disputes when equity is crucial to reach stable agreements, as it occurs in international conflicts involving disadvantaged parties [89,90]. Empathy enhances parental care, interindividual communication and group living, by motivating prosocial behaviours and favouring the development of moral reasoning [72]. The higher empathic abilities of women compared with men, also revealed by the gender bias in yawn contagion, may have social repercussions. The ability to preconsciously decode and replicate the emotions of others, e.g. via yawn contagion and facial mimicry, may allow women to respond with more appropriate behaviours toward others and to be more successful in forming enduring alliances [3,91]. What happens when women's social influence is reduced by forcibly preventing them from decoding facial expressions or auditory signals to connect with others ?
 
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There is no difference in contagious yawning between men and women
Andrew C. Gallup, Jorg J. M. Massen
 
published 7 september 2016 by The Royal Society
Difference in contagious yawning between susceptible men and women: why not?
Ivan Norscia , Elisa Demuru and Elisabetta Palagi
 
published 7 september 2016 by the Royal Society
 
 
1. Comparing the incomparable
 
In their commentary, Gallup & Massen [1] criticize the fact that we did not consider 'more than a dozen' previous publications which did not report gender differences in human contagious yawning. We thank the authors for pointing out this issue and for giving us the possibility to provide a brief explanation on some aspects that are not as obvious as we thought.
 
Our investigation was ethological and our framework was centred on behavioural studies also on non-human primates and other mammals. We therefore selected the articles that were relevant to our comparative and evolutionary approach. Gallup & Massen [1] state that the gender difference in yawn contagion detected in our study is a false positive and that the null effect is real. Unfortunately, the sample that they used to make this assumption (17 negative cases and one positive case) is incorrect and, consequently, so is their conclusion. The possibility to find a phenomenon relies on whether the sample and the methodology used are suitable to detect it. To retain the metaphor used by Gallup & Massen [1], you can flip a coin as many times as you want and never find what you expect if what you expect is to get a six. You should change the approach and roll a dice, instead.
 
The results presented in the article by Palagi et al. [2] were based on naturalistic observations (and not on videos as it is said in table 1 of the commentary [1]) and the database also included bonobos, in which the sex of the trigger and not the sex of the responder tended to influence yawn contagion rates [3]. Therefore, it could not be used to evaluate which variables affect yawn contagion rates in humans only. Four of the articles mentioned in their commentary must be excluded from the sample, because they were focused on sexually immature subjects and on the difference between autistic versus non-autistic children [4&endash;7], whereas our study was focused on non-pathological adults. Children are not suitable to test for gender differences because the power of empathy and yawn contagion is strongly influenced by age [8]. One further article cannot be included because the gender of the potential responder was not considered at all [9], and another one has to be excluded because it investigated yawn contagion and psychopathy [10]. In seven articles, the experimental subjects were either aware of the purpose of the study and/or a control condition was missing (the rate of spontaneous yawning) [11&endash;17]. Adopting a blind procedure&emdash;with the experimental subjects not knowing the purpose of the study&emdash;is crucial when dealing with yawn contagion because simply thinking about yawning can elicit yawns [18]. Knowing the baseline level of spontaneous yawns is also pivotal to properly measure the real differences between the rate of spontaneous and infected yawns.
 
Four of the articles mentioned in Gallup & Massen's commentary [1] used static images as stimulus to elicit a motor pattern [12,14&endash;16], and six were based on self-reports and not on objective observations (as the authors specify in table 1 of their commentary) [12&endash;17]. The commentary's authors state that there is no a priori reason to believe that different methods and measurements would alter the expression of yawns in men versus women consistently in one direction. The literature, however, does not support this statement. Static images of facial expressions lack the dynamic complexity of naturalistic social&endash;emotional interactions and, therefore, have limited external validity [19,20]. There is evidence that static and dynamic images have a different effect on men and women, with the latter showing an increase of the perception of the emotional intensity when exposed to both happy and angry dynamic facial stimuli [21]. As for the validity of self-reporting methods, a significant gender bias has been demonstrated in a wide variety of studies focusing on many different contexts [22&endash;24]. Petrides & Furnham [25], for example, demonstrated gender differences in measured and self-estimated emotional intelligence with men showing higher correlations between measured and self-estimated scores, whereas women underestimated their emotional reactions and skills. Hence, there are solid reasons to believe that different methods and measurements can alter the expression of yawns in men versus women because the existence of methodology-related gender biases has already been highlighted in previous studies focusing on the expression of emotional states. If we exclude the articles that cannot be used for comparisons for the above-mentioned reasons (self-reported scores, static images, no proper control and non-blind procedures), only two articles of the initial pseudo-sample remain. These two studies considered humans in their natural conditions: one [26] was carried out on all individuals to find out what factors influenced the presence and frequency of yawn contagion and the other [27] considered only the susceptible population to detect if other factors could affect the rate of yawn contagion when yawn contagion occurs. Based on the real available sample, and the related probability, it cannot be stated that our result is a false positive.
 
 
2. Comparative versus comparable studies
 
As regards non-human animals, the commentary's authors criticize the fact that we did not cite all the literature taking into account possible sex effects in yawn contagion. This is not correct. We cited the literature that was relevant to support and understand our results. Very briefly, we excluded articles dealing with (i) birds [28] because the framework of our study connects yawn contagion with the mirror neuron system and the mammalian brain, (ii) stressed dogs showing no yawn contagion [29], (iii) animals exposed to videos of humans or avatars [30,31] and (iv) sexually immature subjects [32].
 
The work by Massen et al. [33] deserves a specific comment as it supports our general idea that yawn contagion is also influenced by the role that individuals play in their society. Chimpanzees form male-bonded societies. Hence, it is not surprising that yawn contagion may be higher in response to males, because the relationship with males can be the most meaningful to the group members. As we summarize in Norscia & Palagi [34], there is growing evidence that the social status affects the degree of emotional involvement of individuals and their interest in what others may feel [35,36]. However, we believe that this study should be replicated without using slow motion videos because, as said above, mimicry responses are influenced by the quality of motor patterns. Moreover, the authors failed to demonstrate that the yawning response of chimpanzees was elicited by the video stimulus and not by other group mates yawning nearby. This bias raises serious concerns on how to interpret the final results.
 
The other works mentioned by Gallup & Massen [1] were considered when and if appropriate. As we specify in our article, Campbell & de Waal [37] found that only the social bond influenced yawn contagion rates in chimpanzees, which is similar to what we found in humans in our previous article [26]. The same applies to the study on dogs by Romero et al. [38], which is cited in our article. The importance of social bond in influencing yawn contagion can be so strong as to dampen the effect of any other factor if we consider the whole population (both susceptible and non-susceptible subjects).
 
The commentary's authors also state that 'the findings supporting a female bias in non-humans do not actually describe a female bias that is comparable to what Norscia and co-authors [27] report for humans'. However, we did not state that the other works of non-human animals described the exact same bias that we found. We stated that several other works had found a female skew (not the same skew) in yawn contagion and then we interpreted the different skews in the light of the role that females have in their groups 'according to species-specific social dynamics' ([27], p. 6). Finding exactly the same bias would go against our own framework, which links possible biases in yawn contagion to social dynamics. If the social dynamics are different, so should be the biases.
 
3.When the sample is not simple
 
The commentary's authors confirm that at least within our restricted sample women are more likely to yawn contagiously. And we still claim this. Within the susceptible subjects included in our study, women contagiously yawned more than men. In some of the studies cited in the commentary, some concerns could be raised about the possibility to generalize the results when the analyses are restricted to a certain cohort of individuals (e.g. undergraduate students), uprooted from their context (e.g. laboratory condition) and exposed to unreal stimuli (static images or slow motion videos; e.g. [11,16]).
 
In our case, Gallup & Massen [1] question how we selected the sample for the analysis, only leaving 34.5% of the original dataset. We indicated the size of the original dataset to precisely show that contrary to laboratory-controlled conditions, in natural settings it is necessary to gather an enormous quantity of behavioural bouts to obtain a sufficient amount of data suitable for analyses. This is a common situation in observational studies, not only in humans, but also in non-human animals.
 
It is true that in our 2016 study, we 'did not assess whether there was a difference in contagious yawning frequency in the total sample of men and women'. Indeed, as Gallup & Massen [1] also note, we had already demonstrated in 2011 that in the susceptible and non-susceptible population there is no difference between men and women in the yawn contagion frequency [26]. As a further step, we wanted to verify whether within the population in which the phenomenon of yawn contagion is present, different factors other than social bonding would affect the rates of the yawning response. We confirmed that the social bond is a key factor but also that gender can make the difference in how much a subject responds to another one within the 'yawning dyad'. Gallup & Massen [1] also criticize our choice of considering only the subjects exposed to at least three stimuli (yawns) but we strenuously defend this approach. In a natural setting, with confounding auditory and visual stimuli, we must be reasonably sure that the study stimulus is detected. This approach mirrors laboratory experimental procedures in which the yawning pattern is repeated several times in a single video to make sure that the stimulus is perceived by the observer.
 
In sum, the sample of articles on human contagious yawning that Gallup & Massen used to conclude that our result is a false positive is incorrect, because the cited articles cannot be reliably compared with our study. The comparative studies considering non-human animals were used to discuss why it is reasonable to interpret the different types of biases in contagious yawning in the light of the role that the individuals play in their social groups. Finally, not to replicate previously published results, we focused on the subjects that showed yawn contagion and we made sure that the eliciting stimulus was perceived. In our study, we found that women produce slightly more yawns than men (moderate effect size) and that gender plays a statistically significant role in susceptible people, with women showing a higher level of yawn contagion than men. We are confident that future studies will confirm our results.