Trigger and responder were never completely isolated e. Hence, we considered the yawn responses occurring within a 3 min time window from the yawn emitted by the trigger. To further reduce the autocorrelation bias, in case of a chain of yawns emitted by the trigger more yawns emitted in the 3-min time window we registered as a response only the first yawn performed after the perception of the last yawn.
The database see Supplementary Data Sheet included 84 males, 69 females, 16 youngsters yo , adults ad , and 15 senior se. We fitted the models in R R Core Team, ; version 3.
We established the significance of the full model by comparison to a null model comprising only the random effects Forstmeier and Schielzeth, As the response variable was binary, we used a binomial error distribution. We tested whether the interaction between the sexes or the age classes of the trigger and the responder were significant, but as they were not, we did not include them in the model.
We used a multiple contrast package multcomp to perform all pairwise comparisons for each bonding levels with the Tukey test Bretz et al. We reported the Bonferroni-adjusted p -values, estimate Est , standard error SE , and z -values. As we found at least one predictor was having a significant impact on the response, we moved on with a drop1 procedure. The GLMM also indicated a significant effect of the sex of both triggers and responders, and of bonding see Table 1 : yawn contagion of female responders was higher compared to males Figure 3 , and males, as triggers, were responded to more frequently by others compared to females Figure 2.
In contrast, we found no significant main effects of the age of both triggers and responders, the time slot in which yawns were emitted, and interaction between the sex of the subjects Table 1. Table 1. Figure 1. Line plot of the effect of the social bond between trigger and responder X -axis on the mean occurrence of acoustic yawn contagion Y -axis. Figure 2.
Line plot of the effect of the sex of the trigger X -axis on acoustic yawn contagion mean occurrence Y -axis. Effect of the trigger sex on acoustic yawn contagion when the responder is a female right and a male left. Figure 3. Line plot of the effect of the sex of the responder X -axis on acoustic yawn contagion mean occurrence Y -axis. Effect of the responder sex on acoustic yawn contagion when the trigger is a female right or a male left.
This study shows for the first time that yawn contagion is significantly affected by the social bond between individuals Table 1 even when the triggering stimuli are auditory yawns, which we defined as vocalized yawns that could be heard but not seen visual cue undetectable, auditory cue detectable.
In particular, auditory contagious yawning is significantly more frequent between kin and friends than between strangers and acquaintances Figure 1. This finding supports prediction 1a based on the EBH and not prediction 1b based on the ABH, leading to the conclusion that in humans top-down, selective visual attention cannot be the main driver of the social asymmetry observed in yawn contagion rates Norscia and Palagi, ; Norscia et al.
Contrary to Bartholomew and Cirulli , we found no age effect on yawn contagion, most probably because our database on auditory yawns had a strong prevalence of adults 25—64 years old. The highest levels of auditory yawn contagion in women compared to men confirm the gender bias observed in naturalistic conditions on humans susceptible to yawn contagion by Norscia et al.
The gender bias is also in partial agreement with previous results obtained in controlled settings, including the visual cue Chan and Tseng, ; but see Norscia and Palagi, ; Bartholomew and Cirulli, It has been hypothesized that the high degree of yawn contagion in women might inform emotional contagion Norscia et al.
However, this issue is still under debate because cultural differences across human societies can mold social bonding dynamics in a different way. It is therefore complicate, at this stage of knowledge, to disentangle cultural factors, inter-personal relationship quality, and gender influence in the distribution of yawn contagion.
Indeed, the perception of voice gender primarily relies on the fundamental frequency that is on average lower by an octave in male than female voices, with lower frequency vocalizations traveling further than high frequency ones Marten and Marler, ; Latinus and Taylor, However, to our knowledge, there is no specific study addressing the possible gender bias in yawn audibility and further investigation with experimental trials in controlled condition is therefore necessary to verify this speculation.
In this study, we also found that the differences in yawn contagion rates across categories family and friends, strangers, and acquaintances cannot be explained by differences in top-down, selective visual attention.
This finding is in line with previous literature. Contagious yawning appears to involve brain areas that are more related to the orienting-bottom up network [temporoparietal junction TPJ , brainstem nuclei, ventrolateral prefrontal cortex vlPC ] than top-down related areas [frontal eye fields FEFs , intraparietal sulcus IPS , parietal areas; for a review: Palagi et al.
Moreover, yawn contagion is neither sensitive to the sensory cues present in the signal auditory, visual, or audio-visual Arnott et al. Chan and Tseng found that the ability to detect a yawn as such perceptual detection sensitivity was related to the duration of gaze to the eyes of the stimulus releasing face, but eye-gaze patterns were not able modulate contagious yawning.
In chimpanzees, contagious yawning frequencies were highest between same-group than different-group individuals, even if the responders looked longer at out-group chimpanzee videos Campbell and de Waal, The argument that visual selective attention can bias yawn contagion rates in a specific direction subjects responding more to family than strangers is also undermined by the absence of any specific pattern of social attention in human and non-human primate.
Kawakami et al. The same study also revealed that visual attention did not depend on the target race. By measuring how long the experimental subjects gazed at the screen, Whitehouse et al. By measuring glance rates, Schino and Sciarretta observed that mandrills looked more at their own kin than at non-kin but also more at dominant than at subordinate group mates. Therefore, these studies used to support ABH describe no single pattern of selective attention.
One further important point to consider is the very definition of familiarity and group-membership adopted by most of the studies used to support ABH Massen and Gallup, Instead, familiarity or group-membership were defined on the ground of indirect knowledge e. This definition is fine for the purposes of these studies but it is not as much fine if the results are used to propose alternative explanations for the influence that real social bonding—based on real relationships—may have on a phenomenon, in this case yawn contagion.
For example, Michel et al. In ASD children, yawn contagion can be absent Senju et al. In a recent study, Mariscal et al. This finding is in line with the EBH hypothesis that links yawn contagion rates to social bonding, which can reflect emotional bonding. Our study adds to the discussion over the mechanisms underlying the social asymmetry in yawn contagion for a critical reviews: see Adriaense et al. Bottom-up attention is primarily lead by the sensory perception of the eliciting stimulus whereas top-down, selective attention is a voluntary, sustained process in which a particular item is selected internally and focused upon or examined Katsuki and Constantinidis, In this respect, the acoustic stimulus auditory yawn emitted by the trigger was heard and could elicit a yawning response in the receiver, even though the receiver was not paying any voluntary visual attention to the trigger.
Moreover, the yawning response rates were socially modulated, with auditory yawn contagion being highest in individuals that were most strongly bonded to one another. Hence, top-down selective attention is not the main driver of the social asymmetry observed in yawn contagion, which appears to be a stimulus driven phenomenon-related to bottom-up attention processes. Further investigation is necessary to understand whether and in what way other forms of attention or pre-attentive stages are able to affect yawn contagion.
The dataset used for this study is provided in the Supplementary Material. Written informed consent for participation was not required for this study in accordance with the national legislation and the institutional requirements. IN and EP carried out data collection and conceived and wrote the manuscript.
AZ helped with data collection and manuscript revision, figures, and tables. MG carried out statistical analyses and wrote the related part of the manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors wish to thank Prof. Roberto Barbuti and Prof. Cristina Giacoma for having supported the research at the University of Pisa and the University of Turin, respectively. Adriaense, J. Challenges in the comparative study of empathy and related phenomena in animals. Altmann, J. Observational study of behavior: sampling methods. Behaviour 49, — Amici, F. Response facilitation in the four great apes: is there a role for empathy? Primates 55, — Anderson, J. Psychological influences on yawning in children.
Google Scholar. Arnott, S. An investigation of auditory contagious yawning. Baenninger, R. On yawning and its functions. Barr, D. Random effects structure for confirmatory hypothesis testing: keep it maximal. Bartholomew, A. Individual variation in contagious yawning susceptibility is highly stable and largely unexplained by empathy or other known factors. PLoS One 9:e A regular deck of cards is comprised of 52 cards: 4 aces, 4 jacks, 4 queens, 4 kings, and 4 of numbers Deal out the top 16 cards control group and count the number of face cards , this is the simulated number of people who yawned in the control group.
Deal out the remaining 34 cards treatment group and count the number of face cards , this is the simulated number of people who yawned in the treatment group. Calculate the difference in proportions of yawners treatment - control , and plot it on the board.
Do the simulation results suggest that yawning is contagious, i. GSS questions cover a diverse range of issues including national spending priorities, marijuana use, crime and punishment, race relations, quality of life, confidence in institutions, and sexual behavior. Is there a difference between the average number of hours relaxing after work between males and females. What are the hypotheses? Sta Inference for two variables Testing for independence Is yawning contagious?
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