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mise à jour du
14 avril 2014
Physiology Behavior
2014;130:145-8
A Thermal Window for Yawning in Humans:
Yawning as a Brain Cooling Mechanism
 
Jorg J. M. Massen, Kim Dusch,
Omar Tonsi Eldakar, Andrew C. Gallup 

Chat-logomini

Andrew C. Gallup. Yawning and the thermoregulatory hypothesis
 
 
The thermoregulatory theory of yawning posits that yawns function to cool the brain in part due to counter-current heat exchange with the deep inhalation of ambient air. Consequently, yawning should be constrained to an optimal thermal zone or range of temperature, i.e., a thermal window, in which we should expect a lower frequency at extreme temperatures. Previous research shows that yawn frequency diminishes as ambient temperatures rise and approach body temperature, but a lower bound to the thermal window has not been demonstrated. To test this, a total of 120 pedestrians were sampled for susceptibly to self-reported yawn contagion during distinct temperature ranges and seasons (winter: 1.4oC, n = 60; summer: 19.4oC, n = 60). As predicted, the proportion of pedestrians reporting yawning was significantly lower during winter than in summer (18.3% vs. 41.7%), with temperature being the only significant predictor of these differences across seasons. The underlying mechanism for yawning in humans, both spontaneous and contagious, appears to be involved in brain thermoregulation.
 
 
1. Introduction
 
Yawning occurs with an average duration of 4 to 7 sec, and consists of three distinct phases: an active gaping of the jaw with inspiration, a brief period of acme corresponding with apnea and peak muscle contraction, and a passive closure of the jaw with shorter expiration [1]. In humans [2], as well as a handful of other social vertebrates [3-7], yawning can be categorized into two basic forms: spontaneous and contagious. Both forms include similar motor action patterns, but spontaneous yawns seem to be triggered by physiological mechanisms of homeostasis and arousal since they reliably occur during distinct behavioral contexts [8, 9] and follow a consistent circadian pattern [10]. In contrast, contagious yawns are elicited simply by sensing or even thinking about the action in others [11]. Unlike its spontaneous form, which appears evolutionarily older by its observed presence in all classes of vertebrates [12] and early onset in uterine development [13], contagious yawning appears to be a more recently derived behavior as evidenced by its presence in relatively few highly social species [2-7] and delayed ontogeny [14-18]. Research investigating contagious yawning has emphasized the influence of interpersonal and emotional-cognitive variables on its expression [4, 5, 19-28], but there have been few attempts to combine theoretical frameworks when explaining both contagious and spontaneous effects. Due to the potential multifunctionality of yawning across species [12,29], however, recent reports on social primates have highlighted potentially important differences in yawn morphology or intensity [5, 30, 31] Although it is commonly believed that yawns serve a respiratory function, experimental procedures have shown yawn frequency is independent of brain/blood levels of O2 and CO2 [32]. A more recent theory, which posits that the motor action of yawning functions as a brain cooling mechanism [33, 34], has received growing empirical support [reviewed by 35]. For example, research on both rats and humans shows that yawning is preceded by intermittent rises in brain temperature and localized mild hyperthermia and then followed by equivalent decreases in temperature immediately thereafter [36, 37]. While various critiques have been proposed regarding the thermoregulatory theory [38-42], no study has found evidence contrary to its main predictions and all current arguments remain untenable [35, 43].
 
According to the thermoregulatory theory, the cooling effects of yawns occur through thermoregulatory mechanisms of counter-current heat exchange, evaporative cooling and enhanced cerebral blood flow [44]. Consequently, the effectiveness of yawning is dependent on the ambient air temperature, and the expression of this behavior should be constrained to an optimal thermal zone or range of temperature, i.e., a thermal window. In particular, this theory posits that yawns should (1) increase in frequency with initial rises in ambient temperature, as this stimulates thermoregulatory mechanisms to control temperatures within a normal range, (2) decrease as ambient temperatures draw near or exceed body temperature, since taking a deep inhalation of air above one's body temperature would be counter productive, and likewise (3) should diminish when temperatures fall below a certain point, because thermoregulatory cooling responses are no longer necessary and countercurrent heat exchange could result in deviations below optimal thermal homeostasis. Since both spontaneous and contagious yawns are indistinguishable, aside from different triggers, the predictions of the thermal window hypothesis should apply to both forms. Experimental and observational research reports of spontaneous yawning in non-human primates [10, 5], birds [46, 47], and rats [48] have confirmed the first two predictions of this model. Additionally, it was recently discovered that self-reported contagious yawning frequency in humans varies with seasonal climate variation [49].
 
In particular, two independent groups of pedestrians were sampled in an arid desert climate (Tucson, AZ, USA): the first in summer (37°C) and the other during 'winter' (22°C). Contagious yawning frequency was significantly lower during the hot summer climate (24% vs 45%), with temperature being the only significant factor contributing to this response after controlling for other variables, such as humidity, sleep and time spent outside. Here we tested the lower bound of the thermal window hypothesis by investigating the frequency of self-reported contagious yawning in a climate with a colder winter season (Vienna, Austria). In this case the summer condition provided temperatures equivalent to those in winter months of Tucson, while the winter condition included temperatures at and slightly below freezing.
 
 
4. Discussion
 
Overall, these results show that significantly fewer pedestrians reported contagious yawning during the cold winter (-4 to 7oC), and that, similar to effects observed in an arid desert climate [49], temperature was the only significant predictor of this response when controlling for other variables. As predicted by the thermal window hypothesis, reports of yawning were constrained to an optimal thermal zone or range of ambient temperature (figure 1). Importantly, changes in daylight across the seasons cannot account for these results. First, a particular time frame was chosen for both studies (between 1 and 3 pm) whereby contagious yawning frequencies remain unchanged [53]. Second, the proportion of people that reported yawning in the summer in Vienna, Austria (current study) was comparable to that of the winter in Tucson, Arizona USA [49], whereas there is a large difference in daylight hours between these samples (Summer in Vienna: ± 16h vs. Winter in Tucson: ± 10h). Lastly, an inverse seasonal pattern emerged between the two study locations; i.e., whereas in Tucson there was a high frequency of reported yawning in winter, and a low frequency of reported yawning in summer, in Vienna there was a high frequency of reported yawning in summer, and a low frequency of reported yawning in winter. Thus, it cannot be generalized that people yawn more or less in winter vs. summer, nor with greater or fewer hours of daylight. Instead, the ambient air temperature accompanying the season appears to determine reported yawn frequency. This report adds to accumulating research suggesting that the underlying mechanism for yawning, both spontaneous and contagious, is involved in brain thermoregulation. The thermoregulatory theory provides clear predictions for both the primitive and derived features of this behavior. That is, the thermoregulatory benefits resulting from yawning provide the mechanism by which arousal or state change can be achieved [8, 10], while the spreading of this behavior, i.e., yawn contagion, would therefore coordinate arousal in a group and enhance overall group vigilance [33]. In addition to enhancing the basic understanding of why we yawn, applications from this research include improved treatment and diagnosis of patients with thermoregulatory problems [34, 37, 54, 55].
 
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