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
http://www.baillement.com

mystery of yawning 

 

 

 

 

mise à jour du
21 février 2017
Adaptative Human Behavior and Physiology
2017
Acute Physical Stress Modulates the Temporal Expression of Self-Reported Contagious Yawning in Humans
 
Omar Tonsi Eldakar, Jaime L. Tartar, Daniel Garcia1, Valentina Ramirez, Melissa Dauzonnel, Yana Armani, Andrew C. Gallup

Chat-logomini

 
Andrew C. Gallup. Yawning and the thermoregulatory hypothesis
 
Abstract
A growing number of studies on non-human animals have documented that stressors modulate the expression of yawning. In particular, recent experimental research shows that yawns are initially inhibited following physical stress, but then become potentiated thereafter. However, stress-induced yawning in humans has yet to be demonstrated experimentally. Here, we investigated the temporal relationship between self-reported contagious yawning and an acute physical stressor in 141 human subjects in the laboratory.
 
Using a 2 _ 2 between-subjects design, participants either underwent the cold pressor test (CPT) or a matched control condition prior to viewing a contagious yawning stimulus that was either displayed immediately thereafter or following a 20-min delay. Consistent with the comparative literature, we show an interaction between stress and time conditions, whereby both the incidence and frequency of yawning are lowest in the immediate-CPT trials and highest in the delayed- CPT trials. These findings support a homologous effect of acute physical stress on yawning across birds and mammals that may be related to an adaptive thermoregulatory and arousal function.
 
Résumé
Un nombre croissant d'études animales ont documenté que les facteurs de stress modulent l'expression du bâillement. En particulier, des recherches expérimentales récentes montrent que les bâillements sont initialement inhibés à la suite d'un stress physique, mais qu'ils augmentent de fréquence par la suite.
Le bâillement causé par le stress chez l'homme n'a pas encore été démontré expérimentalement. Les auteurs ont étudié la relation temporelle entre le self-report de contagion du bâillement et un stress physique aiguë chez 141 sujets humains (en laboratoire).
 
Les participants ont subi une exposition au froid et une condition de contrôle c'est à dire de visualisation de bâillements qui a été montrée immédiatement à la suite du stress ou après un délai de 20 minutes.
 
Après une revue de la littérature, les auteurs montrent une interaction entre les conditions de stress et de temps, où l'incidence et la fréquence du bâillement sont plus faibles immédiatement après le stress et plus fréquents à distance. Ces résultats confirment l'analogie des effets du stress physique sur le bâillement des oiseaux et des mammifères. Celui-ci pourrait être lié à une fonction de thermorégulation et de stimulation de la vigilance d'après ces auteurs qui ne mentionnent pas la nature parasympathique du bâillement opposé au stress de nature adrénergique.
 
 
Introduction
 
Yawning is characterized by a powerful gaping of the jaw with inspiration, following by a brief period of muscle contraction and a passive closure of the jaw with expiration (Barbizet 1958). Phylogenetically old, yawns or similar yawn-like mandibular gaping patterns have been observed across vertebrate classes (e.g., Baenninger 1987). Numerous hypotheses have been proposed to explain the adaptive function of yawning (Smith 1999), and this topic is still debated (Guggisberg et al. 2010; Gallup 2011). To date, however, empirical investigations primarily support a role of yawning in promoting arousal and state change (Baenninger 1997; Provine 1986, 2005; Vick and Paukner 2010; Walusinski 2006) through enhanced intracranial circulation and brain cooling (Gallup and Gallup 2007; Shoup-Knox et al. 2010; Walusinski 2014). Consistent with this view, a growing number of studies have documented a close connection between yawning and various stressors across diverse species of mammals and birds. Research on non-human primates indicates that yawning tends to increase during periods of psychosocial stress (Maestripieri et al. 1992). In particular, various studies have documented that yawns occur during antagonist interactions and hostile social situations (Macaca nigra, Hadidian 1980; Theropithacus gelada, Leone et al. 2014), whereby dominant males perform directed threat yawns with canine displays and subordinates may yawn in response to the stressful interaction (Cercocebus albigena and Macaca fascicularis, Deputte 1994; Macaca fascicularis and Macaca fuscata, Troisi et al. 1990; Redican 1982).
 
However, unlike ordinary yawns (see definition above), the display yawner rather than closing their eyes at the peak of the yawn, fixes their attention on the target during the yawning episode to monitor the effect of the threat. These social displays are typically documented among non-human primate species with sexual dimorphism in body size, canine size, and aggressive competition, and were first described by Charles Darwin in The Expression of the Emotions in Man and Animals (Darwin 1872). Importantly, directed threat yawns appear to be fundamentally different from more ubiquitous forms of yawning related to transitions in arousal, and the sex differences in yawn frequency among primates are lost within species with limited sexual dimorphism in canine size (Homo sapiens, Schino and Aureli 1989; Pan troglodytes, Vick and Paukner 2010). Nonetheless, spontaneous yawns have also been linked with more general social and environmental stressors in primates.
 
A study on the behavioral responses of female olive baboons (Papio anubis) showed that the mere presence of a dominant conspecific increased yawning rates by 40% in comparison to when the nearest neighbor was a subordinate (Castles et al. 1999). Similarly, chimpanzees (Pan troglodytes) in the wild have been observed to yawn more frequently when in the presence of humans (Goodall 1968). Chimpanzees in captivity have also been shown to increase spontaneous yawning and self-directed behaviors following vocalizations and noisy displays from neighboring groups of conspecifics, prompting the interpretation of yawning as a behavioral indicator of anxiety in this species (Baker and Aureli 1997). Stress also appears to influence the temporal expression of this response among bonobos (Pan paniscus), with spontaneous yawns occurring at highest frequency during non-stressful situations and being least frequent during periods immediately following social stress (Demuru and Palagi 2012). Furthermore, non-social stressors have been documented to elicit spontaneous yawning in other primates, including grey-cheeked mangabeys (Cercocebus albigena) and, most recently, lemurs (Lemur catta) (Zannella et al. 2015). Specifically, yawns in these species tend to increase following alarm calling in response to predators or after predatory attacks or aggression.
 
Yawning has been implicated as a behavioral sign of stress and anxiety across other mammals as well. For example, one study reported that yawning increased in frequency among wild horses following aggressive behaviors in semi-natural conditions (Górecka-Bruzda et al. 2016). Another recent study investigating the effects of noseband tightening on horse behavior found that heart rate and eye temperature rose significantly during the tightest condition, and that following the removal of the bands yawn frequency increased (Fenner et al. 2016). Furthermore, a mild rise in yawning has been observed among domesticated dogs following certain stressful stimuli (Beerda et al. 1998), leading to various investigations of yawning as a behavioral measure of anxiety. However, the evidence connecting yawning and stress in dogs is mixed, with subsequent studies providing limited support for changes in yawn behavior following various stressful conditions in dogs (e.g., Dreschel and Granger 2005; Hennessy et al. 1998; Part et al. 2014; Schilder and van der Borg 2004). Furthermore, less than 10% of owners identify yawning as a marker of stress in their own pets (Mariti et al. 2012).
 
Controlled laboratory experiments on rodents have allowed researchers to further examine a potential causal link between stressors and the expression of yawning. For example, a recent study demonstrated that classical fear conditioning trials reliably induced yawning, along with anxiety-related behavior and activity in the central nucleus of the amygdala among male Wistar rats (Kubota et al. 2014). A separate study revealed that the repeated witnessing of painful shocks delivered to conspecifics increased yawning frequency in male Long-Evans rats (Carrillo et al. 2015). This report also showed that the heightened yawning following the observation of pain in others was effectively inhibited by metyrapone, an anti-stress drug and glucocorticoid synthesis blocker, providing further support that yawns were an affective response to the repeated observation of distress in others. Other work has shown that adrenalectomy, which stops the production of glucocorticoids, abolished yawning in male Winstar rats (Anías-Calderón et al. 2004). This same study also demonstrated that the administration of a synthetic glucocorticoid, dexamethasone, restored yawning within the same adrenalectomized rats. An increase in yawning has also been documented following rapid rises in ambient temperature that produce thermal stress in Sprague Dawley rats (Gallup et al. 2011). Furthermore, studies have shown that the pattern of physical stressors experienced by rats modulates the expression of yawning. For example, constant swimming and foot shock stressors appear to inhibit drug-induced yawning in albino Wistar rats, while exposure to the same stressors at an intermittent basis significantly increased this response (Tufik et al. 1995). Similarly, experiments on Sprague Dawley rats showed that experiencing foot-shocks at fixed 10-min intervals produced a gradual increase in yawning that peaked at 40-min, while yawning was less pronounced when rats experienced foot shocks at random levels (Moyaho and Valencia 2002).
 
Comparative experiments in birds have shown similar findings pertaining to yawning and stress, both in relation to frequency and temporal effects. In a series of experiments designed to induce thermal stress in captive budgerigars (Melosittacus undulatus), increases in yawning were reliably produced by rapid rises in ambient temperature within a thermal chamber (Gallup et al. 2009, 2010). The pattern of yawning has also been measured in this species following a 4-min handling stressor, which simulates a predator encounter and produces a significant physiological stressor as measured by rises in body temperature (Miller et al. 2010). Within this study it was shown that, in comparison to a control condition, handling significantly modulated the temporal expression of yawning following the encounter (Miller et al. 2010). In particular, yawns were initially inhibited after release (~1.5 yawns/h), but were then potentiated 20&endash;40-min thereafter (>5 yawns/h). A follow-up study also using budgerigars examined the effects of a non-specific stressor, a loud white noise that elicited clear startle responses, on yawn frequency within small groups (Miller et al. 2012). In comparison to handling stress, the loud noise did not produce the same immediate reduction in yawning, but a similar increase in the frequency of this response occurred 20-min thereafter. A more recent paper documents similar temporal effects of stressors on yawning in wild Nadza boobies (Sula granti) (Liang et al. 2015). In the first of two studies, yawning was measured in adult birds during and after an extended human capture-restraint stressor that produces a rise in corticosterone. Consistent with other studies, yawns were absent during the stressor itself, and remained at low frequency from 0 to 30-min following release before significantly climbing in rate 30&endash;60-min thereafter. In the second study, the researchers simply observed behavioral responses of Nadza booby nestlings following maltreatment of non-parental adults. None of the nestlings yawned during the stressful event itself, but nearly every nestling yawned within 15-min afterwards.
 
Overall, a large and growing comparative literature on diverse species of mammals and birds generally implicates stress as a trigger for overall increases in yawning, but that one-time acute physical stressors appear to initially inhibit, then subsequently potentiate this response. The physiological effects of stress are diverse, with a number of components involved in the stress system that lead to behavioral and peripheral changes that function to equilibrate homeostasis and adaptive outcomes (Tsigos and Chrousos 2002). The stress response consists of two major components 1) the locus coeruleus/norandrenergic (LC/NE) sympathetic nervous system (SNS) pathway which releases norepinephrine from the adrenal medulla immediately after stress (Itoi and Sugimoto 2010) and 2) the hypothalamic-pituitary-adrenal (HPA) axis whose end product is cortisol which is released from the adrenal cortex at peak levels approximately 20 min after the cessation of a stressor (Spencer and Deak 2016). Stress also produces rises in body temperature (e.g., Zethof et al. 1994, 1995; Van der Heyden et al. 1997; Olivier et al. 2003), which could be a result of hyperthermia or fever. Hyperthermic responses from stress could occur from increased locomotor or muscular activity and cutaneous vasoconstriction, while fever would be a consequence of a raised thermoregulatory set point (Oka et al. 2001).
 
Although yawning has been associated with stress in humans, and even hypothesized to be linked with rises in cortisol (see Thompson Cortisol Hypothesis, e.g., Thompson 2011), to this point the connection has only been indirect. For example, increased yawning in humans has been noted prior to prolonged stressful or anxiety provoking situations, such as among Olympians immediately prior to competition, musicians waiting to perform, and paratroopers leading up to their first free-fall (Provine 2005). Frequent yawning has also been documented among individuals with some anxiety disorders (Daquin et al. 2001), as well as a variety medical conditions and neurological diseases (Gallup and Gallup 2008; Walusinski 2009). One study even found that a small proportion of college students self-reported that stressful situations are conducive to yawning (Greco et al. 1993). To date, however, we are unaware of any experimental studies assessing this relationship.
 
Here, we describe the results of an experiment investigating how the direct manipulation of an acute physical stressor alters the frequency and temporal expression of yawning among human participants in the laboratory. In particular, we examined how the cold pressor test (CPT), which included the immersion of the non-dominant hand into ice water (2-4 °C) for at least 60-s, alters yawning in comparison to a control condition (immersion into room temperature water 20- 22 °C) at distinct time intervals: immediately following the test and 20-min thereafter. As a physical stressor, the CPT task is more likely to preferentially activate early autonomic (LC/NE) stress pathways over later-responding psychological (HPA) stress pathways; however, these systems are largely interconnected with a large degree of cross-activation. Accordingly, the CPT has been shown to not only increase a biomarker (Banks et al. 2014) and peripheral measures of autonomic arousal (Schwabe et al. 2008), but to also increase cortisol levels with peak activity occurring after a delay (10 min post-stress) (Alomari et al. 2015; Schwabe et al. 2008; Viena et al. 2012). Consistent with previously documented temporal effects following physical stressors in horses (Fenner et al. 2016), rats (Moyaho and Valencia 2002) and birds (Miller et al. 2010, 2012; Liang et al. 2015), we hypothesized that yawning would increase following the CPT, but only in the delayed condition. Because yawning has been documented to be relatively infrequent among participants in laboratory research (Baenninger and Greco 1991), contagious yawning was used as a proxy for spontaneous yawning in this experiment. Contagious yawns appear indistinguishable from spontaneous yawns aside from their triggers (i.e., social vs. physiological), and contagious yawning can be easily manipulated under laboratory conditions (e.g., Platek et al. 2003). Furthermore, growing research shows that physiological variables that alter spontaneous yawn frequency (i.e., those that influence brain and body temperature) have the same effects on yawn contagion, suggesting that both yawn types share fundamental mechanistic pathways (Gallup and Gallup 2007; Gallup and Gallup 2010; Gallup 2016).
 
Discussion
 
This is the first experiment, to our knowledge, to directly assess the effects of stress on yawning in humans. Consistent with the comparative literature, we demonstrated that an acute physical stressor significantly modulated this response among participants in the laboratory. Although brief ice water immersion of the non-dominant hand (CPT) did not produce an overall increase in the proportion or frequency of yawning, it did alter the time course of its expression. Specifically, we show that within the CPT condition self-reported contagious yawns occur at relatively low frequency immediately following exposure to the stressor, but then increase 20-min thereafter. These findings are similar to previous results reported in rats, horses and bonobos (Moyaho and Valencia 2002; Fenner et al. 2016; Demuru and Palagi 2012), and specifically match recently documented effects resulting from handling and capture restraint stress in two bird species (Miller et al. 2010; Liang et al. 2015).
 
There is growing evidence indicating that the motor action pattern of yawning functions to cool the brain through increased intracranial circulation and countercurrent heat exchange with the ambient air (reviewed by Gallup and Gallup 2008; Gallup and Eldakar 2013). For example, predicted patterns of brain/skull temperature change surround yawns in rats (Shoup-Knox et al. 2010) and humans (Gallup and Gallup 2010), and experimentally manipulated behavioral brain cooling mechanisms diminish spontaneous and contagious yawn frequency among human participants in the laboratory (Gallup and Gallup 2007; Gallup and Gallup 2010). Further support for this hypothesis comes from the repeated demonstration that spontaneous and contagious yawn frequency can be effectively increased or diminished as a function of ambient temperature manipulation and variation across diverse species (Gallup et al. 2009, 2010, 2011; Gallup and Eldakar 2011; Massen et al. 2014; Eldakar et al. 2015; for a review see Gallup 2016), as well as the close connection between yawning and thermoregulatory dysfunction (Gallup and Gallup 2008). Stress-induced increases in yawning behavior may reflect LC/NE activation since activation of this system quickly elevates core body temperature (Chrousos 1998).
 
Different explanations have been posited to explain the increase in body temperature following stress. For example, the central autonomic ganglia that are activated as part of the LC/NE stress response trigger a widespread cascade of Bfight or flight^ responses that could produce hyperthermia due to increased muscular activity and cutaneous vasoconstriction. Alternatively, research indicates that stress-induced rises in temperature could also result from a febrile response due to prostaglandin E2-dependent and 5- HT-mediated mechanisms (Oka et al. 2001). Although we did not obtain physiological measures in the current study, the CPT is a physical stressor that clearly reduces skin temperature of the submerged hand (Brusselmans et al. 2015). Despite this localized reduction, the CPT produces vasoconstriction and has been shown to result in an associated rise in the skin temperature of the non-cold exposed hand (Frank and Raja 1994).
 
However, other studies show either no rise in skin temperature (Edelson and Robertson 1986;Washington et al. 2000) or even a decrease in skin temperature in spite of concomitantly measured vasoconstriction (Watson and Nance 1994). This apparently contradictory relationship can be explained by a cold-induced constriction of hand arterioles that can produce a redirection of blood through arteriovenous anastomoses (AVA) resulting in heat loss from the skin surface despite a rosy skin appearance caused by constriction of the AVA (Chwa_czy_ska et al. 2015; Mizeva et al. 2015; Walløe 2016). Accordingly, we argue that either model of stress-induced temperature elevation can effectively explain the temporal pattern of yawning witnessed here. In terms of explaining the hyperthermic response, animals would need to balance the cost/benefit trade-offs associated with yawning immediately following stressful situations. For example, previous research on budgerigars suggested that the initial suppression of yawns following handing restraint might adaptively reduce attention-getting movements and promote effective antipredatory behaviors (Miller et al. 2010).
 
However, birds in that study showing the greatest increases in body temperature after handling yawned sooner following release. Furthermore, stress produces increases in heart rate and blood pressure and adaptive behavioral changes for heightening arousal, alertness and vigilance (Chrousos 1998), which would effectively inhibit the natural mechanisms triggering yawns (Baenninger 1997; Gallup and Gallup 2007). Following a brief recovery period, however, an increase in yawning may reflect a mechanism to provide thermoregulatory benefits and effectively maintain waning vigilance and arousal when external threats have subsided and the environment becomes more predictable. Alternatively, if the CPT stress induced a fever through a rise in the thermoregulatory set point, thermoregulatory warming mechanisms would be triggered initially and cooling mechanisms would be inhibited. Following the removal of the stressor and reduced febrile response over time, the thermoregulatory set point would then be reduced, and cooling mechanisms, such as yawning, would be activated to promote thermal homeostasis. These effects on yawn frequency and fever have previously been described for the use of antipyretics (Gallup and Gallup 2013). Other evolutionary explanations for the previously observed temporal effects on yawn expression following stress in birds include communicating and signaling arousal reduction to group members (Guggisberg et al. 2010; Liang et al. 2015). Multiple functions are possible, whereby yawning could provide thermoregulatory benefits and serve as a signal to conspecifics. However, aside from direct threat yawns with canine displays in non-human primates, there is currently no evidence that yawns provide a meaningful signal to receivers (see Gallup and Clark 2015). For example, group members do not appear to orient towards or respond to yawns of others, and it is not clear what communicative benefits there would be to yawning. Although contagious yawns are inherently social, in that sensing yawns in others triggers them, this does not mean the action pattern actually communicates anything. Furthermore, since yawns occur under a variety of contexts outside of stress (i.e., during changes in arousal and important events, before and after sleep, during boredom, transitions in activity patterns), any signal that is displayed remains nonspecific (Gallup 2011). Therefore, experimental research is needed to test the predictions of social-communication hypotheses.
 
The results reported here could also be interpreted under the recent Thompson Cortisol Hypothesis (Thompson 2011), which posits that yawns are triggered due to rises in cortisol. While this hypothesis may not serve as a global explanation for all forms of yawning, it could provide insight into the specific association between yawning and stress. In particular, the 20-min delay in yawn enhancement following the CPT is consistent with the temporal rises of cortisol observed following stress in humans (Alomari et al. 2015; Cornelisse et al. 2011; Klopp et al. 2012). However, it is important to note that elevations in cortisol resulting from the CPT are relatively low when compared to other tests (reviewed by Schwabe et al. 2008). It is possible that cortisol is not the direct mediator of the stress-induced yawning response since the activity of cortisol as part of the delayed stress response recruits, and is co-activated with, a host of many neuromodulators (e.g. serotonin, dopamine) and induces paracrine adrenal signaling that potentially also influences stress-induced changes in neural processing involved in the yawning response. In addition, results from experiments designed to test the Thompson Cortisol Hypothesis have consistently showed that rises in cortisol among human subjects occur both among those that yawn and do not yawn under normal laboratory conditions (Thompson and Bishop 2012; Thompson et al. 2014a, 2014b). This reproducible effect, i.e., that rises in cortisol occur independent of yawning, indicates that cortisol does not serve as a primary mechanism for triggering this response.
 
The current findings add to the comparative literature on stress and yawning, and provide the first direct experimental demonstration of stress-induced changes in yawning in humans. However, there are some limitations to the current study that should be acknowledged. For one, the subjective nature of yawning may have increased the chances of measurement error, though we have no a priori reason to believe evaluations of yawning would be biased as a function of these conditions and previous research indicates a strong congruence between self-report and objective measures of yawning under similar laboratory settings (Gallup and Church 2015; Massen et al. 2015).
 
Follow-up experiments could obtain video recordings of participants during and after stress to measure both spontaneous and contagious yawns, which would allow for more detailed analyses such as how stress modulates yawn latency or duration (Gallup et al. 2016b). Another weakness to the current study is that no physiological or subjective measures of stress were recorded, which limits our interpretation of the yawning response. However, our previous work, which used the same CPT procedures as the present study, has showed increased cortisol after CPT induction with maximal concentration 30 min post-CPT (Alomari et al. 2015). We recognize that the CPT is only one of many possible stressors that could be applied within a laboratory setting, and may produce a greater physical rather than psychological stress response. Given that yawning has also been documented to occur prior to some stressful and anxietyprovoking situations in humans (Provine 2005), future research should examine how the temporal expression of this response varies as a function of different forms of psychosocial and physical stress. Furthermore, follow-up studies should include selfreport surveys to assess participants' subjective perception to the stressor. In combination these measures could be useful to analyze inter-individual variation in physiological and behavioral responses to stressful manipulations.
 
Understanding the role of yawning in relation to behavioral and physiological symptoms of stress may provide further insights into the latency and degree of eventual recovery from stressful encounters. The temporal changes in human yawning following the CPT reported here (i.e., an initial inhibition followed by an enhancement) mirror recently documented effects in budgerigars and Nadza boobies, suggesting a potential evolutionarily conserved and homologous behavioral/physiological response to onetime acute physical stressors across birds and mammals. In terms of an ultimate functionality, this observed pattern is consistent with previous research supporting an adaptive thermoregulatory and arousal response, though future experimental research could explore a potential signaling function to stress-induced changes in yawning among humans and other animals.