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Fetal yawning assessed by 3D and 4D sonography
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19 janvier 2017
BMC Neurosci
2017;18(1):3
Yawning reduces facial temperature
in the high-yawning subline of Sprague-Dawley rats  
Eguibar JR, Uribe CA, Cortes C, Bautista A, Gallup AC.

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Abstract
Background
Yawning is a stereotyped behavior that enhances blood flow to the skull, and the resulting counterflow has been hypothesized as a mechanism for brain cooling. Studies have shown that yawns are strongly associated with physiological and pathological conditions that increase brain temperature, and that they are followed by equivalent decreases in brain temperature. However, measured reductions in cranial or facial temperatures following yawning have yet to be reported, to our knowledge. To accomplish this, we used a subline of Sprague-Dawley rats that yawn at a much greater rate (20 yawns/h) than do outbred Sprague-Dawley rats (2 yawns/h).
 
Results
Using an infrared camera, we effectively evaluated thermal changes in the cornea and concha of these rats before, during, and after yawns. The maximum temperature in both regions significantly decreased 10 s following yawns (concha: _0.3 °C, cornea: _0.4 °C), with a return to basal temperatures after 20 s.
 
Conclusions
This study is the first clear demonstration of yawning-induced thermal cooling on the surface of the face, providing convergent evidence that this behavior plays a functional role in thermoregulation. As other studies have demonstrated that yawning is capable of reducing cortical brain temperature, our current data support the idea that yawning functions as a thermoregulator, affecting all structures within the head.
 
Thanks to J.R. Eguibar for the picture
 
 Background
 
Yawning is an innate behavior characterized by a stereotyped motor pattern. Wide opening of the mouth and wide dilation of the pharynx and larynx is followed by deep inspiration that ends abruptly with a short expiration. Neck musculature then shrinks and returns to basal levels [1, 2]. Understanding the physiological significance of yawning is important because spontaneous yawning is ubiquitous in vertebrates [3], with reports identifying atypical yawning as a symptom or side-effect of several neurological diseases or medications [4]. Many hypotheses have been proposed regarding the potential physiological functions of yawning; however, they often lack clear physiological evidence [5]. While much of the scientific community believed that yawns serve a respiratory function, experimental procedures performed on humans have demonstrated that yawning and breathing are controlled by separate mechanisms [6]. However, other causes such as fatigue, boredom, and sleepiness have been proposed as causes of increased yawning frequency [4]. One recent theory that has gained recent experimental support proposes that yawning is a brain cooling mechanism [7&endash;9].
 
In homeotherms, brain temperature is determined by three variables: the rate of arterial blood flow, the temperature of arterial blood, and the amount of metabolic heat production [10]. The physical action of yawning can alter the first two variables. Yawning produces significant changes in circulation, including accelerating heart rate by up to 10 additional beats per minute [11, 12]. The deep inhalation and powerful jaw stretching during a yawn also favors increases in blood flow to the skull [13], and the extended contraction of the lateral pterygoid muscle during yawning acts to squeeze blood from the associated plexus [14]. Therefore, the gaping of the jaw and deep inhalation increase arterial blood flow to the brain and enhance venous return, thus acting to remove hyperthermic blood from the skull and simultaneously introduce cooler blood coming from the lungs and extremities. Increased facial blood circulation and associated changes in the ventilation rate are two well-known mechanisms that cool brain temperature [15, 16].
 
The deep inhalation of air that accompanies yawning may also provide counter-current heat exchange by cooling venous blood draining from the nasal and oral orifices that is in close contact with arterial blood supply [16]. Consistent with this view, recent studies in human and non-human primates [8, 17] have shown that pharyngeal cooling rapidly and selectively decreases brain and tympanic temperature by cooling the carotid arteries [17]. Furthermore, anatomical investigations in humans have revealed that the thin sinus walls flex when pterygoid musculature contracts during yawning, indicating that the posterior wall of the maxillary sinus serves as an origin for both medial and lateral pterygoid muscle segments [18]. This powerful flexing of the sinus walls has been proposed to ventilate the human sinus system similarly to what occurs in birds [19], providing a second mechanism through which yawning functions in human cerebral cooling. Accordingly, yawning could reduce brain temperature by ventilating the sinus system and promoting the evaporation of the sinus mucosa [20]. The salivation and tearing that accompany yawning could be a third mechanism for cooling, aiding in heat loss through evaporation [8].
 
Importantly, yawning appears to be constrained to a narrow range of ambient temperature (i.e., a thermal window). Numerous reports have confirmed and replicated the specific thermal window for various species. For heat to dissipate; ambient temperatures must be lower than the body temperature of the subject animal. Thus, as predicted, in warmer environmental situations, yawning did not cool the brain [7&endash;9, 20]. Consistent with models of thermoregulation, variation in ambient temperature elicits predicted fluctuations in yawning frequency in a number of species, including budgerigars [21], rats [22], white-faced capuchin monkeys [23], and humans [20, 24].
 
Initial rises in temperature within this window trigger yawning and other thermoregulatory cooling mechanisms such as panting and behavioral adjustments to reach thermoneutralization. However, as external temperatures continue to rise beyond the thermal window, yawning decreases because counter-current heat exchange becomes less effective. Similarly, yawning is also reduced at extremely cold temperatures, as thermoregulatory cooling responses are no longer necessary [24].
 
Direct measures of internal temperature in rats and humans have shown that brain and oral temperature rise immediately before the onset of yawns, with corresponding decreases in temperature being observed directly following these events [9, 25]. One interpretation is that yawns are triggered by elevated temperature inside the skull, and that the physiological consequences of yawning discussed above result in temperature reduction. Consistent with this view, heightened core body temperature following handling-stress has been shown to be correlated with earlier onset and higher frequency of yawning in birds [26], and experimental manipulations designed to promote brain cooling have been shown to diminish yawning frequency in humans [7]. Furthermore, a number of medical conditions and drugs affect yawning and brain/core temperature in reciprocal patterns. Conditions associated with rises in temperature present with increased yawning, while those associated with lower temperatures present with diminished yawning [8]. However, whether yawning reduces the temperature on the surface of the head or in the face remains unclear.
 
Selective breeding of Sprague-Dawley rats has generated a subline with a higher incidence of spontaneous yawning [27], which is a useful tool for the physiological study of yawning. Yawning frequency (20 yawns/h) in these high-yawning (HY) rats is an order of magnitude higher than in other Sprague-Dawley rats (2 yawns/h) [27&endash;29]. Thus, HY animals allow us an efficient means to evaluate internal and environmental variables that modulate yawning frequency. Indeed, HY rats were used to determine that yawning has a circadian oscillation pattern that includes significantly increased yawning frequency when transitioning from light periods to dark periods [30]. Under constant light conditions, the circadian rhythm of yawning is disorganized, suggesting that this behavior is not endogenously generated [31]. However, restricting food access to just 2 h per day produced a highly significant increase in yawning frequency. This is because food access can be a predictor of food availability and can produce an anticipatory yawning peak [31].
 
High-yawning rats allow us to analyze the role of smell on contagious yawning [32]. HY rats are also more sensitive to cholinergic and dopaminergic agents that increase yawning frequency [33, 34], and to adrenocorticotrophic hormones and oxytocin neuropeptides [29, 35], indicating a higher sensitivity of these sublines to environmentally and pharmacologically induced yawning.
 
Based on past findings regarding yawning and thermoregulation, the present study used a thermographic imaging camera to measure temperature changes associated with spontaneous yawning that occurred in the cornea and concha of HY rats. The concha is a good candidate structure because the ears dissipate more heat than other head regions and act as a thermal buffer mechanism in many mammalian species. Similar structures such as the cornea play critical roles in thermoregulation, and are frequently called thermal dissipaters because they are responsible for heat exchange and they regulate surface temperature [36, 37].
 
During yawning, the upper airways are ventilated, and this possibly cools the blood in the facial artery, which travels around the mouth and nasal cavities, making terminations around the eye and cooling these structures [7]. Thus, the two anatomical areas that we selected are good candidates for directly detecting temperature change in areas not covered by fur.
 
 
Discussion
 
The use of infrared thermal imaging provides an effective means of tracking behavioral thermoregulation through changes in surface temperature [36, 37]. This is the first study to document fluctuations in facial temperature that are temporally locked to yawning, revealing that temperatures in the cornea and concha consistently rise leading up to yawning events as shown in Fig. 5b (_10 s) and then decrease below baseline levels shortly thereafter (10 s). These results are consistent with previous research measuring changes in brain temperature surrounding yawns in rats [25], and provide further evidence supporting the idea that yawning functions to cool the head and cortical surface [7&endash;9].
 
Previous reports indicate that yawns are triggered by rises in brain and body temperature [21, 25, 38], which is consistent with the pattern of temperature change we observed preceding yawns. This is illustrated in Fig. 5b, in which 10 s before a yawn occurs, there is a small increase in the concha temperature that drops significantly during and 10 s after yawning. This is likely because this area is more exposed to thermal influences, as has already been demonstrated in other species [36, 37]. Because rat brain temperature is consistently higher than that of the arterial blood supplying the brain [39], increases in arterial blood flow and enhanced venous return that result from the act of yawning (i.e., wide opening of the mouth and deep inhalation) could explain the cooling we observed within 10 s of yawning. Heat convection by blood depends on several variables, including the volume and velocity of blood flow in the vessels [40]. For example, increased blood-flow velocity can result in a twofold increase in heat transmission by tissue [41], and specific reductions in brain temperature have been observed because of increased localized blood flow [42]. Therefore, the decreased temperatures that we observed at the corneal and conchal surfaces are consistent with various models of bio-heat transfer that take perfusion rates into account [43&endash;46].
 
We must emphasize that the main heat regulator in rats and mice is the tail. However, facial surface area is also a well-known heat dissipater [47, 48]. Indeed, in humans, the eyeball&emdash;and in particular the cornea, iris, and sclera&emdash;are structures with high temperature conductivity because they often have higher temperatures than the environment [49]. Therefore, these eye structures function as thermal dissipaters that work through heat convection, and even evaporation, because tears allow the transmission of heat from inside the cranium to the surface of the eye [49].
 
The decreases in surface temperature at the cornea and concha sites correspond with previously documented changes in brain-tissue temperature following yawning events in rats. Shoup-Knox et al. [25] showed that temperature in the prelimbic cortex rise sharply just before yawns and then begin to drop after about 18 s, with maximum cooling occurring at about 60 s following this transition. This time course is much longer than what we observed externally on the eye and the ear, and metabolic heat production from neuronal activity inside the skull should interact with other structures and blood flow that can be responsible, at least in part, for the delayed responses. Together, these observations provide a consistent timeline for a functional role of yawning in cooling the brain, with temperature reductions at external surfaces preceding those at internal brain tissue. It is valid, therefore, to mention that both phenomena share common mechanisms and are temporally linked. Additional experiments are necessary to establish a causal relationship.
 
Cooling of external surfaces in the head might also contribute to cooling of internal tissues. In humans, the ophthalmic vein, like other emissary veins, has been reported to play an important role in cerebral cooling and may even reverse blood flow depending on the temperature conditions of the environment. Therefore, during hypothermia, blood travels from the brain to the surface of the face, whereas during hyperthermia the opposite pattern occurs [50]. Because yawning in rats and humans has already been demonstrated to be triggered by increases in brain and oral temperature [25, 38], cooling of external surfaces such as the eye and ear could directly alter brain temperature. Our observations of a mean reduction of _0.32 °C in the cornea and _0.48 °C in the concha are consistent with the reduction of just over _0.11 °C in the cerebral cortex of rats following yawns observed in a previous study [25]. The differences can be explained by the heat gain/loss ratio that follows circulation in blood vessels, as well as by differences in the quantity of blood supply to the brain and face, which are governed by different vascular tones and by evaporation in the paranasal sinuses [51]. Importantly, the corneal surface immediately returned to pre-yawning temperatures because blood in the ophthalmic artery carries heat continuously from inside the cranium, and in the case of the concha, heat-loss primarily results from convection and conduction mechanisms.
 
Importantly, Sato-Suzuki et al. [52] showed that chemical or electrical stimulation of the paraventricular nucleus of the hypothalamus evoked yawning and shifted EEG activity from delta to theta rhythms. They also showed an association between a drop in blood pressure and skin conductance supporting changes in the sympathetic inhibitory responses. Our results showed changes in the temperature of facial structures due to changes in the blood flow to the head. These changes are closely associated with the loss of heat in the oropharynx due to air flow, and support the validity of the thermoregulatory role of yawning.
 
Conclusion
 
Our results are consistent with a growing number of comparative studies supporting the thermoregulatory theory of yawning [9]. The use of HY rats in this study provides an effective sample population for this investigation because of their high frequency of spontaneous yawning. However, further studies using similar thermal imaging techniques are needed to replicate these findings in other lines or species with more typical yawning patterns.