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13 mai 2007
www.epjournal.net
2007;5(1):92-101
Yawning as a brain cooling mechanism: nasal breathing and forehead cooling diminish the incidence of contagious yawning
Andrew C. Gallup, Gordon G. Gallup Jr
Department of Psychology
State University of New York at Albany, Albany, USA.

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Read objections and review and letter 73
 
Andrew C. Gallup. Yawning and the thermoregulatory hypothesis
 
Abstract: We conducted two experiments that implicate yawning as a thermoregulatory mechanism. The first experiment demonstrates that different patterns of breathing influence susceptibility to contagious yawning. When participants were not directed how to breathe or were instructed to breathe orally (inhaling and exhaling through their mouth), the incidence of contagious yawning in response to seeing videotapes of people yawning was about 48%. When instructed to breathe nasally (inhaling and exhaling through their nose), no participants exhibited contagious yawning. In a second experiment, applying temperature packs to the forehead also influenced the incidence of contagious yawning. When participants held a warm pack (460C) or a pack at room temperature to their forehead while watching people yawn, contagious yawning occurred 41% of the time. When participants held a cold pack (40C) to their forehead, contagious yawning dropped to 9%. These findings suggest that yawning has an adaptive/functional component that it is not merely the derivative of selection for other forms of behavior.
 
Introduction
Yawning is characterized by gaping of the mouth accompanied by a long inspiration followed by a shorter expiration. In humans, yawning begins in utero by 20 weeks gestation (Sherer, Smith, and Abramowicz, 1991) and continues throughout life. People typically close their eyes at the peak of a yawn, and a single yawn can last for as long as 10 seconds (Daquin, Micallef, and Blin, 2001). Yawning is commonly accompanied by stretching and occurs most frequently before sleep and after waking (Provine, Hamernik, and Curchack, 1987). Yawning has long been associated with boredom and sleep. Under laboratory conditions subjects yawn more frequently after watching uninteresting color patterns than music videos (Provine and Hamernik, 1986). Yawning is widespread and has been recorded in many vertebrates (Baenninger, 1987). In some primates there is a special category of yawning that functions as a threat display (Hinde and Tinbergen, 1958; Tinbergen, 1952). Display yawns expose canine teeth, and unlike normal yawns the yawner keeps their eyes open during the yawning episode to monitor the effect of the yawn on the target subject.
 
Yawning is under the central control of several neurotransmitters and neuropeptides including dopamine, excitatory amino acids, acetylcholine, serotonin, nitric oxide, adrenocorticotropic hormone-related peptides and oxytocin (Argiolas and Melis, 1998). Yawning can be drug-induced, and drugs are especially effective when injections are made into the hypothalamus (Dourish and Cooper, 1990). Apomorphine injections have been reported to produce drug-induced yawning along with penile erection in male mice (Melis, Argiolas, and Gessa, 1987). There have been many attempts to identify the function(s) of yawning in humans (Smith, 1999). However, the adaptive/functional/biological significance of yawning has yet to be established (Provine, 2005). It has long been thought (and is still commonly misconstrued) that the function of a yawn is to increase O2 levels in the blood. However, breathing increased levels of oxygen or carbon dioxide do not affect yawning (Provine, Tate, and Geldmacher, 1987). Yawning is contagious. Seeing, hearing, thinking or reading about yawning can trigger yawns, and attempts to shield a yawn do not stop its contagion (Provine, 2005). Under laboratory conditions, slightly less than half of college students yawn contagiously, and individual differences in susceptibility to contagious yawning have been shown to be related to differences in processing information about oneself (Platek, Critton, Myers, and Gallup, 2003). Witnessing people yawn activates parts of the brain also associated with self-processing (Platek, Mohamed, and Gallup, 2005).
 
Here we investigate the physiological significance of yawning in humans, specifically whether yawning may function as a thermoregulatory mechanism. We propose that yawning serves to keep the brain in thermal homeostasis, and that yawning serves to maintain optimal mental efficiency. We believe that yawning serves as a compensatory cooling mechanism when regulatory mechanisms fail to operate favorably. In order to test this hypothesis, we conducted two separate experiments designed to indirectly manipulate brain temperature. Based on evidence supporting the selective brain cooling model (du Boulay, Lawton, and Wallis, 2000; Mariak, White, Lewko, Lyson, and Piekarski, 1999; Zenker and Kubik, 1996; Falk, 1990; Cabanac, 1986; Cabanac and Caputa, 1979), we choose to manipulate breathing conditions and forehead temperature by noninvasive means. Nasal breathing (du Boulay, Lawton, and Wallis, 2000; Mariak et al., 1999) and forehead cooling (Zenker and Kubik, 1996; Cabanac, 1986) have been shown to be involved in the thermoregulation (cooling) of the brain. Contagious yawning was used as a proxy for yawning in both these experiments for two reasons. Contagious yawning is indistinguishable from spontaneous yawning aside from the fact that the triggers differ, and contagious yawning can be manipulated under laboratory conditions (e.g., Platek et al., 2003).
 
Experiment 1: Breathing Manipulation
The first experiment investigated whether different methods of breathing would affect the occurrence of contagious yawning, and was approved by the local Institutional Review Board. Breathing was the focus of this experiment because of its influence on brain temperature (du Boulay, Lawton and Wallis, 2000; Mariak et al, 1999).
 
Methods
Participants Participants were 44 undergraduate students at the University of Albany. Twenty-seven participants were male and 17 were female, and all were eighteen to twenty-five years of age.
 
Procedure Each participant signed a consent form, and was asked to step into a room and sit by themselves in front of a computer screen. Each participant was then instructed to either inhale and exhale strictly orally, strictly nasally, strictly orally while wearing a nose plug, or allowed to breathe normally (i.e., not instructed how to breathe) during the experiment. Eleven participants were randomly assigned to each of the four breathing conditions. Participants were told to breathe in the manner instructed for a period of two minutes prior to and while watching a brief video tape lasting two minutes and fifty seconds. This same video was used in a previous contagious yawning study by Platek et al. (2003).
 
The video consisted of 24 7-s digital videos of eight volunteers (four male, four female), each depicting three separate conditions (neutral, laughing or yawning). These videos were presented in random order on the computer screen to each participant using Microsoft Media Player. Each participant was observed through a one-way mirror by a researcher who recorded their yawns. At the conclusion of the video presentation, participants were asked whether they had yawned during the experiment. Two of the participants (one in the oral group and one in the normal breathing group) who did not show detectable signs of a yawn, each reported yawning once. These self-reported instances of yawning were included in the data set.
 
Results
Figure 1 shows the distribution of yawning across all four groups. There were no yawns in the nasal breathing group. In all other groups, at least 45% of viewers yawned at least once. In the strictly oral breathing group (not the nose plug condition), 54% of viewers yawned at least once. There were no significant effects of gender on yawning. Of the 16 yawners (9 male, seven female), six yawned several times (two male, four female). Multiple yawning occurred most frequently in the two oral breathing conditions. The average number of yawns per group ranged from three yawns per person in the oral group to 1.2 yawns per person in the normal breathing group. Frequency of yawns between groups was significantly different, •2(3) = 20.45, p<.001. A comparison of the number of people yawning in the oral and nasal breathing groups also differed significantly, •2(1) = 6.00,p<.02. Using a binomial test based on the frequency of contagious yawning (41.5%) reported by Platek et al. (2003), the absence of yawning in the nasal breathing group was significant (p = .0027).
 
 
Experiment 2: Forehead Temperature Manipulation
The second experiment investigated whether forehead cooling had an impact on the occurrence of contagious yawning. Forehead temperature was the focus of this experiment because of its influence on brain temperature (Zenker and Kubik, 1996).
 
Participants
Participants consisted of an additional sample of 33 undergraduate students at the University of Albany. Twenty participants were female and 13 were male, and all were eighteen to twenty-five years of age.
 
Procedure
After each participant signed a consent form, they were asked to step into the same room used in the previous experiment and were seated in front of the same computer screen. Each participant was then either instructed to hold a warm pack, a cold pack, or a pack at room temperature to their forehead during this experiment, which lasted for the same length of time as the previous experiment (4 min, 50sec). Eleven participants were randomly assigned to each condition.
Each pack consisted of a hand towel folded over a few times and placed into a Ziploc plastic bag. To influence the temperature of the hot and cold packs, the hand towel was soaked in either warm water (46 oC) or cold water (4 oC) before being placed into the plastic bag. Temperature of the water and packs was monitored using a digital thermometer.
 
The hot and cold packs were all within one degree Celsius of the intended temperature for every participant at the beginning of the testing procedure. The room temperature condition was achieved by placing a separate, dry towel into the plastic bag.
Participants were instructed to hold the pack to their forehead for a period of two minutes prior to the video, and to continue holding the pack to their forehead for the duration of the video. The same video from the first study was shown to the participants on a computer screen using Windows Media Player. Each participant was observed through a one-way mirror by a researcher who recorded the incidence of yawning. Two of the participants (one in the cold pack group and one in the hot pack group) who did not show detectable signs of a yawn, each reported yawning once. These self-reported instances of yawning were included in subsequent analyses.
 
Results
Only one participant yawned in the cold pack group (see Figure 2), which was a self-reported but not independently verified instance. In the other two groups 41% of the participants yawned at least once. In the hot pack group, 36% of the participants yawned, while in the room temperature condition, 45% of the participants yawned. Eighteen yawns were recorded in the hot and room temperature groups while only one self-reported yawn was recorded in the cold condition. There were no significant effects of gender on yawning. Of the 10 people who yawned, three yawned more than once (two male, one female). Figure 2 shows the distribution of yawning across all three groups. Of the people who yawned, the average number of yawns ranged from 2.25 per person in the warm pack group to one yawn per person in the cold pack group. The difference in number of yawns between groups was significant, •2(2) = 6.87, p<.05. Again, using the data from Platek et al. (2003) on the occurrence of contagious yawning, a binomial test applied to the number of people yawning in the cold pack group was also significant, p = .0199.
 
General Discussion
Different methods of breathing had a significant effect on the incidence of contagious yawning. Nasal breathing antagonized contagious yawning, while participants in the other breathing conditions yawned around 48% of the time. Manipulating forehead temperature also had a significant effect on the occurrence of contagious yawning. A cold pack held to the forehead greatly reduced contagious yawning, while warm and room temperature packs had no effect. The two conditions thought to promote brain cooling (nasal breathing and forehead cooling), practically eliminated contagious yawning. Only one out of a total of 22 combined participants in the nasal breathing and forehead cooling conditions yawned, and that participant showed only one self-reported, but not independent verified instance of yawning. In the other conditions, 25 out of 55 participants yawned for a total of 51 yawns.
 
The manipulations involved in the breathing experiment are related to those done in a study by Provine (1986), where participants were instructed to think about yawning while clenching their teeth. Clenched teeth yawns were rated as abnormal and less satisfying, however clenching the teeth did not block yawns. Yawning still occurred as often as in baseline conditions and the duration of these yawns was not significantly different. This suggests that it was not simply the immobilization of the jaw in the nasal breathing group that eliminated yawning (even though the participants were not instructed to close their mouths, they were instructed to inhale and exhale nasally).
 
Based on evidence that clenching the teeth does not block yaning (Provine, 1986) we submit that it is the breathing manipulation (and the corresponding thermoregulation effects: see below) that alter the incidence in contagious yawning and not the difference between an opened or closed jaw.
 
Brain cooling model
Yawning has many physiological consequences that are concordant with those needed for the regulation of brain temperature. The constriction and relaxation of facial muscles during yawning increases facial blood flow and these changes alter cerebral blood flow (Zajonc, 1985). Yawning causes an overall increase in blood pressure (Arkenasy, 1996), arousal as measured by skin conductance (Greco and Baenninger, 1991), and heart rate (Heusner, 1946); all of which promote inc?eased blood flow during the period immediately prior to yawning. Research by Cabanac and Brinnel (1985) shows that during hyperthermia (exercise-induced heat stress), blood flow is increased from the skin of the head into the cranial cavity, and this increase is essential for proper cooling of the brain. Similar physiological consequences occur during powerful stretching, and yawning is accompanied by stretching almost half the time (Provine, Hamernik, and Curchack, 1987). This increase in blood flow and cerebral blood flow (as a result of yawning) function like a radiator to produce alteration of temperature in the brain. Likewise, the gaping of the mouth and deep inhalation of cool air taken into the lungs during a yawn can alter the temperature of the blood in the brain through convection.
 
Thermoregulation has been strongly linked to structures of the hypothalamus (Cooper, 2002). Some recent research using tissue slices pinpoints the complex circuits within the hypothalamus serving thermoregulation (Boulant, '1996). Interestingly, yawning also appears to be regulated by the hypothalamus. Yawning is under the control of many neurotransmitter and neuropeptides, and the interaction of these substances in the nucleus of the hypothalamus can facilitate or inhibit yawning respectively (Argiolas and Melis, 1998). Dopamine is a common neurotransmitter that is released by the hypothalamus. When injected into the brain, dopamine agonists (compounds that activate dopamine receptors) not only produce yawning (Collins, Witkin, Newman, Svensson, Cao, Grundt, and Woods, 2005), but have also been shown to increase heat production (Yamawaki, Lai, and Horita, 1983; Lin, 1979).
 
Acute dopamine/norepinephrine reuptake inhibition has been shown to increase both brain and core temperature in rats (Hasegawa, Meeusen, Sarre, Diltoer, Piacentini, and Michotte, 2005). Prolonged sleep deprivation in rats also produces increases in brain temperature (Everson Smith, and Sokoloff, 1994). Interestingly, yawning is ordinarily 'associated with being sleepy or tired, and a common symptom on many sleep deprivation checklists is excessive yawning.
 
The fact that nasal breathing antagonized yawning is consistent with the thermoregulatory hypothesis. Nasal breathing has been identified as one of the three putative mechanisms involved in cooling the brain. The vertebral venous plexus, which is located in the brainstem, is cooled by the vertebral artery as a result of nasal breathing (du Boulay, Lawton, and Wallis, 2000). Nasal breathing also cools other parts of the brain, including the frontal cortex (Mariak et al., 1999). Nasal mucosal blood flow decreases in response to skin cooling, increases in response to skin warming, and it rises in response to increases in core temperature (McIntosh, Zajonc, Vig, and Emerick, 1997).
 
We suggest that the cerebral cooling stimulated by nasal breathing was strong enough to inhibit mechanisms that would normally trigger yawning.
 
Cooling the forehead simulates a combination of the other two mechanisms thought to cool the brain, one being cooling of venous blood by the skin which in turn cools the arterial (carotid) blood supply to the brain. The other major brain cooling mechanism is the dissipation of heat through facial emissary veins (Zenker and Kubik, 1996; Cabanac, 1986; Cabanac and Brinnel, 1985), or heat loss through the skull. The density of sweat glands on the forehead is three times that of the rest of the body (Cabanac, 1986) and under normal conditions, blood from the face and forehead would be cooled by evaporation of sweat from the face and scalp.
 
Predictions of the Model
On the basis of this evidence we propose that yawning has a thermoregulatory function, and that yawning evolved to promote/maintain mental efficiency by keeping brain temperature in homeostasis. There are several other ways to test this model. For instance, we predict that yawning should be influenced by variation in ambient temperature. We predict that as ambient temperatures approach body temperature, yawning should diminish, and once temperature exceeds body temperature yawning should stop. If yawning functions to regulate brain temperature, yawning above 37°C would warm the brain and would be counterproductive unless the individual is in a hypothermic state. Conversely, when ambient temperature drops below a certain point, perhaps -10'C, yawning could produce a thermal shock by sending a wave of unusually cold blood to the brain. It follows that when people develop a fever, yawning should stop. That is, when body temperatures exceed normal values, it may simulate conditions ordinarily associated with an increase in ambient temperature above 37°C and activate mechanisms that inhibit yawning. This may be the reason the application of the warm pack to the forehead in Experiment 2 failed to stimulate an increase in yawning.
 
We also predict yawning to increase when people are engaged in difficult mental tasks. Increased cortical metabolic activity associated with higher information processing loads would increase brain temperature and trigger compensatory yawning. It has been noted that yawning occurs frequently in transition periods from inactivity to activity and vice versa (Baenninger, Binkley, and Baenninger, 1996; Provine, Hamernik, and Curchack, 1987), which is consistent with the idea that yawning plays a role in mental efficiency. It has also been argued that the contraction of facial muscles during a yawn forces blood through cerebral blood vessels to the brain, which may function to increase alertness (Barbizet, 1958; Heusner, 1946).
 
According to our, hypothesis, rather than promoting sleep, yawning should antagonize sleep. It has been widely believed that yawning in the presence of others is disrespectful and a sign of boredom (e.g., witness the fact that many people cover their mouths when they yawn). However, according to our account yawning more accurately reflects a mechanism that maintains attention. Likewise, when someone yawns in a group setting as evidence for diminished mental processing efficiency, contagious yawning may have evolved to promote the maintenance of vigilance.

 
-Gallup AC, Miller ML, Clark AB Yawning and thermoregulation in budgerigars Melopsittacus undulatus Animal Behav 2009;77(1):109-113
-Gallup AC, Gallup G. Yawning as a brain cooling mechanism: nasal breathing and forehead cooling diminish the incidence of contagious yawning. Evolutionary Psychology www.epjournal.net; 2007;5(1): 92-101
-Gallup AC, Gallup GG Jr. Yawning and thermoregulation. Physiol Behav. 2008;95(1-2):10-16
-Gallup AC, Miller ML, Clark AB Yawning and thermoregulation in budgerigars Melopsittacus undulatus Animal Behav 2009;77(1):109-113
-Gallup AC, Gallup Jr GG Venlafaxine-induced excessive yawning: a thermoregulatory connection Prog Neuro Psychopharmacol Biol Pyschiatry 2009;33(4):747
-Gallup AC, Gallup GG Jr, Feo C. Yawning, sleep, and symptom relief in patients with multiple sclerosis. Sleep Med. 2010
-Platek SM, SR Critton, et al Contagious yawning: the role of self-awareness and mental state attribution Cogn Brain Res 2003; 17; 2; 223-7
-Platek S, Mohamed F, Gallup G Contagious yawning and the brain Cognitive Brain Research, 2005;23:448-452

Deklunder G, Dauzat M, Lecroart JL, Hauser JJ, Houdas Y.
Influence of ventilation of the face on thermoregulation in man during hyper- and hypothermia.
Eur J Appl Physiol Occup Physiol. 1991;62(5):342-348.
 
It has been suggested that a thermal countercurrent exchange may occur in the cerebral vascular bed of humans, thereby creating for the brain a state of relative thermal independence with regard to the rest of the body. However, worrying questions have arisen concerning this suggestion. Experiments were carried out on seven young male volunteers. Hyper- and hypothermic conditions were produced by immersion in water at 38.5 degrees C and 25 degrees C, respectively. During the last few minutes of immersion, the face was cooled or warmed by ventilation with a 200 l.min-1 air flow at 5 degrees C or 40 degrees C, respectively. Internal and peripheral temperatures were recorded. Blood flow in the anastomotic vessels between face and brain was measured by Doppler techniques associated with computerized frequency analysis. The general responses were as classically described, i.e. an increase in peripheral and central temperatures during immersion in the warm bath and a decrease in these variables in the cold bath. The reactions produced by cooling or warming the face were small and easily explained by the direct changes of the heat load they induced. Whatever the thermal conditions, the blood flow in the anastomotic vessels between the vascular bed of the face and that of the brain was never reversed. It was concluded that there was no experimental evidence for an efficient thermal counter-current exchange in the vascular bed of the human head
References
 
Argiolas, A., and Melis, M.R. (1998). The neuropharmacology of yawning. European Journal of Pharmacology, 343, 1-16.
 
Arkenasy, J.J. (1996). Inhibition of muscle sympathetic nerve activity during yawning. Clinical Autonomy Research, 6, 237-39.
 
Baenninger, R. (1987). Some comparative aspects of yawning in Betta splendens, Homo sapiens, Panthera leo, and Papio sphinx. Journal of Comparative Psychology, 101, 349-354.
 
Baenninger, R., Binkley, S., and Baenninger, M. (1996). Field observations of yawning and activity in humans. Physiology and Behavior, 59, 421-425.
 
Barbizet, J. (1958). Yawning. Journal of Neurology, Neurosurgery, and Psychiatry, 21, 203-209.
 
Boulant, J.A. (1996). Hypothalamic neurons regulating body temperature. In Fregly, M. J. and Blatteis, C. M., (Vol. Eds.), Handbook of Physiology, Section 4, Vols. 1-2, Environmental Physiology. (pp. 105-126). Oxford, Oxford University Press.
 
Cabanac, M. (1986). Keeping a cool head. News in Physiological Sciences, American Physiological Society, 1, 41-44.
 
Cabanac, M., and Brinnel, H. (1985). Blood flow in the emissary veins of the head during hyperthermia. European Journal of Applied Physiology, 54, 172-176.
 
Cabanac, M., and Caputa, M. (1979). Natural selective cooling of the human brain: Evidence of its occurrence and magnitude. Journal of Physiology, 286, 255264.
 
Dib B, Cabanac M. Skin or hypothalamus cooling: a behavioral choice by rat Brain Res. 1984;302(1):1-7.
Rats were chronically implanted with a hypothalamic thermode. After recovery the thermode was heated and the rats were exposed to 4 ambient temperatures (Ta) 20, 30, 35 and 40 degrees C. For each Ta they were subjected to 3 conditions: (1) they could press a bar which provided them with a cool wind; (2) they could press a bar which cooled the hypothalamic thermode; and (3) both bars were active and the rat could press either one. Skin, hypothalamic, and rectal temperatures were recorded at the same time. The results indicate that when rats had either only or by choice access to the lever that cooled their hypothalamus, they used it in such a way as to prevent their hypothalamus from overheating. A lower priority was given to the maintenance of skin temperature.
 
Collins, G.T., Witkin, J.M., Newman, A.H., Svensson, K.A., Grundt, P., Cao, J., and Woods, J.H. (2005). Dopamine agonist-induced yawning in rats: A dopamine receptor-mediated behavior. Journal of Pharmacology and Experimental Therapeutics, 314, 310-319.
 
Cooper, K.E. (2002). Molecular biology of thermoregulation: Some historical perspectives on thermoregulation. Journal of Applied Physiology, 92, 1717-1724.
 
Daquin, G., Micallef, J., and Blin, 0. (2001). Yawning. Sleep Medicine Review, 5, 299312.
 
Dourish, C.T., and Cooper, S.J. (1990). Neural basis for drug-induced yawning. Neurobiology of Stereotyped Behavior, 91-116. Oxford: Clarendon Press.
 
du Boulay, G., Lawton, M., and Wallis, A. (2000). Selective brain cooling in animals: Internal carotid's significance for 'sudden infant death syndrome. Ambulatory Child Health, 6,36-38.
 
Everson, C.A., Smith, C.B., and Sokoloff, L. (1994). Effects of prolonged sleep deprivation on local rates of cerebral energy metabolism in freely moving rats. Journal of Neuroscience, 14, 6769-6778.
Although sleep deprivation interferes with biological processes essential for performance, health, and longevity, previous studies have failed to reveal any structural or functional changes in brain. We have therefore measured local rates of cerebral glucose utilization (ICMRglc) with the quantitative autoradiographic 2-14C-deoxyglucose method in an effort to determine if and, if so, where sleep deprivation might affect function in sleep-deprived rats. Sleep deprivation was maintained for 11-12 d, long enough to increase whole body energy metabolism, thus confirming that pathophysiological processes that might involve brain functions were evolving. Deep brain temperature was also measured in similarly treated rats and found to be mildly elevated relative to core body temperature. Despite the increased deep brain temperature, systemic hypermetabolism, and sympathetic activation, ICMRglc was not elevated in any of the 60 brain structures examined. Average glucose utilization in the brain as a whole was unchanged in the sleep-deprived rats, but regional decreases were found. The most marked decreases in ICMRglc were in regions of the hypothalamus, thalamus, and limbic system. Mesencephalic and pontine regions were relatively unaffected except for the central gray area. The medulla was entirely normal. The effects of sleep deprivation on brain tended, therefore, to be unidirectional toward decreased energy metabolism, primarily in regions associated with mechanisms of thermoregulation, endocrine regulation, and sleep. Correspondence was found between the hypometabolic brain regions and some aspects of peripheral symptoms.
 
 
Falk, D. (1990). Brain evolution in Homo: The "radiator" theory. Behavioral and Brain Sciences, 13, 333-381.
 
Braga J, Boesch C. Further data about venous channels in South African Plio-Pleistocene hominids.
J Hum Evol.1997;33(4):423-447.
Original data about venous channels in South African Plio-Pleistocene hominids are discussed. To assess possible changes in blood volume flow of fossil hominids, we test whether dimensions of three extracranial venous foramina were different between Australopithecus africanus and Australopithecus (Paranthropus) robustus. Moreover, providing further data about the small sample of South African Plio-Pleistocene hominids, we also attempt to re-analyse the incidence of divided hypoglossal canals and four emissary foramina in a very large sample of extant African apes representing all ages, species and subspecies, in A. africanus and in "robust australopithecines". Up to now, only very poor data on extracranial dimensions of venous foramina were available for fossil hominids. However, this topic provides interesting information about the modifications of volume flow during human evolution. Assuming that in fossil hominids, as in humans, dimensions of condylar and mastoid foramina, as well as those of jugular foramina, depended on volume flow through them, we conclude, first, that volume flow through internal jugular veins was comparable in South African australopithecines, extant chimpanzees and humans, and second, that, in comparison with the extant less-encephalized chimpanzees (presumably reflecting the ancestral condition), volume flow was higher through condylar veins in A. (P.) robustus. This increase was responsible for a significantly greater amount of blood drainage from the brain (and consequently an increased arterial blood supply). We support the view that encephalization was the prevailing functional explanation for volume flow increase through condylar veins in A. (P.) robustus, in comparison with its ancestor with its presumably more ape-like degree of encephalization. Considering the incidence of emissary canals and foramina, significant differences between A. africanus, "robust australopithecines" and all the extant African ape species, were tested statistically. Concerning the condylar canal, we did not find differences between "robust australopithecines" and extant African apes. Concerning the incidence of divided hypoglossal canals, mastoid canals, parietal and occipital foramina, no difference was found between extant African apes, A. africanus and "robust australopithecines". High frequencies of either condylar or mastoid canals cannot be regarded as a "pongid condition". Moreover, we did not find convincing data to support the hypothesis that mastoid emissary veins (partly representing a putative "radiator" for cooling the brain) were selected in A. africanus, in comparison with "robust australopithecines".
 
Greco, M., and Baenninger, R. (1991). Effects of yawning and related activities on skin conductance and heart rate. Physiology and Behavior, 50, 1067- 1069.
 
Hasegawa, H., Meeusen, R., Sarre, S., Diltoer, M., Piacentini, M.F., and Michotte, Y. (2005). Acute dopamine/norepinephrine reuptake inhibition increases brain and core temperature in rats. Journal of Applied Physiology, 99, 1397-1401.
 
Heusner, A.P. 1946. Yawning and associated phenomena. Physiological Review, 25, 156168.
 
Hinde, R.A., and Tinbergen, N. (1958). The comparative study of species specific behavior. In A. Roe and G. C. Simpson (Eds.), Behavior and Evolution, 251-268. New Haven, CT: Yale University Press.
 
Lin, M.T. (1979). Effects of dopaminergic antagonist and agonist on thermoregulation in rabbits. Journal of Physiology, 293, 217-228.
 
Mariak, Z., White, M.D., Lewko, J., Lyson, T., and Piekarski, P. (1999). Direct cooling of the human brain by heat loss from the upper respiratory tract. Journal of Applied Physiology, 87,1609-1613.
 
McIntosh, D.N., Zajonc, R.B., Vig, P.S., and Emerick, S.W. (1997). Facial movement, breathing, temperature, and affect: Implications of the vascular theory of emotional efference. Cognition and Emotion, 11, 171-195.
 
Melis, M.R., Argiolas, A., and Gessa, G.L. (1987) Apomorphine-induced penile erection and yawning: Site of action in the brain. Brain Research, 415, 98-104.
 
Platek, S.M., Critton, S.R., Myers T E, and Gallup, Jr. G.G. (2003). Contagious yawning: the role of self-awareness and mental state attribution. Cognitive Brain Research, 17, 223-227.
 
Platek, S.M., Mohamed, F.B., and Gallup, Jr., G.G. (2005). Contagious yawning and the brain. Cognitive Brain Research, 23, 448-452.
 
Provine, R.R. (1986). Yawning as a stereotyped action pattern and releasing stimulus. Ethology, 72, 109-122.
 
Provine, R.R. (2005). Yawning. American Scientist, 93, 532-539.
 
Provine, R.R., and Hamernik, H. B. (1986). Yawning: Effects of stimulus interest. Bulletin of the Psychonomic Society, 24, 437-438.
 
Provine, R.R., Hamernik, H.B., and Curchack, B.B. (1987). Yawning: Relation to sleeping and stretching in humans. Ethology, 76, 152-160.
 
Provine, R.R., Tate, B.C., and Geldmacher, L.L. (1987). Yawning: No effect of 3-5% C02, 100% 02, and exercise. Behavioral Neural Biology, 48, 382-393.
 
Sherer, D.M., Smith, S.A., and Abramowicz, J.S. (1991). Fetal yawning in utero at 20 weeks gestation. Journal of Ultrasound Medicine, 10, 68.
 
Smith, E.0. (1999). Yawning: An evolutionary perspective. Human Evolution, 14, 191-98.
 
Tinbergen N (1952) Derived activities Their causation, biological significance, origin, and emancipation during evolution. Quarterly Review of Biology, 27, 1-32.
 
Yamawaki, S., Lai, H., and Horita, A. (1983). Dopaminergic and serotonergic mechanisms of thermoregulation: Mediation of thermal effects of apomorphine and dopamine. Journal of Pharmacology and Experimental Therapeutics, 227, 383-388.
 
Zajonc, R.B. (1985). Emotion and Facial Efference: A Theory Reclaimed. Science, 288, 15-21.
 
Zenker, W., and Kubik, S..(1996). Brain cooling in humans - anatomical considerations. Anatomy & Embryology (Berl), 193, 1-13.
Vascular arrangements allowing a bulky transfer of venous blood from the skin of the head and from nasal and paranasal mucous membranes to the dura matter provide an excellent anatomical basis for the convection process of cooling, caused by evaporation of sweat or mucus. The dura mater, with its extraordinarily high vascularization controlled by a potent vasomotor apparatus, may transmit temperature changes to the cerebrospinal fluid (CSF) compartment. Temperature gradients of the CSF may in turn influence the temperature of brain parenchyma (1) directly, along the extensive contact area between the cerebrocortical surface and the CSF-compartment, or (2) indirectly, via brain arteries that extend over long distances and arborize within the subarachnoid space before entering the pial vascular network and brain parenchyma. Numerous subarachnoid and pial arterial branches exposed to the CSF have diameters in the range of the vessels of the retia mirabilia of animals in which selective brain cooling has been clearly established experimentally. It is also shown that the arrangements of venous plexuses within the vertebral canal provide anatomical preconditions for a cooling of the spinal cord via the CSF. The possibility of spinal cord and spinal ganglia cooling by temperature convection via venous blood--cooled in the venous networks of the skin of the back--flowing through numerous anastomoses to the external and internal vertebral plexuses and, finally, into the vascular bed of the spinal dura is discussed on the basis of anatomical facts.

Who knows whether there is really a need for cooling the brain?
 
Gallup & Gallup conducted two experiments that implicate yawning as a thermoregulatory mechanism.
 
Gallup and Gallup propose to renew the theory of the yawn's finality. In order to observe yawns among the participants with the experiments, they projected a film showing the successive yawns of eight people (man and woman) randomly stopped by scenes of laughter or neutral facial expressions. Then, they counted up the yawns induced by "contagion" (echokinesia). In general, the unavoidable interaction between voluntary and automatic control affects the outcome of many experiments in humans. Moreover, contagious yawning is not identical to spontaneous yawning.
 
First experiment :
They show that the yawns occur normally and that 45% of the particpants yawn when they can open the mouth but that no yawn takes place if the instruction is given to hold the mouth completely closed. This fact is established for a long time: for example, the Equidae, which breathes only by the nostril, yawns opening widely the mouth like all the other vertebrates.
 
"The first experiment demonstrates that different patterns of breathing influence susceptibility to contagious yawning. When participants were not directed how to breathe or were instructed to breathe orally (inhaling and exhaling through their mouth), the incidence of contagious yawning in response to seeing videotapes of people yawning was about 48%. When instructed to breathe nasally (inhaling and exhaling through their nose), no participants exhibited contagious yawning."
 
Second experiment:
"In a second experiment, applying temperature packs to the forehead also influenced the incidence of contagious yawning. When participants held a warm pack (460C) or a pack at room temperature to their forehead while watching people yawn, contagious yawning occurred 41% of the time. When participants held a cold pack (40C) to their forehead, contagious yawning dropped to 9%. These findings suggest that yawning has an adaptive/functional component that it is not merely the derivative of selection for other forms of behavior."
 
The only fact of laying a cold stimulus on the forhead is enough to stimulate the awakening and inhibits the yawn. In the same way, a constant attention does not make receptive to the echokinesia of yawning. Inversely, heat does not have this waking up effect. The increase in the ambient temperature facilitates sleepiness and thus yawning.
 
Room temperature is not considered. However, a quantitative analysis of the effects of different temperatures of the air inhaled via nose or mouth would be interesting.
 
Forehead cooling is not affecting directly and only the brain. It is a peripheral thermal input favoring inhibition and reinforcement of oral and nasal respiration, respectively, to warm the inhaled air. Oral ventilation in this condition would be necessary only to comply with the oxygen demand during exercise
 
The researchs of Cabanac and Brinnel as reported by G & G relate to the control of the cerebral temperature during the fever. There is no work (to my knowledge) indicating that the cerebral activity modifies the internal temperature of the brain in a variable way according to the level of attention. Functional MRI studies in humans have shown that even when the brain is not engaged in any specific tasks, spontaneous fluctuations occur in the blood-oxygen-level dependent (Bold) signal (which is thought to reflect neural activity). These resting state fluctuations are not chaotic but are in fact anatomically and temparally consistent. The significance of this resting state activity is unclear but, intriguingly, it even occurs when humans or animals are unconscious. Thus, spontaneous fluctuations in brain activity maintain the brain in constant temperature somehow the step of neuronal activities (Vincent JL. et al.).
 
Sleep onset is likeliest to occur on the falling limb of the temperature cycle. The offset of sleep occurs most often on the rising limb of the circadian body temperature curve. In human, the most pronounced occurrences of yawning stays at awakening in the morning, in association with the stretching of muscles (pandiculation), and as sleep is about to occur, without stretching, as well as in any condition of lessened vigilance (Baenninger 1996, Greco 1993). Repetitive and monotonous activities trigger repeated yawns as have shown studies of individuals at their work stations. In not a single circumstance, the yawns appear with the acme of the circadian rhythm of the temperature.
 
The old authors often spoke about the yawns during the fever but have given to them the significance of a clinical sign fortelling the onset of vigilance's disorders. The assertion "deep inhalation of cool air taken into the lungs during a yawn can later the temperature the temperature of the blood in the brain through convection" appears largely conjectural. The air in the lung attains 37° so far its inhalation and prevents to harm the lungs. Ford GP, Reardon DC. report that intubated delivery of air into the lungs at a temperature significantly below body temperature, especially over a prolonged period, is likely to inhibit recovery from brain injuries.
 
Many authors (Parmeggiani 2007) have reported changes in brain temperature during the ultradian sleep cycle in several mammalian species. The temperature decrease in NREM sleep appears as a normal effect of thermoregulation operating at a lower set point temperature than in wakefulness. In contrast, the increase in brain temperature related to REM sleep appears paradoxical from the viewpoint of normal thermoregulation. The problem of the physiologic mechanisms underlying this temperature change remains unresolved.
 
Changes in brain temperature are in general relevant to both the energy metabolism of the brain and the function of the preoptic-hypothalamic thermostat. Heat is produced by cellular energy metabolism and is transferred to the arterial blood in inverse relation to its temperature, which is lower than that of the brain in normal conditions. It is obvious that brain homeothermy is altered essentially by quantitative imbalances between metabolic heat production and heat loss.
 
There are different mechanisms for cooling the brain in mammals and more than a single mechanism may be operative. In general, the cool venous blood flowing from the systemic heat exchangers of the body (upper airway mucosa, ear pinna, horn, tail, skin, according to species) to the heart mixes with the warm venous blood returning to the heart from heat-producing body tissues.
 
This systemic mechanism cools the arterial blood including that flowing to the brain (systemic brain cooling). In addition to systemic brain cooling, there is also a mechanism for selective brain cooling. In species like the cat, dog, sheep and goat, the carotid blood supply to the brain is again thermally conditioned prior to entering into the circle of Willis by countercurrent heat exchange between carotid rete and venous sinuses (e.g., sinus cavernosus). The carotid rete is a network of fine vessels (rudimental in the dog), derived from the external branch of the common carotid artery. The arterial blood flowing to the brain in the carotid rete is surrounded by sinus venous blood cooled in the upper airway mucosa and flowing in an opposite direction to the heart. The carotid rete is connected to the circle of Willis through a short artery (homologous to the distal part of the internal carotid artery of species lacking the carotid rete). As a result of the countercurrent heat exchange, the temperature of the carotid blood reaching the circle of Willis is further decreased with respect to that of the aortic arch blood. Vertebral artery blood is not thermally conditioned by a countercurrent heat exchange mechanism and enters into the circle of Willis at the temperature of the blood in the aortic arch.
 
In conclusion, the difference between the temperatures of vertebral artery blood (systemic cooling only) and carotid artery blood (both systemic and selective cooling) flowing into the circle of Willis depends on the heat loss from the carotid rete. Eventually, the average brain temperature is determined by the relative amounts of carotid and vertebral artery blood contributing to the total blood flow of the brain.
 
Another mechanism for selective brain cooling is typical of species lacking the carotid rete (e.g., rabbit and rat). It is provided by conductive heat exchange between the basal portion of the brain, including the circle of Willis, and the basal venous sinuses that drain cool venous blood from the upper airway mucosa.
 
The effects of systemic and selective brain cooling appear in the temperatures of the hindbrain and forebrain, respectively. This is shown by the positive difference between pontine and preoptic-hypothalamic temperatures in cats, rabbits and rats.
 
Heat loss from systemic heat exchangers, affecting carotid blood temperature through the systemic venous return to the heart (systemic brain cooling), is the most important determinant of brain temperature in primates. Concerning humans, in particular, there is no consensus as to whether a mechanism for selective brain cooling plays a significant role.
 
Skin or hypothalamus cooling: a behavioral choice by rat
Dib B, Cabanac M.
Brain Res. 1984;302(1):1-7
Rats were chronically implanted with a hypothalamic thermode. After recovery the thermode was heated and the rats were exposed to 4 ambient temperatures (Ta) 20, 30, 35 and 40 degrees C. For each Ta they were subjected to 3 conditions: (1) they could press a bar which provided them with a cool wind; (2) they could press a bar which cooled the hypothalamic thermode; and (3) both bars were active and the rat could press either one. Skin, hypothalamic, and rectal temperatures were recorded at the same time. The results indicate that when rats had either only or by choice access to the lever that cooled their hypothalamus, they used it in such a way as to prevent their hypothalamus from overheating. A lower priority was given to the maintenance of skin temperature.
 
 
REM sleep related increase in brain temperature: a physiologic problem.
Parmeggiani PL. Arch Ital Biol. 2007;145(1):13-21.
 
Prolonged unintended brain cooling may inhibit recovery from brain injuries: case study and literature review
Ford GP, Reardon DC Med Sci Monit 2006;12(8):CS74-77

Andrew C. Gallup. Yawning and the thermoregulatory hypothesis