Psychonomic Bulletin & Review /997. 4 (2), /98-::07

On yawning and its functions

RONALD BAENNINGER Temple University, Philadelphia, Pennsylvania

The forms and behavioral correlates of yawning are described, and the phylogenetic and ontoge­ netic aspects of the act are examined with particular attention to its possible functions. Much evi­ dence supports the view that yawning is an important mediator of behavioral arousal levels, a view that is further strengthened by a review of endocrine, neurotransmitter, and pharmacological mech­ anisms of yawning: A major function of yawning appears to involve maintenance or increase of arousal when environments provide relatively little stimulation.

Why do humans and many other species ofmammals, Ordinary behavioral acts such as yawning, laughing, birds, fish, amphibians, and reptiles perform the elabo­ crying, scratching, belching, sneezing, or sighing are rarely rate behavioral display that we call a yawn? In this re­ studied per se in any detail by psychologists, except in­ view I examine research on yawning by psychologists, sofar as they communicate or express something to oth­ pharmacologists, ethologists, and neuroscientists during ers about an individual's state. Niko Tinbergen, the Nobel the past century, paying particular attention to the possi­ Prize winning ethologist, suggested in 1963 that the ble role ofyawning in regulating arousal. analysis of any behavioral act should include four basic aspects: (1) the way in which the act develops normally Respiration or Arousal? in individuals and the extent to which it becomes modi­ Yawning may have different functions in different fied during ontogeny; (2) its evolution and phylogenetic species, but on the basis of evidence reviewed in this history; (3) mechanisms underlying the behavior, in­ paper I suggest that yawning is one important way ofreg­ cluding its physiology and the stimuli that elicit it; (4) its ulating arousal in a remarkable variety of species, in­ functions or adaptive value for individuals and species. cluding humans. In particular, according to this hypoth­ In this review, a thorough description of yawning and esis, yawning is likely in situations where wakefulness its behavioral correlates in several species is followed by and the maintenance ofarousal level are important, but an examination ofits ontogeny, phylogeny, and underlying where the environment is relatively unstimulating. Arousal mechanisms. The thread used to tie all the diverse data and permits vigilance, attentiveness, and wakefulness, and is observations together is the basic hypothesis that a major typically measured in terms ofmotor activity and physi­ function ofyawning is to regulate levels ofarousal. ological variables such as heart rate, galvanic skin re­ sponse, electroencephalogram (EEG), or muscle tension. FORMS AND CORRELATES OF YAWNING The Oxford English Dictionary describes yawning in the context of boredom, whereas Gray s Anatomy (Cle­ Charles Darwin (1873) described yawning as com- mente, 1985) and the Encyclopedia ofHuman Biology mencing with (Dulbecco, 1991) do not even show yawning in their in­ dexes. To the extent that they consider it at all, most lay a deep inspiration, followed by a long and forcible expira­ people and physicians appear to believe that yawning is tion; and at the same time almost all the muscles of the a respiratory phenomenon, a way to get oxygen to the body are strongly contracted, including those around the eyes. During this act tears are often secreted, and I have brain (Greco, Baenninger, & Govern, 1993). In fact, seen them even rolling down the cheeks. (p. 164) there is meager evidence for this respiratory hypothesis and, on the basis of this review, it appears to be an in­ On the basis of X-ray photographs, Barbizet (1958) de­ complete explanation at best. scribed yawns in humans as having three phases. In the first phase a progressive, slow opening ofthe mouth is ac­ companied by dilation ofthe thorax, pharynx, and larynx, I gratefully acknowledge the ideas and helpful criticism ofmy col­ as well as a lowering ofthe diaphragm. Although opening leagues MaryAnn Baenninger, Alan Cowan, Monica Greco, and Luci of the mouth and deep inspiration also occur at other Paul, as well as the reviewers for this journal. I am also grateful to Byron Campbell at Princeton University, Bjorn Holmgren and Ruth times, it is only during yawning that the enormous expan­ Urba-Holmgren at the University ofPuebla, and Gordon Russell at the sion ofthe pharynx (three to four times normal), the low­ University of Lethbridge for their hospitality and intellectual stimula­ ering ofthe hyoid bone, and ofthe tongue occurs. The glot­ tion. A Study Leave and Grants-in-Aid from Temple University were tis is dilated to its utmost in this phase, and is therefore not of major assistance in making this work possible. Correspondence should be addressed to R. Baenninger, Department of Psychology, the cause ofthe inspiratory sound that may be heard. Temple University, Philadelphia, PA 19122 (e-mail: baenning@vm. In the second phase, the maximal opening ofthe mouth temple.edu). produces contraction of lip dilators, eyelid contraction

Copyright 1997 Psychonomic Society, Inc. 198 FUNCTIONS OF YAWNING 199

(often causing occlusion of the eyes), and nostril dila­ gaping, which involves rapid opening and closing ofthe tion, together with wrinkling of skin at the base of the mouth with the teeth visible. nose, and eyebrow lifting. Maximal dilation of the phar­ ynx occurs, and thoracic capacity is increased further by THE CONTEXT OF YAWNING stretching. Tears and saliva are frequently secreted, and vasoconstriction in the digits and cardiac acceleration Particular times of day are associated with yawning, have also been reported (Greco & Baenninger, 1991; which raises the possibility of an endogenous temporal Heusner, 1946; Proctor, 1964). Such measures are clearly rhythm. Anias, Holmgren, Urba-Holmgren, and Eguibar related to arousal as defined by polygraph recordings. (1984) found that light-to-dark transitions were associ­ Inspiration ceases abruptly in the third phase and ex­ ated with daily peaks ofyawning by laboratory rats. The piration is slow and noisy; an "aah" sound may originate fact that yawning increased well before dark onset sug­ in the larynx, the pharynx returns to normal size, the gested to these authors that yawns were not simply in­ mouth closes rapidly, and the facial muscles return to duced by darkness, and that a genuine circadian rhythm normal. Barbizet (1958) reported that the whole se­ existed. In humans the transition from light to dark is quence lasts4-7 sec, a figure confirmed in humans by Pro­ also associated with frequent yawning but, unlike rats, vine (1986) and by Baenninger and Greco (1991). there is also a peak in yawning in the transition from dark The same basic sequence appears in all major classes to light. Provine, Hamernik, and Curchack (1987) found ofvertebrates, and in my own studies ofyawning in fish that yawning by college students was most frequent dur­ and mammals, I have adopted it as a criterion (i.e., slow ing the hour just before sleeping and after morning opening of the mouth, with inspiration in mammals, and awakening. Greco et al. (1993) replicated this finding but a more rapid closing and exhaling after several seconds). also found a smaller peak in early afternoon before the Although we cannot be certain that a behavioral se­ sleepiness peak reported by Mavjee and Horne (1994). quence is equivalent in species as different as Siamese Baenninger, Binkley, and Baenninger (1996) reported fighting fish, domestic dogs, cats, walruses, lions, and that nocturnal awakening was associated with yawning humans, the use of the same descriptive word simplifies in adult subjects who were wearing activity monitors. communication. Daily transitions from inactivity to activity (early morn­ Stretching ofthe limbs often accompanies yawning in ing) and from activity to inactivity (late evening) were humans, depending on whether they are standing, seated, strongly associated with yawning. Their subjects did not or lying down. In some quadrupeds, such as rats and yawn when they were actually lying in bed waiting to fall dogs, stretching of the forelegs occurs. Ferrari, Floris, asleep, and their yawning before retiring to bed can be and Paulesu (1955) reported a stretch/yawn syndrome in interpreted as attempts to maintain wakefulness or dogs, and this syndrome was also found in rats (Gessa, arousal. Pisano, Vargiu, Grabai, & Ferrari, 1967) and guinea pigs Although these regular daily variations in yawning (Rodriguez, Serra, Terrasawa, Goldfoot, & DeWied, frequency might represent an endogenous rhythm, an al­ 1981). Donovan (1978) reported the stretch/yawn syn­ ternative explanation appears to be more parsimonious drome in human males (accompanied by penile erections and general. If yawning occurs in anticipation ofregular and even ejaculations). daily events that require increased arousal, we would ex­ Penile erection has been observed to accompany drug­ pect yawning after sleeping, during sedentary activities induced yawning in several mammalian species, includ­ that require arousal or vigilance (such as attending lec­ ing rabbits and rats (Bertolini, Vergoni, Gessa, & Ferrari, tures and driving a car, as reported by Greco et al., 1993), 1969; Huston, 1971; Mogilnicka & Klimek, 1977). Phoe­ and as a way of maintaining wakefulness in the late even­ nix and Chambers (1982) found penile erections associ­ ing. As noted, these are precisely the contexts in which ated with yawning in rhesus monkeys (both normal and frequent yawning has been found. Also supporting the pseudohermaphrodite) in response to synthetic testos­ hypothesis that yawning is a means of increasing or terone injections; these authors also reported that yawn­ maintaining arousal are the reports by Baenninger ing by female rhesus monkeys was elicited by testos­ (1987) and Holmgren et al. (1991) that zoo and labora­ terone. More recently Melis, Stancampiano, Lai, and tory animals yawn before their regular feeding times, ap­ Argiolas (1995) reported that nitroglycerin, a potent va­ parently in anticipation of this major event oftheir days sodilator, induced both yawning and penile erections in in captivity. Perhaps for similar reasons, Koch, Montag­ male rats. Whether this association with penile erections ner, and Soussignan (1987) found that children in also exists in yawns that are spontaneous is not yet clear, kindergarten showed daily peaks of yawning at the be­ but the association of arousal and yawning is empha­ ginning and just before the end of their school days sized by these findings. (when maintaining wakefulness may be difficult, and Finally, Ushijima, Yamada, Inoue, Tokunaga, and Fu­ free time beckons). rukawa (1984) reported that tongue protrusion accom­ panied yawning by rats. Van Woerden et al. (1988) also PHYLOGENETIC ASPECTS OF YAWNING found tongue protrusion, grimacing, and jaw opening in the yawns of human fetuses. Salamone, Lalies, Channell, The daily lives of carnivorous mammals are charac­ and Iversen (1986) distinguished yawning in rats from terized by large variations in arousal level, from seden- 200 BAENNINGER tary tranquillity to stalking, chasing, and killing prey. (Myrberg, 1972), and jewel fish, Microspathodon chry­ Methods for achieving rapid and frequent changes in sums (Rasa, 1971). Yawning has been seen in reptiles states ofarousal should be present among carnivores. By such as tortoises (Luttenberger, 1975), and in turtles, contrast, the lives ofgrazing herbivores are relatively in­ lizards, and crocodiles (Craemer, 1924). Barthalmus and variant; the difficulty of deriving enough protein and Zielinski (1988) found yawning in northern water other nutrients from grasses requires that herbivorous snakes, Nerodia sipedon. Among birds, yawning has mammals spend most of their waking time eating. In been reported in ostriches (Sauer & Sauer, 1967), and I general, carnivores yawn much more frequently than have observed it in herring gulls; Dumpert (1921 ) as­ herbivores, as the arousal hypothesis would predict. In serted that it is universal in the class Aves. Craemer re­ 35 h of observation, Greco (1992) never saw giraffes ported yawning by toads and frogs, accompanied by yawn, perhaps because of their unique respiratory and bending and stretching of the hind legs, but it has not circulatory adaptations. Barbizet (1958) claimed that been reported in other amphibians such as newts or sala­ yawning was virtually absent in herbivores, but species manders. Thus, although the published observations are as different as horses and hippopotamuses clearly do extremely incomplete, yawning appears to occur in all yawn on occasion, and Craemer (1924) reported it in classes of vertebrates. At the very least, this suggests that both Perissodactyla (e.g., horses, tapirs, rhinoceroses) it has important and basic functions, but mere occur­ and Artiodactyla (e.g., swine, deer, antelope, cattle, rence of a behavioral trait, even in a variety of species, sheep). I have observed frequent yawning among the does not prove that it is adaptive. horses that wait along Central Park South to give car­ Although we may know relatively little about how nat­ riage rides to tourists in New York City. ural selection has affected yawning, the work of Holm­ Among the carnivores, yawning is frequent in the fis­ gren and Urba-Holmgren and their collaborators (1991) sipeds, both the Felidae (cat family) and Canidae (dog makes it clear that artificial selection can modify the fre­ family) (Baenninger, 1987; Ferrari et aI., 1955; Konor­ quency of yawning. Selective breeding resulted in a ski, 1967; Marini, 1981). It has also been found in pin­ strain of rats that yawns frequently (nearly 25 yawns/ nipeds (seals, sea lions, walruses). In fur seals (Arcto­ hour) and a strain that yawns very little (less than once/ cephalus forsteri) and walruses (Odobenus rosmarus), hour) by the 25th generation. Differences between fre­ Miller (1975) reported that yawning was associated with quent (HY) and infrequent (LY) populations were al­ erecting the mystacialvibrissae. Among other mammalian ready apparent by the F3 generation. orders, yawning has been reported in rodents (rats by Anias et aI., 1984; guinea pigs by Rodriguez et aI., 1981), ONTOGENETIC ASPECTS OF YAWNING lagomorphs (rabbits, Opp, Obal, & Krueger, 1988), and various species of nonhuman primates (Baenninger, 1987; Blanton (1917) reported yawning by neonates within Deputte, 1994; Hadidian, 1980; Louboungou & Ander­ 5 min after birth, almost as if they were waking up after son, 1987; Phoenix & Chambers, 1982; Redican, 1975). delivery from their uterine environment. Taylor-Jones To the best of my knowledge, there have been no formal (1927; see also Gill, White, & Anderson, 1984) con­ reports on yawning by any species of the Chiroptera firmed that newborns yawn a few minutes after taking (bats), Marsupialia (opossums, kangaroos), Insectivora, their first breath. It is possible that neonatal yawns, like Edentata (sloths, anteaters, armadillos), Cetacea (whales, adult yawns upon awakening, may serve to increase dolphins, porpoises), Monotremata (echidnas, platypus), arousal. Feldman, Brody, and Miller (1980) reported that Proboscidea (elephants), or Sirenia (manatees, dugongs). yawning was more frequent in female neonates than in Yawning may occur in all these orders too, but it has not males. been noted in published observations. Perhaps even more remarkable is the report by Smoth­ Behavior leaves no fossils, so unambiguous evidence erman and Robinson (1987) that rat fetuses showed on how and why yawning evolved is impossible to ob­ yawning at Day 20 of gestational development. Van Woer­ tain. Skulls of extinct species can tell us only whether den et al. (1988) observed regular mouth movements in yawning was possible, not whether it occurred. We can utero during certain human prenatal phases: yawns, gri­ know only the pattern by which traits appear, or do not maces, and tongue protrusion were clearly seen. Sherer, appear, in species that exist now, which may help us to Smith, and Abramowicz (1990) also observed yawns in derive the phylogenetic history ofa behavioral trait such a 20-week-old human fetus. The fetal environment is as yawning. If all existing species in each genus, family, presumably less stimulating than the postnatal one; like and order of mammals, birds, fishes, amphibians, and adult yawns in boring situations, fetal yawns may serve reptiles had been observed to yawn, we could trace the to increase arousal for some purpose. act back to the primitive chordates from which all verte­ Prenatal yawns could also be responses to uterine brates evolved. Sharks and rays are among the most chemistry, or to the internal physiological state of the primitive members of the phylum Chordata, but yawning fetus. Such yawns are incompatible with the "respiratory has not been reported in them. hypothesis." Although the fetus requires oxygen and In fish, yawning has been reported in species as di­ must expel carbon dioxide, it does not do so by using the verse as Siamese fighting fish, Betta splendens (Baen­ adult respiratory mechanism. Fetal lungs are incom­ ninger, 1987), damsel fish, Eupomacentrus partitus pletely developed until near term, and external stimula- FUNCTIONS OF YAWNING 201 tion is often necessary at the time of birth in order to tended to be more active than frequent yawners. Ifyawn­ start their normal operation. Thach and Taeusch (1976) ing is a way ofregulating activity or arousal, it is possi­ observed sighing in newborn human infants and sug­ ble that some people have learned to regulate arousal by gested that it served as an inflation-augmenting reflex yawning whereas others have not, using other means in­ for the newly functioning lungs. Proctor (1964) pointed stead. To what extent is the rate ofyawning by individu­ out that many respiratory physiologists interpret sighing als modifiable? functionally as a "small yawn." Provine (1986) has maintained that yawning is a Fetal mouth movements, grimacing, and stretching "stereotyped action pattern" that is elicited by the sight might be the means by which neonates are able to pro­ ofsomeone yawning, or by reading, thinking, or talking duce normally integrated yawns within minutes after about yawning. Earlier ethologists referred to such acts being born. Perhaps it is only postnatally that yawning as "fixed action patterns," emphasizing that they were becomes functional (whether that function proves to be fixed not only in their topography but also in the small arousal regulation or not). Human data on this point are number of stimuli that would elicit them. If Provine is lacking, but Holmgren et al. (1991) found that male rats correct, yawning should be relatively fixed in its form increased their frequency ofyawning during the 1st year and should appear only in response to certain stimuli. To oflife. Neonatal yawning is unlikely to be an imitative or my knowledge, there have been no reports ofPavlovian contagious response to adult yawning, and Piaget (1951) conditioning in which previously neutral stimuli come asserted that yawns elicited by seeing another individual to elicit yawning. yawn did not occur until the 2nd year of life. During the The extent to which the frequency of action patterns or 1st year, yawns appear to be spontaneous; imitative or operant acts may be controlled by their consequences contagious yawning may prove to be an interesting de­ has interested American psychologists for many years. velopmental marker. Thorndike (1911) successfully trained cats to lick or There have been no reports ofage-related changes in scratch when those acts resulted in release from a box. the actual form of human yawning, but it is clear that Can yawning similarly be brought under the control of there are developmental changes in the daily pattern of its rewardingor punishing consequences?Konorski (1967) yawning, as well as in its frequency, its eliciting stimuli, found that food reward of "true" yawning was nearly and whether it is under voluntary control. Troisi, Aureli, impossible in dogs, although what he termed "pseudo­ Schino, Rinaldi, and DeAngeli (1990) found that male y.awns" (of short duration) did increase in frequency macaques begin to yawn much more frequently than fe­ when they were rewarded. Louboungou and Anderson males when androgen levels rise at sexual maturity from (1987) used food rewards in training pigtail macaques juvenile to adult levels, a difference that is then main­ (Macaca nemestrina) to yawn more frequently, at rates tained throughout life (Deputte, 1994). In nonhuman pri­ up to 150 times per hour. Anderson and Wunderlich mates, it appears that males yawn with increasing fre­ (1988) found a similar result in Macaca tonkeana. Small quency as they grow older (Chambers & Phoenix, 1980; (1977) found that frequency of human yawning could be Deputte, 1994; Hadidian, 1980), perhaps because main­ changed in the laboratory by using a complex training tenance of arousal levels becomes more difficult for procedure in which subjects imagined a contingency be­ aged monkeys. Hadidian found that the dominant male tween yawning and certain visual images. in wild troops yawned most frequently. It is not clear Operant conditioning may also reduce the frequency whether this is because increased arousal and vigilance of acts followed by aversive events, as in punishment. are required to be an alpha male, or because dominant Tsunetomo (1979), a Japanese samurai, remarked that individuals have higher androgen levels, or because yawns "it is bad taste to yawn in front ofpeople" and suggested are used by dominant males as threat displays. that stroking the forehead upward or licking the lips with During their 1st year of school, children yawn five mouth closed were successful in inhibiting yawns. Most times as frequently as they did in nursery school (Koch people appear to have learned techniques to suppress or et al., 1987). At this important juncture in their lives, inhibit their own yawns in interviews, conversations, or children are expected to reduce their level of physical ac­ lectures where polite behavior is expected. In fact, the tivity during school hours and to conform to school study of yawning in the experimental laboratory has rhythms and constraints. Yawning is a familiar sight to been hampered by subjects' unwillingness to yawn in most teachers, even those who are not boring, and would the presence ofexperimenters (Baenninger, 1987; Greco be expected if yawning is a way to maintain arousal in a & Baenninger, 1989). Social factors may inhibit overt sedentary environment providing relatively low levels of yawning, but the motor pattern still occurs and the result stimulation. is a closed-mouth, teeth-clenched yawn in which activ­ ity of jaw muscles can usually be seen. Greco (1992) MODIFIABILITY OF YAWNING punished her subjects for yawning during a boring sim­ ulated driving task by withholding money. Subjects re­ Baenninger, Binkley, and Baenninger (1996) found duced their yawning frequency, but also made more care­ that some of their adult subjects reliably yawned 30 less driving errors, a result that lends support to the times each day,whereas others did so only once or twice. hypothesis that yawning helps to maintain the level of In that study, those who yawned relatively infrequently arousal or vigilance. 202 BAENNINGER

PHYSIOLOGICAL MECHANISMS another model for the neural control ofyawning that in­ OF YAWNING volved excitatory cholinergic, peptidergic, and seroton­ ergic influences, together with dopamineric and norad­ Many hours may be spent in waiting for a subject to renergic inhibitory influences. Thus, this apparently yawn spontaneously. Behavioral pharmacology has pro­ simple instinctive act may be under the control ofa com­ vided important knowledge about the mechanisms of plex set ofneurotransmitter mechanisms. yawning, in part because hormones or drugs may reli­ ably elicit yawning. Whether drug-induced yawns are Hormones identical to those that occur without drugs remains a Since 1955, when Ferrari et aI. discovered that injec­ concern in interpreting this research. tion ofACTH into cerebral ventricles ofdogs produced a syndrome of yawning and stretching, they and their Drugs That Induce Yawning colleagues have replicated (Argiolas, Melis, Stancam­ Withdrawal from opiate narcotics is associated with piano, & Gessa, 1989; Gessa et al., 1967) and extended frequent yawning in human adults (O'Brien, 1976), as this finding to a number of other hormones, such as well as in infants undergoing withdrawal from maternal MSH (Ferrari, Gessa, & Vargiu, 1963); Laping and addiction to heroin, morphine, or methadone (Rudolph, Ramirez (1986) found that prolactin induced both yawn­ Barnett, & Einhorn, 1977). Yawning may be elicited in ing and stretching in male rats. rats by cholinomimetic drugs such as physostigmine and Argiolas, Melis, and Gessa (1986) found that oxy­ pilocarpine (Urba-Holmgren, Gonzalez, & Holmgren, tocin, another pituitary hormone, was an extremely po­ 1977; Yamada & Furukawa, 1980). Physostigmine in­ tent inducer of yawning and penile erection in rats. Ar­ hibits acetylcholine metabolism, and pilocarpine is a giolis, Melis, Stancampiano, and Gessa (1989) found cholinergic agonist; both produce yawning in infant rats, that injection ofoxytocin and related peptide hormones with a maximum frequency of8-10 yawns in 15 min (each into the lateral ventricles ofrats produced both yawning lasting 3-4 sec). Antagonistic effects of atropine and and penile erection, concluding that central oxytocin re­ scopolamine were found by Ferrari et aI. (1955) in their ceptors that mediate the expression of both penile erec­ original work, indicating that yawning is cholinergically tion and yawning are structurally related to those recep­ mediated (because of its susceptibility to muscarinic tors present in uterus and mammary glands. blockers). Numerous other experiments have confirmed the as­ Both cholinergic (Cowan, 1978) and dopaminergic sociation ofhormone-induced yawning and penile erec­ (Mogilnicka & Klimek, 1977) components were subse­ tions (Berendsen & Nickolson, 1981; Gower, Hemmie, quently discovered. Low doses ofapomorphine or other Berendsen, Princen, & Broekkamp, 1984; Holmgren, dopamine agonists (Holmgren & Urba-Holmgren, 1980; Urba-Holmgren, Trucios, Zermeno, & Eguibar, 1985; Marini, 1981; Mogilnicka & Klimek, 1977) induce yawn­ Serra, Collu, Loddo, Celasco, & Gessa, 1983). Sponta­ ing with stretching, chewing movements, and penile erec­ neous yawning in humans, dogs, and rats may be ac­ tion in male rats. Mogilnicka and Klimek suggested that companied by stretching, but is not normally accompa­ treatment with low doses ofdopamine agonists activates nied by any overt signs of sexual excitement. Sexual presynaptic inhibitory dopamine receptors (so-called au­ arousal has been reported in some case reports of drug­ toreceptors). These are more sensitive to dopamine and related yawning. Donovan (1978) reported that both in­ dopamine agonists than are postsynaptic receptors. Thus, tracranial ACTH and MSH elicited the stretch/yawn low dopamine doses may stimulate these autoreceptors, syndrome in human males, accompanied by erections inhibiting synthesis and release ofdopamine, thereby de­ and even ejaculations. Modell (1989) reported the case creasing dopaminergic transmission. of a 30-year-old woman taking fluoxetine (Prozac, a Holmgren and Urba-Holmgren (1980) proposed that serotonin reuptake blocker) whose frequent yawning was two sets of dopaminergic and cholinergic neurons, lo­ associated with such signs of sexual arousal as clitoral calized in the brain, are organized in series with the for­ engorgement and moderate orgasms. No relationship be­ mer tonically inhibiting the latter. Cholinergic neurons tween estrogen and yawning has been found in rats (Holm­ exert a direct excitatory influence on a hypothesized cen­ gren, Urba-Holmgren, Aguiar, & Rodriguez, 1980) or tral motor pattern generator for yawning. In this model, monkeys (Phoenix & Chambers, 1982),whereas in guinea low doses ofapomorphine, by activating dopamine pre­ pigs estrogen antagonizes yawning induced by apomor­ synaptic autoreceptors, produces yawning by disinhibi­ phine (Rodriguez et al., 1981). tion ofthe cholinergic excitatory neurons. Higher doses Chambers and Phoenix (1980) found a positive corre­ ofdopamine agonists directly inhibit the cholinergic neu­ lation between testosterone levels and rate of sponta­ rons, suppressing yawning. neous yawning by aging male rhesus monkeys. Gener­ Negative and positive modulating influences by nor­ ally among nonhuman primates, males yawn considerably adrenergic, glutamatergic, and serotonergic mechanisms more frequently than do females (Bertrand, 1969; De­ have also been demonstrated (Holmgren & Urba-Holm­ putte, 1978, 1994; Goy & Resko, 1972; Hadidian, 1980; gren, 1980; Lanthorn & Isaacson, 1979; Urba-Holrn­ Hall & Devore, 1965; Redican, 1975). Deputte (1994) gren, Holmgren, Rodriguez, & Gonzalez, 1979; Yamada reported that mangabey males yawned six times more & Furukawa, 1981).Dourish and Cooper (1991) proposed often than females, whereas in macaques the ratio was FUNCTIONS OF YAWNING 203 eight times more. Such results suggest the possibility Geldmacher (1987) in which subjects breathed air mix­ that yawning (or gaping) may serve as an aggressive tures containing more than normal amounts of carbon threat display, since in these primate species the canine dioxide (3%-5%); their rate of breathing increased but teeth ofmales are much more prominent than in females. the frequency of yawning was unaffected. Exercise that Troisi et al. (1990) found that yawns were associated doubled their rate ofbreathing also had no effect on sub­ with intermale threats. Packer (1979) observed that an jects' yawning frequency. Conversely, subjects breathing adult male baboon yawned less frequently after one ofits pure oxygen did not show decreased yawning. It seems prominent canine teeth broke. In our species, Schino and clear that yawning is something more than an odd kind Aureli (1989) reported no differences between yawning ofrespiration. frequency of males and females; the canine teeth of human males are not noticeably larger or more threaten­ Cerebral Blood Flow ing than those offemales. In 1881, Russell (cited in Heusner, 1946, p. 159) pro­ Yawning appears to be associated with hormonally in­ posed that yawns may "effect a stimulation ofthe brain duced stretching, gaping, and penile erection, which are through increased activity of the circulation." Changes clear signs of increased arousal. It is not clear which in intracerebral flow ofblood are almost certain to bring comes first, but peptide and steroid hormones appear to about changes in cortical arousal. Decreased intracere­ be involved in yawning that is associated with both ag­ bral blood flow produced by hemorrhage (Barbizet, gressive threats and sexual arousal. 1958) and motion sickness (Johnson & Jongkees, 1974) are accompanied by increased yawning. Karasawa et al. Yawning and Respiration (1982) monitored cerebral blood flow and EEG ofthrom­ Greco et al. (1993) found that most oftheir survey re­ bosis patients and found that yawning occurred under spondents believed that too little oxygen or too much two circumstances: when EEG indicated low cortical carbon dioxide were the main causes of yawning (i.e., arousal and when partial pressure ofoxygen in the carotid the respiratory hypothesis). At best, the respiratory hy­ artery decreased. Such a pattern is certainly consistent pothesis is incomplete-for example, both boredom and with the hypothesis that yawning affects arousal by seeing other people yawn are potent causes of yawning. bringing about an increase in intracerebral blood flow. Breathing faster or more deeply is a more effective way Askenasy (1989) has proposed an elaborate way in of increasing oxygen intake and expelling carbon diox­ which the act of yawning might increase cerebral blood ide than a single deep inspiration, especially since a pe­ flow. According to this hypothesis, inhaling stretches riod ofapnea usually follows a yawn (Hauptmann, 1920; bronchial muscles and stimulates vagus nerve terminals Lehman, 1979). Nevertheless, the hypothesis has been that bring about dilation of arterioles via cholinergic widely held since its mysterious origins in the 19th cen­ pathways. This decreases resistance to peripheral circu­ tury (Dumpert, 1921). lation and enhances blood flow. Gaping ofthe jaw con­ Yawning is more complex than simply opening the tracts the lateral pterygoid and soleus muscles, which mouth and breathing in deeply, although some of the empties rich venous plexuses contained in them (the physiological results are similar. Greco and Baenninger plexuses are sometimes referred to as "peripheral hearts"). ( 1991) found that wide opening of the mouth and deep This action ofthe jaw muscles enhances venous return, breaths produced changes in skin conductance and heart which promotes blood hyperoxygenation and thus stim­ rate that were initially similar to changes produced by ulates cerebral blood flow (including the ascending retic­ full yawns, but the patterned action of a yawn may be ular activating system). Although this mechanical hy­ controlled by a different neural mechanism. Gschwend pothesis provides a plausible explanation of how (1977) reported on a patient with a transsecting glioma yawning may be related to arousal, any direct evidence ofthe pons who was able to yawn normally even though for it is still lacking. he was unable to open or close his mouth voluntarily. Periods of apnea are not followed by compensatory Middle and Inner Ear Events yawning after breathing is resumed, as the respiratory Laskiewicz (1953) proposed that yawning served to hypothesis would require. In mammals, the normal pat­ adjust air pressure in the middle ear. However, although tern of breathing includes relatively shallow breaths in­ people may be observed to yawn in high-speed elevators, terrupted by occasional sighs. In the absence ofsighs or especially if they have respiratory infections that block deep breaths, this shallow breathing pattern may result in the Eustachian tube, it is a cumbersome alternative to the areas of atalectasis (similar to collapse), with diminished simple act of swallowing (which also opens the valve compliance and hypoxemia in the alveoli of the lungs arrangement in the Eustachian tube). (Mead & Collier, 1959). Thet, Clerch, Massaro, and Mas­ Involvement of the inner ear is suggested by the fact saro (1979) found that a single large inflation removed that motion sickness is accompanied by yawning (Gray­ areas of atalectasis that occurred during 2 h of normal biel & Knepton, 1976; Johnson & Jongkees, 1974), as is ventilation in excised rat lungs, a finding replicated by car sickness (Nakanishi, Hinoki, Ito, Izumikawa, & Baron, Nicholas, Power, and Barr (1982). 1980). Deaf-mute people with congenitally incomplete The clearest evidence against the respiratory hypoth­ labyrinths of the inner ear are immune to motion sick­ esis comes from a laboratory study by Provine, Tate, and ness and the accompanying yawning (Johnson & Jong- 204 BAENNINGER kees, 1974). Motion-produced sickness is associated with to Greco et al. that yawning was associated with driving pooling ofblood in lower parts ofthe body and, as these more than with any other daytime activity except sitting authors suggested, yawning may therefore be a way of in lectures. Although none of the studies is conclusive compensating for decreased intracranial blood circula­ by itself, there seems little doubt that transitions in ac­ tion by increasing venous return to the heart. Thus, inner tivity are associated with yawning. Whether yawning ear involvement may lend further support to the idea that causes arousal or activity changes or such changes cause yawning is a way ofregulating cerebral blood flow (and yawning is not yet clear. thus arousal). Threats, Conflict, or Stress The Tonsillar Hypothesis Baenninger (1987) found that male Siamese fighting McKenzie (1994) proposed that yawning is a reflex fish, a species with an elaborate threat display, yawned muscular contraction that ensures intermittent evacua­ frequently during aggressive encounters but never when tion ofthe palatine tonsillar fossae, thereby ensuring that alone. Darwin noted that "baboons often show their pas­ the tonsils are exposed to new antigens and preventing sion and threaten their enemies .. , by opening their excessive accumulation of foreign material, microor­ mouths widely as in the act ofyawning" (1873, p. 136). ganisms, and inflammatory products. Since the palatine Troisi et al. (1990) found that in addition to sleep/wak­ tonsils appear to lack an evacuating reflex, but are lo­ ing transitions, yawns by M.fascicularis and M.fuscata cated in a dark, moist environment where they are ex­ were associated with intermale threats, conflict, and anx­ posed to masticated food and bacteria, they should be iety, findings replicated by Mastripieri, Schino, Aureli, chronically infected. They are not, and McKenzie sug­ and Troisi (1992). These authors suggested that yawning gested that yawning may be a reflex to clear the tonsils may be an example ofa displacement act reflecting psy­ of infectious materials. He provided no data relevant to chosocial stress, a state that is certainly congruent with his ingenious suggestion. In an unpublished study I found arousal. no relationship between yawning frequency and whether Deputte (1994) reported that "emotion" yawns fol­ respondents had tonsils or not. lowed social interactions, particularly in tense con­ frontations between males, while Hadidian (1980) found ENVIRONMENTAL CAUSES OF YAWNING that dominant males yawned much more than others in the macaque troops he observed. Findings in other non­ Transitions human primate species also support the association of Troisi et al. (1990) found that yawns by Macaca fas­ yawning with arousing encounters between males (Hall, cicularis and Mifuscata were associated most often with 1962; Hinde & Rowell, 1962). transitions between sleep and waking. Myrberg (1972) found that damsel fish Eupomacentrus partitus yawned Boredom and Sleepiness during transitions between their different activities, It is not surprising that boredom, inactivity, and lack while Baenninger (1987) reported that zoo-housed lions ofinterest are associated with yawning. Students in lec­ Panthera leo and mandrills Papio sphinx yawned more ture classes yawn at a much higher rate than those in aer­ frequently just before feeding time, a result that was obics classes, dining halls, or libraries (Baenninger, replicated in laboratory rats by Holmgren et al. (1991). 1987). More frequent yawning is associated with view­ Moyaho, Eguibar, and Diaz (1995) found that yawning, ing uninteresting, repetitive stimuli than with viewing grooming, and emotional reactivity of laboratory rats interesting stimuli (Provine & Hamernik, 1986). Ifmain­ were all associated with arousal variation. Breeders and taining wakefulness is important, yawning may be a way owners ofdogs and cats have reported that yawning and to remain awake and attentive, even when physical or stretching normally occur during transitions from rest­ mental stimulation is lacking. ing to waking or exercising. Deputte (1994) found that Existing data do not unambiguously support an asso­ 90% of yawns were associated with rest/activity transi­ ciation between yawning and sleepiness. Skorzewska tions during nearly 800 h in which he observed two et al. (1993) found no significant correlations between species ofOld World monkeys. sleepiness scores of subjects who were injected with In humans, frequent yawning follows awakening in scopolamine and their yawning frequency. Baenninger the morning or attempting to stay awake in late evening and Greco (1991) found no correlations between fre­ (Greco et aI., 1993; Provine et al., 1987). Awakening quency ofyawning by laboratory subjects and the num­ during the night was also followed by yawning and sub­ ber ofhours slept the previous night. sequent activity (Baenninger et al., 1996). Subjects in During actual sleep, yawning apparently does not this last study wore activity monitors for 2-week periods occur at all, according to Lal, Grassino, Thavundayil, and almost invariably increased their activity rate within and Dubrovsky (1987). This is what the arousal hypoth­ 15 min after yawning. Dumpert (1921) reported that pa­ esis would predict, since the struggle to maintain wake­ tients yawn when returning to conscious awareness after fulness has been abandoned by a sleeping individual. being hypnotized. Finally, driving automobiles requires Sleep includes different phases, however, and during frequent transitions between active concentration and REM or "paradoxical" sleep, the EEG record shows a passive boredom. Subjects who kept activity logs reported cortical arousal pattern that is more similar to the wak- FUNCTIONS OF YAWNING 205

ing state than to the patterns during slow wave sleep. If (1989). Penile erection and yawning induced by oxytocin and related the arousal hypothesis of yawning is correct, we might peptides-Structure-activity relationship. Peptides, 10, 559-563. expect to find yawns occurring in conjunction with tran­ ASKENASY,1. J. (1989). Is yawning an arousal defense reflex? Journal ofPsychology, 123, 609-621. sitions from slow wave to REM sleep phases. This would BAENNINGER, R. (1987). Some comparative aspects of yawning in be an important test ofthe arousal hypothesis. Betta splendens, Homo sapiens, Panthero leo, and Papio sphinx. Journal ofComparative Psychology, 101,349-354. Contagion, Suggestion, or Social Facilitation BAENNINGER, R., BINKLEY, S., & BAENNINGER. M. (1996). Field ob­ servations ofyawning and activity in humans. Physiology & Behav­ Although the contagiousness of yawning is apparent ior, 59, 421-425. in social situations, this phenomenon is difficult to study BAENNINGER, R., & GRECO, M. (1991). Some antecedents and conse­ in the laboratory because subjects appear reluctant to quences ofyawning. Psychological Record, 41, 453-460. yawn when being observed (Greco & Baenninger, 1989). BARBIZET, J. (1958). Yawning. Journal ofNeurology, Neurosurgery & Laboratory subjects did not yawn in response to seeing Psychiatry, 21, 203-209. BARTHALAMUS. G., & ZIELINSKI, W. (1988). Xenopus skin mucus in­ live or televised actors yawn while reading uninteresting duces oral dyskinesias that promote escape from snakes. Pharma­ material (Baenninger, 1987). In an unreplicated study, cology, Biochemistry & Behavior, 30, 957-959. Moore (1942) reported some contagious yawns in the BERENDSEN, H. H., & NICKOLSON, V.J. (1981). Androgenic influences laboratory, in church services, and during a film. He also on apomorphine induced yawning in rats. Behavioral & Neural Bi­ ology, 33,123-128. found that some blind subjects yawned in response to an BERTOLINI, A., VERGONI, W., GESSA, G. L., & FERRARI. W. (1969). In­ audio recording ofyawns. It is not known whether con­ duction of sexual excitement by the action of ACTH in brain. Na­ tagious yawning requires awareness ofthe stimulus, al­ ture, 221, 667-669. though Heusner (1946) asserted that it could be activated BERTRAND, M. (1969). The behavioral repertoire ofthe stumptail at "subconscious levels." Thinking or reading about macaque. Basel: Karger. BLANTON. M. G. (1917). The behavior ofthe human infant during the yawning is a stimulus for the actual performance ofthe first 30 days of life. Psychological Review, 24, 456-483. act (Baenninger & Greco, 1991; Greco & Baenninger, CHAMBERS. K. C; & PHOENIX, C. H. (1980). Diurnal patterns oftestos­ 1991; Provine, 1986). terone, dihydrotestosterone, estradiol and cortisol in serum of rhe­ sus males: Relationship to sexual behavior in aging males. Hor­ mones & Behavior, 15,416-426. Yawning and Arousal CLEMENTE, C. D. (1985). Gray s Anatomy (30th ed.). Philadelphia: Lea The hypothesis underlying this review is that an im­ & Febiger. portant function ofyawning is to modify levels ofcorti­ COWAN, A. (1978). Cholinergic link in yawning. Nature, 271,187-188. cal arousal, especially in situations where there is little CRAEMER, E (1924). Uber Sodbrennen und Gahnen. Gastroenterologia external stimulation and where a low level of arousal Archiv fiir Verdauungskrankheiten, 33,149-162. DARWIN, C. (1873). Expression ofemotions in animals and man. New could be costly or dangerous. Most of the findings re­ York: Appleton. viewed have been consistent with this hypothesis. Yawn­ DEPUTTE, B. (1978). 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Neural basis ofdrug induced arousal, especially with respect to sexual arousal, inter­ yawning. In S. J. Cooper & C. T Dourish (Eds.), Neurobiology of male threat displays, and conflict. stereotyped behavior (pp. 91-116). Oxford: Oxford University Maintaining or attaining a particular level ofarousal is Press, Clarendon Press. an important matter in the life of most vertebrates, and DULBECCO, R. (1991). Encyclopedia ofhuman biology. San Diego: Ac­ ademic Press. yawning, to the extent that it serves as a means for doing DUMPERT, V. (1921). Zur Kenntnis des Wesens und der physiolog­ so, should be seen as an important part of adaptive be­ ischen Bedeutung des Gahnens. Journal fiir Psychologie und Neuro­ havior. The physiological, ontogenetic, and phylogenetic logie, 27, 82-95. findings reviewed here are consistent with this view. FELDMAN. J. E, BRODY, N., & MILLER, S. A. (1980). Sex differences in non-elicited neonatal behavior. Merrill-Palmer Quarterly, 26, 63­ 73. 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(Manuscript received November 8,1995; SMOTHERMAN, W. P.,& ROBINSON, S. R. (1987). Prenatal expression of revision accepted for publication November 15, 1996.)