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mise à jour du
20 octobre 2002
Nature
19 may 1977; 267
et
Nature
12 jan 1978; 271
Is yawning a cholinergic response ?
R Urba-Holmgren, RM Gonzalez, B Holmgren
Centro Nacional de Investigaciones Cientificas, Apartado 6990, La Habana, Cuba
 Departamento de Ciencias Fisiolbgicas, Instituto de Ciencias, Universidad Autônoma de Puebla, Puebla (Mexico)
Tous les travaux de MR Melis & A Argiolas 
Tous les travaux de M Eguibar & G Holmgren
Chat-logomini
Barbizet was perhaps right in suggesting that the commonplace, ubiquitous and apparently non-significant of the act of yawning, might have contributed to the relative lack of attention given by physiologits to this behavioural phenomenon. The physiological signifiance of yawning and the nervous mechanisms triggering and coordinating its various components remain unclear. Frequent yawning has been mentioned as a symptom in some diseases of the central nervous system, particularly in cases of frontal tumours and encephalitis. A stretching and yawning syndrome has been observed in cats, dogs and monkeys after intracisternal or intraventricular injections of adrenocorticotrophic and melanotrophic hormones, or synthetic polypeptides with ACTH and/or MSH activities, but the relation of these observations to the basic mechanism of yawning has not been stutied. During experiments designed to explore cholinergic potentiation of d-amphetamine induced head-shaking in infant rats, we have made some observations that indicate the involvement of central cholinergic response in yawning.

Infant rats, from 6h after birth up to 14 d old, were ijected intraperitoneally (ip) with physiostigmine salicylate (0,1 mg of the free base per kg body weight, dissolved in 0,9%NaCl to a total volume of 0,01 ml per g body weight). The rats began to yawn about 5 mn after injection. In the following 15 mn the number of yawns reached an average of 10-12 during first 10 d of life. Some animals yawned twice per minutes, and others only a couple of times in 15 mn. In rats aged under 10d physiostigmine induced yawning was practically universal. Between days 10 and 14 of life the frequency of yawning fell rather steeply, to a levelof only 2 or 3 yawns per 15 mn, with some animals showing no yawning reponse. At the 14th day yawning occurence had decreased to 69% of the population. Each yawn was preced by salivation, licking of the forepaws and cleaning movements of the snout, or "gomming" or chewing movements, and sometimes by a sudden stretching of the forelimbs. The yawn itself was a slow wide opening of the mouth, with marked protrusion of the toungue, and lasted about 3-4 s.

A dose effect graphe of physiostigmine induced yawning in 9d old rats is show fig 2. That this particular action of the anticholinesterasic drug is centrally mediated is strongly suggested by control experiments with neostigmine methylsulphate, which passes the blood-brain barrier with difficulty. When injected i.p., in a dose of 0.2 mg per kg, neostigmine induced only 1.6 yawns per 15 min (12 animals). Although this effect is significantly different from that observed in rats injected with saline (P<0.01) it was only of the order of one-sixth of the effect obtained with physostigmine. With higher doses of neostigmine no yawning was observed. Pilocarpine hydrochloride, a cholinomimetic drug that passes readily into the brain, induced yawning up to the same level as physostigmine.

Cholinomimetically induced yawning seems to be due to the stimulation of central 'muscarinic' receptors ' because it is rapidly and completely blocked by scopolamine hydobromide, at doses of 2.5 to 5 mg per kg (Fig3). That 'nicotinic' cholinergic receptors are not participating was demonstrated with nicotine administered by i.p. injection. Doses of nicotine (0.1 mg/kg) which induced clear central effects on head-shaking (unpublished observations) did not induce yawning.

We observed physostigmine induced yawning at a more or less stable level of 2-3 yawns per 15 mn in rats from 14 to 90 d of age, but practically only in males. In a pool of 62 animals (31 females and 31 males, 14 to 5.4 d old) from the same litters, males performed an average of 3.1 yawns in 15mn after physostigmine injection, whereas females, performed 0.5 yawns in the same period. The difference is highly significant, (P<0.002) by the Mann-Whitney U test. It may be recalled that Hall, in his interesting description of the bebaviour of monkey towards mirror-images, in which "yawning" or "gasping" responses were very frequent, also observed that adult females "rarely, if ever yawned".

Our results suggest that in the rat thre is a central cholinergic mechanism, with muscarinic receptors, underlying the act of yawning. The mechanism matures at a very early age, suggesting that it is localised at the lower levels of the brainstem. Later development of higher placed cholinergic mechanisms may determine that other effects evoked by cholinomimetic agents injected systemically might be hindering the expression of yawning in olders rats. Intense and continous scratching, or tremor or rigidity, as produced respectively by pilocarpîne and physostigmine in rats aged over 10d, or some other central or peripheral actions affecting the level of vigilance, might be partially counteracting the yawn-inducing effect.

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Nature vol 271 12 january 1978

Cholinergic link in yawning A. COWAN Department of Pharmacology,Temple University School of Medicine, Philadelphia, Pennsylvania 19140

Holmgren et al, recently focused attention on the basic mechanism behind the act of yawning. They reported that physostigmine and pilocarpine induce yawning in young male rats and hypothesised that acentral cholinergic link may be involved in the reflex. Our results support surch proposal.

Yawning is a characteristic sign of with-drawal from morphine in man and monkeys. When naloxone (0.5 mg per kg bodyweight), but not physiological saline, was injected subcutaneously (sc) into three ex-addict baboons (two male and one female, 4.4 - 5.2 kg), 98 d after abrupt with-drawal of morphine, a low incidence of yawning (2-4 episodes) occurred within 15 min; on this occasion, other signs of long-term withdrawal were absent. Seven days later, the same baboons were again challenged with naloxone, 20 mn after physostigmine (0.05 mg per kg s.c.). Although this dose of physostigmine per se did not elicit yawning, with each animal there was a threefold increase in the incidence of yawning.

Although a cholinergic link may indeed be involved in yawning, it should be recognised that other factors are also important. Thus, dimethyltryptamine causes yawning after intramuscular administration t0 rhesus monkeys yet there is no evidence that this hallucinogen has marked effects on the cholinergic system in this species.

Urba-Holmgren and Holmgren reply

In Cowan's experiments 'with exmorphine addict baboons, although physostigmine 0.05 mg pet kg s.c. per se did net evoke yawning, this dose strongly potentiated naloxone-induced yawning. Perhaps a higher dose of physostigrnine (0. 10 mg per kg) would have elicited yawning directly even in monkeys, as it does in rats and in infant guinea pigs, kittens and dog pups (unpublished observations). In infant rabbits we have had te use a still higher dose (0.15 - 0.20 mg per kg).

We certainly agree with Cowan that other factors are also important in yawning. The stretching and yawning syndrome induced by ACTH and MSH is a well-known example. In recent experiments with (3,4 dihydroxyphenylamino)-2-imidazoline (DPI, Böhringer) we have observed that this drug, which according to Cools et al has a specific and potent agonistic activity at dopamine inhibitory receptors, in doses of 5 mg per kg intraperitoneally, elicits moderate, but statistically significant yawning in infant rats (from 9 to 15 d in age). It would berash at this stage, to hypothesise that drugs shown te elicit the yawning act necessarily through a final common path including a cholinergic link.

BIBLIOGRAPHIE
Tous les travaux de MR Melis & A Argiolas 
Tous les travaux de M Eguibar & G Holmgren
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  • Eguibar JR et al Behavioral differences between selectively bred rats: D1 versus D2 receptors in yawning and grooming Pharmacology, Biochemistry and Behavior 2003; 74; 827Ð832
  • Moyaho A et al Induced grooming transitions and open field behaviour differ in high and low-yavning sublines of Sprague-Dawley rats. Anim Behav 1995; 50 ; 61-72
  • Urba-Holmgren R, Trucios N, Holmgren B, Eguibar JR, Gavito A, Cruz G, Santos A Genotypic dependency of spontaneous yawning frequency in the rat Behav Brain Res 1990 Oct 30;40(1):29-35
  • Urba-Holmgren R, Santos A, Holmgren B, Eguibar JR Two inbred rat sublines that differ in spontaneous yawning behavior also differ in their responses to cholinergic and dopaminergic drugs Behav Brain Res 1993 Sep 30;56(2):155-9
  • Urba-Holmgren R, Holmgren B, Rodriguez R, Gonzalez RM Serotonergic modulation of yawning Pharmacol Biochem Behav 1979 Sep;11(3):371-2
  • Urba-Holmgren R, Gonzalez RM, Holmgren B Is yawning a cholinergic response? Nature 1977 May 19 267 (5608): 261-2 et commentaires Cholinergic link in yawning A Cowan Nature 12/01/78 271 p187-188
  • Urba-Holmgren R, Holmgren B, Leon BA, Ugarte A Age-dependent changes in serotonergic modulation of yawning in the rat. Pharmacol Biochem Behav 1992 Oct;43(2):483-6
  • Argiolas A Yawning and penile erection: central dopamine-oxytocin-adrenocorticotropin connection Ann N Y Acad Sci1988;525:330-7