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Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal

mise à jour du
3 octobre 2010
South African Journal
of Science

Yawning and the Thyroid Gland
A. Pellatt, P. G. Wright and L. S. Levine
Department of General Anatomy
Department of General Physiology, School of Dentistry
University of the Witwatersrand, Johannesburg, South Africa


In this article, the phenomenon of yawnng is reviewed, and its associations are indicated and discussed. The possibility that the thyroid gland may be compressed during yawning with the resultant liberation of thyroid hormones is subsequently tested exiperimentally in the baboon. The results obained give no support to this hypothesis and it seems likely that the function of yawning will remain a mystery for some time.
The phenomenon of yawning has attracted sporadic speculation for many years. Certain clinical and physiological associaions have been noted, but these have never been subjected to deliberate experimental inquiry. Darwin in 1872, described the act shortly, noted that it sometimes had an association with slight fear and was impressd by the excretion of tear fluid which often accompanied it. He offered no explanation for yawning.
Cramer observed that the familiar gaping movements of fishes, amphibians and repiles simulate yawning in man, and both he and Heinroth believed that true yawning occurs in birds. Heusner, in his review of he subject, stated that true yawning takes place in primates and carnivores but not in herbivores. Jones noted that ungulates, which do not sleep in a relaxed position, or which even sleep whilst standing, do not yawn.
Yawning in man has many associations but it is difficult to discern any unifying theme amongst them. By common experience yawning is most frequently associated with physical or mental tiredness. The greater the degree of such tiredness the more frequent and more pronounced is the yawning: indeed, on occasions, yawning is rapidly repeated and almost uncontrollable. Surprisingly, yawning is also often marked after awakening from sleep, either immediately or after a short interval. Boredom, a sort of psychic tiredness such as may occur during prolonged endurance of enervating company, may be associated with repeated yawning - perhaps, as sugested by G. K. Chesterton, a sort of frozen yell! During states of anxiety and fear yawning is also not infrequent.
Clinicians have long noted certain morbid associations. Nausea is often accompanied by marked yawning, especially when a duodenal ulcer is present. Several observers have remarked upon the frequency of yawning after severe haemorrhage from any cause. Both hypoxia and arterial hypotension were invoked by Nash11 to explain this, but there are no supporting experimental data.
Hunger and hypoglycaemia are frequently associated with yawning. Increased rates of yawning have been noted in hysteria and in certain epileptic aurea.
Paroxysmal yawning may occur in encephalitis and in the presence of expanding intracranial lesions, notably cerebellar abscess or More recently, yawning has been artificially induced in cats, dogs and monkeys by intracisternal or intraventricular injections of corticotropin and melanotropin or physostigmine. The effect was most marked when injection was made into the third ventricle or into those hypothalamic areas closest to the hypophysis. This correlates with the findings of Waldvogel, who induced yawning by electrical stimulation of the same region.
Finally, there is an association between maleness and yawning. Hall noted that adult female monkeys 'rarely if ever' yawned; Urbá-Holmgren et al. noted a 6:1 ratio in physostigmine-induced yawning between males and females; Phoenix et al. recorded a dramatic drop in frequency of yawning in male rhesus monkeys following castration, the drop being immediately and completely reversible by replacement therapy with testosterone. Johnson and Phoenix recorded a dramatic increase in yawning rate in ovariectomised female rhesus monkeys given testosterone.
Personal observations confirm this association between maleness and yawning in the case of the Chacma baboon. In the course of many hours of observation by one of us (A.P.), the female baboon has never been seen to yawn, whereas the male yawns on the average 10 to 12 times every hour.
Although no unifying concept can at present causally link all these associations with yawning, several hypotheses have been advanced concerning its possible physiological significance. Most prominent amongst these and generally held also by lay persons, is that yawning effects an increase in lung aeration; that the oxygen level in the blood is thereby raised and the oxygen supply to the brain increased. Ganong states that it has also been suggested that stretching of the lung during inspiration opens up underventilated alveoli and prevents atelectasis. He also notes that yawning increases venous return to the heart, as does any deep inspiration.
None of these ideas has been subjected to experimental test, but a priori it seems unlikely that lung aeration and blood oxygenation are much increased by yawning. Mayer and Hauptmann argue that yawning effects no ultimate increase in lung aeration, because the apneic period which follows a yawn more than compensates for any temporary increase in aeration afforded by a single deep breath. Furthermore, a few simple deep breaths would be far more economical in increasing pulmonary aeration than is yawning, with its complex involvement of numerous groups of nonrespiratory muscles. It is conceivable that paroxysmal yawning may cause a significant increase in blood oxygenation, but no figures are available.
It has also been suggested, by Last, that a yawn may promote venous flow from the base of the brain and cranium where flow may tend to be sluggish, partly by the normal increase in venous return to the thorax during inspiration and partly by compression of the pterygoid venous plexus by the lateral pterygoid muscle which contracts during opening of the mouth. As a behavioural phenomenon, yawning has also been interpreted as a threat signal, especially in baboons, and somewhat whimsically as a relic of pre-language evolution, when it was perhaps used as a community signal that the time for sleep had arrived!
Finally, Heusner in his 1946 review mentioned that he had heard the suggestion that, as certain muscles in the neck squeeze upon the thyroid gland during a yawn, they cause expression of excess thyroxine into the blood and thereby accelerate metabolism. He was, however, unable to find any reference to this idea in the literature.
Anatomical considerations
Arising from work on the facial muscles of the Chacma baboon (Papio ursinus), the present authors came independently to consider the same hypothesis of thyroid gland compression as that suggested by Heusner. The male baboon is probably the most inveterate yawner in the animal kingdom. Captive male baboons may yawn at a mean rate of some 10 to 12 times an hour, and rates as high as 24 times an hour have been recorded. Associated with the high rate of yawning and with the markedly elongated, heavy jaws of the baboon is the very great development of the platysma muscle - relatively bigger in all dimensions than in any animal of comparable size. The muscle is the main mandibular depressor in the baboon.
Anatomical analysis, however, shows that, whilst mandibular depression (that is, opening of the mouth) may constitute the most impressive external feature of a yawn in both baboon and man, it is certainly not the most essential feature - at any rate not in man, who is quite capable of yawning with the mouth closed, as is sometimes dictated by social custom.
The essential movement in any yawn is depression of the larynx and hyoid bone by the infrahyoid muscles - sternohyoid and omohyoid. Indeed, as Mayer noted and as can be easily confirmed by palpation, descent of the larynx occurs at the onset of a yawn, the larnyx reaching its lowest point almost immediately and being held there until after the acme of the yawn. Opening of the mouth simply assists this laryngeal descent by relaxing the suprahyoid musculature, whilst the subjective sensation of dilation of the pharynx is due merely to its passive stretching by the down-going larynx, since the pharynx is not provided with dilator muscles.
Numerous other muscles may contract during a yawn but these are not dealt with here as they are not essential to the act. Even contraction of the diaphragm, which usually causes a prominent inspiration during the initial phase, can by voluntary effort be almost completely inhibited. The only absolutely essential and ineradicable movement, the sine qua non of a yawn, is descent of the larynx. So marked, indeed, is this descent that even in persons with long necks the lower half of the larynx may pass into the thorax behind the manubrium sterni, while in those with short necks virtually the entire larynx becomes intrathoracic. Contraction of the diaphragm, whatever may be the significance of the resulting inspiration, contributes to the laryngeal descent by traction on the trachea.
The thyroid gland is firmly attached to the thyroid cartilage by relatively dense areolar tissue, by expansion of the pretracheal fascia which envelop it, and by the sternothyroid muscle. All three of the major infrahyoid muscles (sternohyoid, sternothyroid and omohyoid) overlie the thyroid gland. Sternothyroid has a particularly intimate relationship, because, in addition to delimiting the upper margin of the lateral lobe of the gland by its attachment to the cartilage, it also completely envelops the outer surface of the lobe. With this arrangement of the infrahyoid muscles relative to the gland, it seems probable that during a yawn the gland is not only drawn down with the larynx, but also subjected to pressure by the overlying infrahyoid muscles (especially sternothyroid) and by being squeezed into the narrow confines of the thoracic inlet. Compression of the thyroid gland in this manner would probably augment the flow of venous blood from it, and thus promote the outflow of preformed thyroid hormones into the circulation.
Two facts are relevant here: the thyroid gland has one of the highest rates of blood flow in the body; and the gland is placed adjacent to the large internal jugular vein and drains by short, wide channels into this, or downwards directly into the large brachiocephalic veins. Thus thyroid hormones are passed into the rapid jugulobrachiocephalic blood stream as quickly as possible. Any external pressure on the gland would tend to augment this outflow of thyroid hormones, a point well taken by the surgeon who is excising a toxic goitre. Undue pressure on a gland which has not been modified by iodine treatment during thyroidectomy is very likely to result in development of a thyroid 'storm' or 'crisis' during the early postoperative period, as a result of flooding of the circulating blood by expressed thyroid hormones. It is therefore postulated that yawning may be a natural means of exerting moderate pressure on the thyroid gland, thereby promoting expression of preformed thyroid hormones into the circulation in response to multifactorial stimuli arising from hypotension,' nausea, haemorrhage or tiredness. As a preliminary test of this hypothesis, an experiment was designed, in which measurements of the triiodothyronine (T3) level in thyroid venous blood were made before, during and after simulated yawning in adult male Chacma baboons (Papio ursinus).
Materials and methods
Four experiments were carried out. On the first three occasions ajarge, fully adult male baboon (mass 32 kg) was used, whereas the fourth animal was subadult male (mass 23 kg).
Experiment I
The animal was sedated with ketamine hydrochloride (Parke-Davis, 200 mg I.M) and anaesthesia was induced and maintained with pentobarbitone sodium (May Baker) IV. throughout the experiment.
Through an anterior paramedian incision in the right side of the neck, the right internal jugular vein was exposed and dissected free over a length of approximately 60 mm. This length lay adjacent to the lateral lobe of the thyroid gland and received the large middle thyroid vein. Temporary silk snares were placed around the vessel at upper and lower extremities of the exposed section and held in place with clamps. These snares could be tightened to occlude flow in the vessel or loosened to permit its resumption.
A polythene catheter of approximately 2 mm internal bore was introduced into the prepared section of vein so that its tip lay near the ostium of the middle thyroid vein. The other end of the catheter was connected to a 5cm3 syringe, into which blood could be withdrawn.
Yawning was simulated by stimulation of the nerves to the infrahyoid muscles. The ansa cervicalis, composed of contributions from cervical spinal nerves C1, C2 and C3, was dissected free. Its branches to the infrahyoid muscles (sternohyoid, sternothyroid and omohyoid) were identified and the ansa transected in two places above the origin of these branches.
The distal ends of the ansal nerves were secured across silver/silver chloride electrodes. Stimulation by 0.2 ms square pulses of 10 V at 40 Hz produced full mandibular depression. Three 10-s periods of stimulation, separated by 10-s intervals, were employed and blood was withdrawn during the cycle. As indicated in Fig. 1 by black arrows, six of the samples were withdrawn during such stimulation, withdrawal of the sixth being accompanied by manual compression and massage of the thyroid gland. The remaining 17 samples served as controls.
Five millilitre samples of thyroid venous blood were withdrawn over one-minute periods and transferred to centrifuge tubes in ice. Coagulation was prevented by heparin (Boots). After centrifugation for S mm, separated plasma was withdrawn and frozen.
Triiodothyronine (T3) was assayed by radioimmunoassay using the T3 RIA (PEG) kit from the Radiochemical Centre, Amersham.
Experiment 2
Because the results of experiment 1 showed decreasing levels of T3 in the series of samples, it was suspected that anaesthesia with pentobarbitone might be the cause, as indicated by Pitt-Rivers and Trotter.
The procedure was therefore repeated using ketamine hydrochloride and omitting any stimulation of the infrahyoid muscles, in order to observe the undisturbed output of T3. Anaesthesia was induced with ketamine hydrochloride (400 mg l.M.) and maintained with 100 mg I.V. at 15-min intervals. Surgical details and sampling procedure were identical to that in experiment 1, except that only 20 samples of blood were taken. Radioimmunoassay was performed as before.
Experiment 3
Because results in experiment 2 indicated a reasonably basal level of T3 in the series of samples, it was decided to repeat the experiment, using only ketamine hydrochloride anaesthesia and again stimulating the ipsilateral infrahyoid muscles.
Anaesthesia was induced with ketamine hydrochloride (400 mg 1.M.) and maintained with 100 mg 1.V. at 15-min intervals. Surgical and sampling procedures were as described for the two earlier experiments. Ten blood samples were taken during simulated yawning, preceded and followed by five control samples. Radio immunoassay was performed as before.
Experiment 4
Results in experiment 3 showed no increase in T3 output during stimulation. It was considered that there might be shunting of thyroid blood from the sampling and stimulation side (right) to the cotralateral side, as a result of unilateral compression of the gland. It was therefore decided to pérform a final experiment, applying the stimulus to the infrahyoid muscles of both sides and sampling blood from both sides of the thyroid gland simultaneously.
Induction and maintenance of anaesthesia using ketamine hydrochloride was as detailed in experiment. Bilateral surgical exposure and cannulation of the internal jugular veins was performed. Samples of 2.5 cm3 were withdrawn from each internal jugular vein and these were then pooled to make combined samples of 5 cm3 each. Ten samples were taken during simulated yawning, preceded and followed by five control samples. Radioimmunoassay was performed as before.
Results and discussion
The T3 activity of the blood-samples for each experiment is shown in Fig. 1. It is apparent that simulated yawning produced by nerve stimulation did not alter the T3 concentration of the thyroid venous blood.
The results give no support to the hypothesis that yawning is a device for muscular compression of the thyroid gland at times when augmentation of thyroid hormone outflow might be appropriate. In particular, the results of experiment 4, during which possible anaesthetic effects and escape of venous blood to the contralateral side had been eliminated, show a remarkably constant T3 level.
In experiment lit was perhaps surprising that even manual compression and massage of the gland caused no detectable increase of T3 in the issuing venous blood, in view of the clinical experience of thyroid 'storm' or 'crisis'. However, When the depressant effect of pentobartitone anaesthesia is considered, it may be that production of T3 was diminished and there was little or. no available T3 to be expressed.
The physiological significance of yawning therefore remains unelucidated. The question arises; does artificially induced contraction of the infrahyoid musculature exactly mimic that which occurs during a natural yawn? It seems unlikely that it does, since observation of mandibular and laryngeal movement during simulated yawns showed it to be of sudden onset and almost immediate maximal intensity. The rapid opening movement was unlike the controlled, relatively gradual development of muscular force and laryngo-mandibular descent seen during an ordinary yawn. It may therefore be that any resulting compression of the thyroid gland in these experiments does not mimic that caused by a normal yawn. Although these results offer no support for the hypothesis, they cannot be regarded as conclusive evidence against the idea. However, if normal yawning does have an effect it is remarkable that simulated yawning and compression produced no discernible change.
It seems likely, therefore, that yawning will remain a mystery for some time. Heusner ends his 1946 review by noting those aspects of the problem which at that time still remained completely unexplored, namely, 'the behaviour of the cerebral circulation; measurements of cardiac filling and output; the chemistry of the respiratory component; the nature of the motor discharge in the stretch component, and the possibility of endocrine (e.g. thyroid) changes' adding 'Until such observations are completed, any formulation of the physiological significance of this act will rest upon an insecure foundation'.
The work here reported explores to some extent Heusner's last aspect, albeit inconclusively. In view of the 'apparently nonsignificant nature of the act of yawning it seems improbable that much interest will be aroused in the future. The mystery may remain - a big yawn!