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.
Introduction
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.
Associations
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.
Hypotheses
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!
