Yawning is a common phenomenon
expressing certain physiological and
psychological states. It is a reflex act
involving the central nervous systema (CNS),
lungs, blood vessels, salivary and lacrimal
glands, respiratory (diaphragm and acessories)
and other skeletal muscles. Historically,
Hippocrates described yawning as an exhaustion
of the fumes preceding fever. In the early XVII
Century, Gallien and Oribase mentioned yawning
in their work. In the XIX Century, Charcot also
referred to yawning in his lessons on medicine.
Yawning is present in all mammals and at least
its mandibular form occurs in all vertebrates.
The earliest appearance of yawning in man was
observed in a 15-week-old embryo. Yawning is a
complex behavior not yet fully understood and in
man it is thought to relate more to boredom than
to feelings of physical fatigue. On the basis of
certain relevant clinical and experimental data,
a review of yawning appears to be justified.
DESCRIPTION. Once initiated, yawning
can not be suppressed but its manifestations can
be modified. In humans, yawning can be divided
in three distinct phases: a long inspiratory
phase; a brief acme; a rapid expiration
phase:
1) Inspiratory phase. Yawning may be preceded
by looking about, moving or arranging one's
hair. Then the lower jaw opens involuntarily
reaching maximal widening while a 4 to 6 seconds
deep inspiration drains air through both the
mouth and the nose. The nostrils flare, the
respiratory thoracic acessory muscles contract
in an increased inspiration placing a larger
volume of air in contact with the maximally
widened nasopharynx. The soft palate moves up
sealing rhinopharynx momentarily and the vocal
cords abduct maximally. The sub-hyiod muscles
contract bringing the tongue forward, descending
the hyiod bone to the level of the seventh
cervical vertebrae. The mid-inspiration closure
of the Eustachian tubes produces a transient
hypoacusia whercas the end-inspiratory opening
of the Eustachian tubes produces a clicking in
the cars. Yawning is usually associated wi th
vigorous stretching of the limbs, torso and
abrief shivering. During stretching, the soleus,
lateral pterygoids and the diaphragm muscles
contractemptying their voluminous venous plexus,
thus increasing the venous retum to the heart
with a slightof increase of the heart rat.
2) Acme. This brief phase only lasts 2 to 4s.
Extension of the neck, forced closure of the
eyes , lacrimation and salivation occur and a
vague sensation of pleasure is also described to
occur. A larger bolus of air is placed in
contact with the maximally exposed nasopharynx
at the acme.
3) Expiration. The acme comes suddenly to an
end, the muscles involved in the two previous
phases relax and a quick passive expiration
occurs and subsequenfly a brief apnea ensue.
MECHANISMS. Fatigue and boredom are
the two most potent stimuli causing yawning
whercas drowsiness is the most common cause of
it in humans. When the environment is boring and
no longer able to sustain the subject's
attention, the bored mind has to make an effort
to maintain contact with the surroundings. These
feelings of boredorn through the prefrontal
cortex modi fy the pattem of activity of the
brain stem reticular formation and of the brain
stem midline raphe serotoninergic system. This
generates a subjective sensation of drowsiness
which induces yawning. Various physiological
changes occur during yawning. Vigorous
stretching of limbs with contraction of the
lateral pterygoids, soleus, diaphragm and ether
muscles (the so-called peripheral hearts),
increase the venous retum to the right chambers
of the heart thus increasing the cardiac output
and consequently increasing cerebral blood flow.
The deep and prolonged inspiration phase of
yawning reverses hypoxia, hypercapnia and
alveolar collapse. The deep inhalation also
stretches the terminal bronchioles and alveoli.
This will also dilate bronchial musculature
stimulating the vae terminals, thus releasing
acetylcholine which in tum dilates the systernic
arterioles even further. The result is a
decreased peripheral resistance, increased
arterial cerebral blood flow, increased oxygen
saturation and decreased C02. Hyperoxygenation
and increased cerebral blood flow activate the
brain stem reticular formation leading to
increased alertness.
Yawning seems indeed to be an alerting
reflex. In that line, Karasawa et al showed that
in patients with occlusive cerebrovascular
disease yawning emerged when the EEG showed
slowing of the posterior background activity
occurring simultaneously with a mild hypoxemia.
Apparently, boredom, fatigue and drowsiness all
lead to hypovenfilation and mild hypoxia.
Yawning would be a response of the brain stem
reticular formation to reverse drowsiness and
tu, maintain attention and alertness.
Yawning is at the neuronal level the result
of concertedly functioning complex neuronal
networks whose anatomical center is most likely
located in the lower brain stem nearby the
brainstem reticular formation. The yawning
neuronal complex is interconnected with the
neuronal aggregates of: (a) respiratory neurons;
(b) motor nuclei of the 5 th, 7th, 10th, and
12th cranial nerves; (c) the phrenic nerve and
accessory respiratory muscles; (d) the
parasympathetic terminals of the lacrimal
glands; (e) the frontal cortex. In favor of this
anatomic location there is the report by
Geschwend who described a tetraplegic patient
with a pontine glioma who could not open his
mouth spontaneously but was able to yawn.
Opening of the mouth through the motor cortex
was impossible but reflexogen yawning was still
possible because of the short interconnections
between the reticular neurons and the motor
axons of the fifth and seventh cranial nerves.
Another tetraplegic and locked-in syndrome
patient suffering from a glioma of the anterior
pons could yawn but could not open his mouth
voluntarily. The preservation of the reticular
formation network made yawning possible whereas
the interruption of the cortical motor fiber in
the ventral pons prevented voluntary mouth
opening.
ABNORMAL YAWNING. Abnormal repetitive
yawning may be the consequence of opiate
withdrawal; intoxication with CNS depressants;
drug side effects (tricyclic antidepressants,
reserpine); lesions to the CNS such as
postencephalific conditions, CNS tumors. apallic
syndrome, cerebral malformations, transtentorial
herniation. Yawning is associated with
diminished brain oxidative metabol ism. Such is
the case of anemia or cerebral anemia (occlusion
of the carotid arteries), hypoglycemie states.
In these situations, yawning through its action
on the cerebral blood flow, is a protective
homeostatic reflex to increase brain oxygen
levels in situations of decreased brain
oxidative metabolism.
WHY WE YAWN is not entirely clear why
people yawn. It could net purposelessly have
survived the evolutionary process with reason.
Whereas actual yawning is not elicited
voluntarily, it is an ideomotor action
easilyelicited by suggestion, by thoughtful
preoccupation with yawning and by unconscious
imitation. It is layman's knowledge that yawning
is acontagious behavior. Bell et al were able te
induce yawning in undergraduate students by
instructing them te think about it, showing
yawning is perhaps a stereotyped imitative
behavior. It is also commun knowledge that
yawning can emerge before psychologically or
physically strenuous situations. No explanation
for this is found in current medical literature.
On the other hand, psychotic patients have a
tendency to yawn less. This bas perhaps some
bearing on the finding of increased yawning
after apomorphine in animals. Yawning may have
acquired a paralinguistic meaning with
evolution. As a nonverbal passive behavior, it
may have a role in human communication
expressing a refusal te participate in a
dialogue. Alternatively, the purpose of yawning
has te do with the sense of smell as a larger
bolus of air is placed in contact with the
maximafly exposed nasopharynx. Yawning possibly
is a protective response with a more logical
reason for its existence than te reverse hypoxia
and alveolar collapse during periods of
hypoventilation.
BIOCHEMISTRY OF YAWNING. Various
agents can induce yawning in animals.
Dopaminergic and cholinergic agonists, ACTH-MSH,
oxytocin produce yawning in rats. The
stretching-yawning syndrome in animals (SYS)
which includes penile erection is befleved te
involve doparninergic inhibitory circuits and
cholinergic activation. The intraventricular
administration of ACTH and alpha-MSH stimulating
hormones induce SYS in different animal species.
This is a specific and centrally mediated effect
of the ACTH-MSH peptides and it is not obtained
after peripheral administration. It bas been
suggested that septalhippocampal cholinergic
neurons arc involved in the production of SYS
following administration of these peptides. This
same effect of ACTH is also found interspecies.
Hypothalamic extract from rats will induce this
behavior in recipient rabbits. Another
hypothalamic peptide, oxytocin, was found te be
the single most potent stimulus producing
yawning, stretching and penile erections in
animals when injected directly into die CNS
(intraventricularly). Systemic injection of
apomorphine and other dopaminergic or
cholinergic agonists also produce SYS.
Apomorphine may induce yawning by increasing the
release of oxytocin directly from the
Paraventricularis Nucleus (PVN) of the
hypothalamus. Among pharmacological agents able
te prevent oxytocin, ACTH-MSH and
apomorphine-induced yawning and penile erection,
morphine is certainly one of the most effective.
Dopaminergic, oxytocinergic, cholinergic
antagonists prevent SYS. Lesions to the PVN
prevent apomorphine but not ACTH-induced yawning
suggesting ACI'H induœs yawning through
different pathways from those of doparnine
agonists. Hypothalamic oxytocin probably
functions as the final common pathway
neuropeptide released in response te different
chemical stimuli. Centrally injected ACTH-MSH
seems to induce yawning through the release of a
second and yet undetermined messenger. ACTH-MSH
docs net act on the PVN of the hypothalamus nor
is it mediated by the release of oxytocin like
apomorphine.
CONCLUSIONS
No single, peptide, neurotransmitter,
neuronal systern alone can be assigned to
yawning. Yawning involves dopaminergic,
cholinergic neuronal systems, ACTH-MSH,
oxytocinergic peptides and its anatomical center
is most likely located in the lower brain
stem.
Yawning is a multifarious reflex possibly
subserving the purposes of: a) protectively
enhancing arousal and attention; b) reversing
mild brain hypoxia or hypoxemia; c) enhancing
the sense of smell; d) non-verbal
communication.
