Yawning can be regarded as a prototype of
stereotypical behaviors recycled through the
evolution for different purposes along with
increasing complexity of the central nervous
system, correlated with the richness of social
interactions. In this chapter, past and current
hypotheses concerning the generation and
usefulness of yawning are discussed.
INTRODUCTION
Cognition, emotion, behavior and memory are
all brain functions. However, this was not
accepted to be true until the end of the 18th
century. While eating, drinking, urination,
sight and walking seem easy to understand, the
purpose of other functions that originate in the
brain, such as sleep, dreaming, hiccups and
laughter remains mysterious. Yawning belongs to
this second group of functions, which appear
more difficult to understand than the other
functions of the brain. This might explain the
vast array of beliefs and hypotheses, as varied
as they are strange in certain cases, associated
with what for human being is a daily behavior.
As we shall see, several diverse hypotheses
exist in 2011, but for the moment none can be
scientifically verified.
What is a yawn?
Yawning is a stereotyped and often
repetitive motor act characterised by gaping of
the mouth accompanied by a long inspiration of
breath, a brief acme, and then a short
expiration of breath. Stretching and yawning
simultaneously is known as pandiculation, which
is not merely a simple opening of the mouth but
a complex, coordinated movement bringing
together a flexion followed by an extension of
the neck and a wide dilatation of the
pharyngolarynx with strong stretching of the
diaphragm and anti-gravity muscles. Yawning is
involuntary and only humans seem capable of
altering its occurrence for cultural or social
reasons. It is highly stereotypical because no
environmental input changes the sequence of
movements. Yawning is observed in cold-blooded
and warm-blooded vertebrates, from reptiles with
rudimentary "archaic" brains to human primates,
in water, air and land environments. Ethologists
agree that almost all vertebrates yawn. Yawning
is morphologically similar in reptiles, birds,
mammals and fish (Deputte, 1994; Fraser, 1989;
Walusinski, 2004). These behaviors may be
ancestral vestiges maintained throughout
evolution with little variation
(phylogenetically old origins). Correlatively,
yawning can be viewed as early as 12 weeks
during fetal development (ontogenetically
primitive) (Walusinski, 2010).
Different types of yawns
The triune brain hypothesis is a model of
the evolution of vertebrate forebrain and
behavior proposed by the American
neuroscientist, Paul D. MacLean (1913-2007).
MacLean originally formulated his model in the
1960s and propounded it at length in his 1990
book, The Triune Brain in Evolution. The triune
brain consists of the reptilian complex (archaic
brain), the paleomammalian complex (limbic
system), and the neomammalian complex
(neocortex), viewed as structures sequentially
added to the forebrain in the course of
evolution (Mc Lean, 1990). Although the model
never won wide acceptance among comparative
neurobiologists, it helps to explain the
different types of yawns:
1) universal yawning, is seen in nearly all
vertebrates, is associated with sleep and
arousal or with hunger and satiety, and appears
to be generated by the reptilian brain (Giganti,
2010).
2) what ethologists describe as emotional
yawning, is only seen in some mammals (but data
still being collected), and is generated by the
paleomammalian brain. This is the yawn, which
helps to pacify after stress. Dogs in veterinary
situations or caged chimpanzees yawn more
frequently than during non-stressful times.
Ethologists call this type of behavior a
displacement activity. In humans, athletes yawn
repeatedly before competitions, as do
parachutists before jumping and actors before
making their entrance. In these cases, yawning
has a calming, anti-stress effect. This might
explain why yoga teachers use yawning to relax
their students. A related type of yawning is
that associated with sexuality in dominant male
macaques, who yawn repeatedly before mating, as
if to make their status within the group known.
This sort of yawn disappears following
castration and reappears if testosterone is
injected (Aureli, 1997; Beckmann, 1981; Deputte,
1994; Maestripieri, 1992; Zucker, 1998) .
3) "contagious yawning", is observed only in
great apes and humans who display a theory of
mind. This ability to respond to yawning in
others is absent in autistic people. Functional
imaging shows activation of the same brain
structures as those used to decode empathy. As a
neocortical activity (frontal and parietal
lobes, insula and, amygdala), communicative
yawning is a sign of involuntary empathy (Helt,
2010; Senju, 2010).
One can conclude that through evolution, a
behavior can be recycled for different purposes
according to the increasing complexity of the
central nervous system, correlated with the
richness of social interactions.
Neuropharmacology of
yawning
Most of the significant advances towards our
understanding of the neuropharmacological
regulation of yawning have been made during the
past 50 years. We now know that a variety of
neurotransmitters and neurohormones are involved
in the induction and regulation of yawning,
including acetylcholine, dopamine, glutamate,
serotonin, oxytocin, gamma-aminobutyric acid
(GABA), opioids, adrenergics, nitric oxide, as
well as the pro-opiomelanocortic-derived
peptides, e.g., adrenocorticotropic and
alpha-melanocyte stimulating hormones (ACTH and
alpha-MSH, respectively). Most yawning is
mediated by at least 3 distinct pathways, all of
which appear to converge on cholinergic neurons
within the hippocampus, despite the diverse set
of neurotransmitters involved. In addition, the
importance of the hypothalamus (parvocellular
nucleus, PVN) in regulating yawning has been
demonstrated, as many of these neurotransmitters
appear to affect yawning through their
interactions with oxytocinergic neurons within
the PVN. For instance, activation of these
oxytocinergic neurons by dopamine, glutamate,
nitric oxide and oxytocin is known to induce
yawning, whereas inhibition of these neurons by
µ-opioids and GABA has been shown to reduce
the frequency of yawning. It is important to
note that although the effects of ACTH and
alpha-MSH are also mediated by the hypothalamus,
the induction of yawning by these peptides does
not involve oxytocinergic neurons. Similarly,
the induction of yawning by serotonin is known
to occur independent of oxytocinergic neurons
within the PVN; however, the brain regions
responsible for serotonergic yawning are
currently unknown.
Despite the great advances made towards our
understanding of the neuropharmacological
regulation of yawning, further studies are
needed to fully elucidate how these
neurotransmitter systems interact with each
other, as well as the specific receptor subtypes
and brain regions involved in the induction and
inhibition of yawning. Such an understanding
would not only advance the use of yawning as a
tool for the pharmacological characterization of
receptor subtype-selective agonists,
partial-agonists and antagonists, but also
further our knowledge of how a variety of
environmental and pharmacological manipulations
(i.e. dietary conditions or chronic drug
treatments) affect the receptor systems involved
in mediating yawning. In addition, a more
complete understanding of the
neuropharmacological regulation of yawning could
also provide insight into the specific roles of
different neurotransmitter systems and/or
receptor subtypes in the occurrence of yawning,
under a variety of physiological conditions and
disease states in which changes in the frequency
of yawning are known to occur (Collins,
2010).
OLD THEORIES NOW CONSIDERED
FALSE
Life, in all its aspects, has always given
rise to thought and questioning. Explanations of
physiological phenomena have always provided us
with reassurance. As noted by Henry Louis
Mencken (1880-1956): "Explanations exist and
have always existed, because there is always a
simple solution to each human problem, a clear
solution that is plausible and false" (Mencken,
1934). . The history of knowledge on yawning is
a perfect example of this precept. The causes
and consequences of this intriguing phenomenon
have defied the human mind for centuries. The
most ancient theory on yawning was applied in De
flatibus liber, "a treatise on wind" written by
Hippocrates in 400 BC. He observed: "Yawning
precedes a fever, because the large quantity of
air that has accumulated ascends all at once,
lifting with the action of a lever and opening
the mouth; in this manner the air can exit with
ease. Like the large quantities of steam that
escape from cauldrons when water boils, the
accumulated air in the body is violently
expelled through the mouth when the body
temperature rises". This idea persisted until
the 17th century (de Mercy, 1831).
Santori Santorio (1561-1636) or Sanctorius
of Padua was a physician in Venice and student
and friend of Galileo. He may be considered as
one of the founders of experimental physiology.
He tried to quantify physiological and
pathological phenomena with measuring devices
such as the scale, the thermometer and the
metronome. With a scale of his own invention, he
measured and compared weight gain and loss in
humans, particularly by perspiration. He built
an entire medical theory based on the weight
differences related to nutrition, releases via
the emunctories and perspiration, calling it
static medicine. He mentioned yawning in his
aphorisms: "Yawning and limb extension after
sleep show that the body perspires abundantly,
similar to the rooster that flaps its wings
before it starts to sing. The urge to yawn and
stretch the limbs upon waking stems from the
abundance of perspirable matter, creating an
inclination to perspire. Through yawning and
limb extension, we perspire more in one half
hour than we would during other times in three
hours" (Santori, 1634).
Johannes de Gorter (1689-1762), a prolific
Dutch author in all areas of medicine in the
early 18th century, holds a key place in the
history of knowledge on yawning. In his book, De
Perspiratione insensibili in 1755, he attributed
yawning "to a need for faster blood circulation
and to cerebral anemia" (de Gorter, 1725). This
marks the birth of an idea that would persist
for two centuries, repeated by almost all
authors: yawning improves brain oxygenation.
This hypothesis seems to predict that yawning is
triggered when blood or brain oxygenation is
insufficient, i.e. when oxygen (O2) levels drop
and carbon dioxide (CO2) concentration rises.
Provine et al. demonstrated, in 1987, that
healthy subjects who are exposed to gas mixtures
with high levels of CO2 or to physical exercise,
do not yawn more frequently. Similarly, high
levels of O2 had no influence on the yawning
rate (Provine, 1987). Although hypoxia is
frequent in patients with heart or lung disease,
no increased yawning is usually observed in
these patients. Yawning in the human fetus and
in fish also rules out this hypothesis. During
periods of low blood oxygenation, yawning does
not increase and thus cannot improve brain
oxygenation .
HYPOTHESES THAT HAVE NOT BEEN
EXPERIMENTALLY TESTED
A number of other hypotheses have arisen
over time. Cahill (1978) argued that yawning
prevents lung atelectasis; Pellatt et al. (1981)
suggested that the thyroid gland may be
compressed during yawning with the resultant
liberation of thyroid hormones; Forrester (1988)
presumed that yawning renews surfactant film in
the lungs; McKenzie (1994) thought that yawning
may enhance the evacuation of the tonsilar
fossae.
Because yawning opens the Eustachian tubes
and therefore ventilates the tympanal cavities,
Laskiewicz, in 1953, postulated that yawning may
be a "defence reflex" to equalise air pressures
in the ear, triggered by altitude changes or
other conditions leading to air trapping in the
middle ear.
Matikainen et al. (20008) argue that yawning
causes movements and compressions that may
affect the carotid body that is situated
strategically at the bifurcation of the common
carotid artery. Thus, yawning may stimulate the
carotid body, by compression. The carotid body
is a chemosensory organ that monitors blood
chemicals and initiates compensatory reflex
adjustments to maintain homeostasis. The
'afferent' sensory discharge induced by changes
in blood chemicals, e.g. low PO2 (hypoxia), is
relayed by carotid sinus nerve fibers. A
parallel autonomic (parasympathetic) 'efferent'
pathway that is the source of carotid body
inhibition is less known. These autonomic
neurons are embedded in 'paraganglia' within the
glossopharyngeal and carotid sinus nerves. While
the phylogeny of the carotid arteries is well
established, the phylogeny of the carotid body
is not. There has been a reduction in the
distribution of peripheral respiratory O2
chemoreceptors from multiple, dispersed sites in
fish and amphibia to a single dominant receptor
site in birds and mammals. In the process, the
cells in the fish gill associated with O2
chemosensing are replaced by the glomus cells of
the mammalian carotid body. Though it is, with
or without carotid bodies, all these vertebrates
yawn widely (Campanucci, 2007; Milsom,
2007).
All these theories do not explain the
association of yawning with arousal and
sleepiness. None of these proposals have been
experimentally tested and there is currently no
evidence for such mechanisms.
Why a fetal yawn?
The advent of ultrasound technology in the
1970s enabled live, unobtrusive observations of
fetal behaviors in humans, vastly increasing our
knowledge of many types of subtle motor activity
(swallowing, respiratory movements, smiling, and
yawning) and thus human fetal development.
Yawning is a phylogenetically old and thus
ontologically precocious behavior. Ultrasound
investigation reveals its onset between 11 and
15 weeks of gestation. The fact that yawning has
survived without evolutionary variations
suggests its importance in terms of
developmental need. The strong muscular
contraction involved in yawning has a
metabolically expensive cost. If we agree with
the terms of the Darwin's evolutionary
propositions, the cost in brain activity must be
outweighed by the advantages gained in terms of
developmental fitness. Thus, a structural
hypothesis suggests an activating role in
neurotrophin synthesis, leading to a cascade of
both new synapse formation or recruitment and
activation throughout the diencephalon,
brainstem and spinal cord. The phenomenon of
activity-dependent development has been clearly
shown to be one mechanism by which early sensory
or motor experience can affect the course of
neural development. Activity-dependent
development may be a ubiquitous process in brain
maturation by which activity in one brain region
can influence development in other regions. It
must be specified that human research on
prenatal programming of behavior is
intrinsically correlational, never
manipulatively experimental, and frequently
based upon homologies with other vertebrates
(Almli, 2001; Petrikovsky, 1999; van Woerden,
2008; Walusinski, 2010).
CURRENT THEORIES UNDER SCIENTIFIC
DISCUSSION
In this section, we will only discuss
universal vertebrate yawning, i.e. the oldest
yawning in phylogenetic terms, which is
generated by the reptilian brain.
The arousal-sleepiness
hypothesis
Each individual, based on his or her own
experience, realizes the link that exists
between fatigue, sleepiness and yawning.
Monotonous circumstances lead to yawning, e.g.
idle waiting, public transportation and long
periods of motorway driving. A correlation
exists between the degree of sleepiness and the
increased yawning frequency. Furthermore,
yawning exhibits a circadian rhythm. Following
sleep, it is more frequent and associated with
stretching (the term pandiculation is used,
referring to yawning together with generalised
stretching of anti-gravity muscles). It is also
more frequent during the drowsiness that
precedes sleep (Giganti, 2010). Herbivores, who
sleep less and have shorter periods of
paradoxical sleep than carnivores or frugivores,
yawn less often. Yawning and pandiculation lead
to maximum opening of the upper respiratory
tract and increase muscle tone in anti-gravity
muscles. All motor activity results in adaptive
feedback. The strong muscular contraction
involved in yawning and pandiculation initiates
sensory feedback, via the somatosensory tract
(posterior funiculus), with projection to the
locus ceruleus (trigeminal-cervical-spinal
sensorimotor loops), the ascending reticular
activating system in the brainstem and the
lateral hypothalamus. According to the most
developed theory at this time, the physiological
function of yawning is to stimulate vigilance,
rather than arousal, and also muscle tone,
through feedback to the above-mentioned
structures, which play a role in arousal,
vigilance and muscle tone. One of the main
arguments for this arousal enhancement derives
from the observation that yawns are followed by
a significant increase in motor activity.
Notwithstanding, sleepy individuals trying to
stay awake change body positions and move their
limbs. These movements have an arousing effect
measurable by EEG, as yawning has (Walusinski,
2006). For Guggisberg et al. "the increased
motor activity observed after yawns is probably
not an indicator of an arousing affect of
yawning, but an effective countermeasure against
the underlying drowsiness". Guggisberg et al.
have analyzed spectral EEG changes after yawns
in humans and the results were negative. Yawning
activates the autonomic system but for
Guggisberg et al., this is unspecific and
related to the associated movements and
respiration. These researchers noticed no
specific increase in skin conductance
(indicating increased arousal level) after
yawning (Guggisberg, 2007). Note that the
hypothesis explored by Guggisberg was that
yawning induces arousal, whereas the initial
theory was to interpret yawning as a means of
stimulating vigilance and not specifically
arousal.
Role of yawning and pandiculation in
interoception and the body schema
Given the demonstration that yawning does
not impact arousal, the theory that vigilance
rather than arousal is stimulated can be
reformulated. In the Aristotelian tradition,
school children learn that we have five senses.
But we receive information from a sixth sense,
interoception, which includes proprioception,
i.e. the ability to perceive sensory stimuli
inside our bodies. The term interoception,
related to somaesthesia, was proposed by
Sherrington, as was the term proprioception
(Sherrington, 1906). Arousal is essential to
consciousness, which requires the ability to
integrate sensory information about the outside
world as well as our sensations concerning our
internal physical state, modulated by emotion
and memory.
Afferent sensations from the musculoskeletal
system converge, via the spinothalamic and
spinoreticular tracts, on the thalamus and raphe
nuclei and from there, on the thalamocortical
tract to the postcentral gyrus in the parietal
lobe. The thalamus and the paraventricular
nucleus in the hypothalamus are part of a
circuit that sends and receives signals from the
locus ceruleus and the mammillary bodies; all of
these structures are involved in autonomic
reflexes. The cranial, trigeminal (V), facial
(VII) and vagus (X) nerves and the motor and/or
sensory cervical nerves C1-C4 also convey
somaesthetic information that converges on the
nucleus of the solitary tract (NTS). The NTS is
an interface for peripheral information needed
to stimulate the ascending reticular activating
system in the brain stem, particularly the locus
ceruleus, which activates arousal systems
(adrenergic system at the pons, dopaminergic
system at the peduncles, histaminergic system at
the hypothalamus and cholinergic system at the
nucleus basalis of Meynert). The neurons of the
NTS project to the parabrachial nucleus, which
in turn projects to various brain stem,
diencephalic and thalamic sites. These
structures also project to the visceral sensory
area of the insula, amygdala and lateral frontal
cortex, especially the right lateral frontal
cortex. These circuits enable a subcortical
homeostatic activity that is unconscious and
automatic to result in a conscious
representation. Autonomic, somatic and limbic
integration make it possible to extract a bodily
perception, which may in turn lead to a
sensation of pleasure (Cameron, 2002; Craig,
2003; Critchley, 2004). Thus, muscle tone
variations in peripheral anti-gravity muscles,
transmitted by these pathways, may trigger
yawning and pandiculation which, through the
powerful muscular contractions that accompany
them, may activate vigilance systems.
Our perception of musculoskeletal activity
therefore brings a feeling of well-being and a
more acute bodily reflectivity of the self, for
example during arousal, as proposed by
James-Lange's theories of emotion or by
Damasio's somatic marker hypothesis of
consciousness (James, 1884; Lange, 1885;
Damasio, 1999).
Yawning: an auto-regulatory role in
the locomotor system
For Bertolucci, "pandiculation seems to be
elicited by a complex array or sequence of
stimuli, which might include both exteroceptive
signals (e.g. light-darkness) and interoceptive
ones (e.g. circadian endocrine cycles and
somatic interoception). Yawning is a series of
coordinated actions that unfold sequentially,
building up soft tissue contractile tension to a
peak, at which point the joints of the limbs and
trunk are maximally extended or, alternatively,
the trunk is arched in flexion. After the peak,
the soft tissue tension level plummets, yielding
a sense of pleasure and well-being. The actions
can be regional or involve the whole body, and
are often bilaterally symmetrical". The
musculoskeletal system is constantly being
reshaped by the mechanical constraints to which
it is exposed. For example, prolonged
immobilisation leads to muscle loss and skeletal
demineralisation.
Bertolucci argues that "pandiculation with
its specific and vigorous muscle activity, might
be a means to compensate for the mechanical
signals delivered by rest periods and
sub-optimal movements". Yawning might be
considered a feedback mechanism resulting from
stiffness, and possibly be triggered by extended
periods of immobility in asymmetrical positions.
If the body tends to stiffen, pandiculation "can
serve to restore the limb (and related
musculature) to an original (homeostatic)
state". [...] "The patterns of
pandiculation are automatic. Through intense and
involuntary deep muscle co-contractions, the
soft tissues actively elongate themselves
against the bony structures as the joints are
stiffened. Each movement within the pattern
emerges in sequence, apparently from the
recruitment of a mosaic of reflexes, the
sequence of which can neither be anticipated nor
purposely performed. Just as a spontaneous yawn
feels quite different from a deliberate
imitation of one, spontaneous pandiculation
feels quite different from a voluntary
pandiculation-like stretch. Because the
voluntary and emotional motor systems have
discrete neural pathways, pandiculation's
distinctive internal sensations might be
attributable to the motor unit recruitment
sequences dedicated to automatic movement
patterns". [...] "The importance of
stretching to the maintenance of musculoskeletal
health is well-known. In humans, each of the
myriad of physical fitness regimens that include
stretching has its own rationale; and although
all muscle groups should be stretched, different
regimens address particular problems and are
intended to compensate for various patterns of
muscle shortness or consequent joint mobility
restriction. But how do animals in the wild
maintain musculoskeletal health? They perform no
voluntary stretching and still maintain their
motor capabilities". [...] "The
mechanical balance between hard and soft tissues
dictates stress distribution, which plays a key
role in cell shape and metabolism. In
pandiculation, the intense mechanical stimuli
produced by forceful co-contraction of
antagonist muscle groups might serve as
appropriate organizing signals to the cells and
tissues by re-optimizing the mechanical
conditions of their environment".
Pandiculation "might be a biological
compensation for periods of immobility and/or
vicious body positions, restoring the animal's
mobility by breaking up abnormal muscle
metabolism cross-links formed by inactivity or
suboptimal activity". [...] "Perhaps the
vigorous co-contractions of pandiculation
systematically reshape the structural linkage
among segments and simultaneously signal the
cells (via mechanotransduction) to synthesize
the cellular muscle components required to
maintain the appropriate environment. If so,
pandiculation might help restore optimal
musculoskeletal arrangements, and thus optimize
motor capabilities" (Bertolucci, 2011).
The thermoregulation
hypothesis
The existence of yawning across almost all
vertebrate species suggests important basic
functions, and the spontaneous and involuntary
nature of a yawn lends support for it having
adaptive significance. Recent research by Andrew
C. Gallup suggests that a biological function of
yawning among homeotherms is central
thermoregulation. Comparative research from
birds, rats and humans suggests, for them, that
yawning reduces brain and body temperature and
is influenced by the range and direction of
ambient temperature change. According to their
model, the increased facial and brain
circulation that follows yawning acts like a
radiator, by eliminating calories from blood in
the brain via the face and head and by
introducing cooler blood from the extremities
and lungs into the brain. In one of the
experiments developed by this team, subjects
wore a refrigerated pack on their foreheads.
Under these conditions, they were less
susceptible to contagious yawning than with no
forehead refrigeration. It should be noted that
cold temperatures have an arousing effect and
can by themselves modify the outcome. Other
experiments on birds in various temperature
conditions showed an increased frequency in the
number of yawns with increasing temperature.
However, no other parameters that could
interfere with this finding were taken into
consideration, which significantly limits the
scientific value of this study (Gallup, 2010,
2011). In a recent experiment, Gallup et al.
explore the relationship between brain
temperature and yawning after they have
implanted thermocoupled probes in the frontal
cortex of rats to measure brain temperature
before, during and after yawning. Temperature
recordings indicate that yawns and stretches
occurred during increases in brain temperature,
with brain temperatures being restored to
baseline following the execution of each of
these behaviors (ShoupKnox, 2010). They
conclude: "Decreases in brain temperature
following a yawn may be the physiological
mechanism mediating cortical arousal".
Furthermore, according to calculations by
Hannu Elo, this hypothesis is physically
impossible. It is impossible to lower body
temperature through yawning, unless the yawns
result in heavy perspiration. Similarly, yawning
cannot lower brain temperature, which would
require water evaporation (lungs and respiratory
tract), loss by conduction, thermal radiation
and a slowdown in metabolism (Elo, 2010, 2011).
In addition, this theory overlooks the existence
of fetal yawning and yawning in poikilotherms
such as reptiles. For these reasons, the
hypothesis of brain cooling through yawning
obviously requires further analysis, with due
consideration given to anatomy and physiology as
well as the actual need, if any, to cool the
brain.
Yawning and the cerebrospinal fluid
system
Domenico Cotugno was the first, in 1764, to
evoke the circulation of cerebrospinal fluid
(CSF) (Cotugno, 1988). The beating of the heart
and the movements associated with breathing
cause pressure variations in the ventricular
system. Each deep inhalation is followed be an
increase in CSF flow rate in the fourth
ventricle (Schroth, 1992).
Jaw kinematics, together with inhalation,
has been shown to alter intracranial
circulation. Lepp (1982) describes jaw
kinematics as follows. Jaw movements activate
the pterygoid musculovenous pump, located in the
upper part of the anterior parapharyngeal space,
known as the prestyloid parapharyngeal space. As
a result, this pump, also known as the paratubal
pump, can impact the mechanism of venous blood
flow out of the endocranium, mainly via the
plexus venosus foraminis ovalis. The pterygoid
cistern, a component of this pump, corresponds
to the cavernous part of the pterygoid plexus.
It is an extracranial extension of the cavernous
sinus and passes through the foramen ovale. It
plays an important role as an intermediary
station of acceleration for return blood flow
from the brain (Bouyssou, 1985 ; Patra, 1988).
Lepp notes that it would be reasonable to
consider jaw kinematics together with the
lateral pterygoid muscle as a venous trigger,
given that they act as the starter for the
alternating musculovenous pumping action that
takes place in the cavernous part of the
pterygoid plexus. This pumping action is
particularly efficient during isolated yawning,
especially when the mouth reaches its maximum
opening. However, Lepp emphasizes that yawning
itself is often merely the initiation of a
musculovenous motor chain reaction, which
extends to the limbs and the entire skeletal
musculature as tonic waves propagated in the
rostrocaudal direction to the ends of the
fingers and toes (Lepp, 1982).
It would thus appear that the large
inhalation and maximum opening of the mouth
accelerate the circulation of CSF. Already in
1912, Legendre and Piéron demonstrated
the presence of a hypnogenic factor in the CSF,
which accumulates during the waking state
(Legendre, 1912). Research into the hormonal,
non-neuronal factors that induce sleep, which
has been conducted for nearly 100 years, has
identified over 50 molecules. Of current
interest is the prostaglandin PGD2, a hormone
that acts locally and is produced by the
meninges. When it binds to a specific receptor,
transduction occurs from the leptomeninges to
brain parenchyma through the activation of
adenosine production, which induces sleep in the
ventrolateral preoptic (VLPO) nucleus of the
anterior hypothalamus (Huang, 2007, 2011).
Yawning and pandiculation may accelerate
clearance of PGD2, thus reducing sleepiness.
They may also act on other neuromediators that
are currently unknown.
CONCLUSION
We close this survey of the different
functional theories on yawning, none of which
have been scientifically demonstrated, by
proposing that yawning appears to be a
homeostatic process involving circadian
variations in vigilance and emotion. Yawning
externalizes a parasympathetic stimulation
during the balancing of adrenergic and
cholinergic homeostasis of the autonomic
nervous. Thus, yawning seems closer to a
behavioral stereotypy than to a reflex. This is
indeed a curious behavioral display and is a
beautiful example of an involuntary expression
that is pleasurable and that we, as humans, use
voluntarily to deliberately communicate
boredom.
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