The
mystery behind "yawning": a physiological
insight
Dipak Kumar Dhar
Ritik Arora
Department of Physiology,
Himalayan Institute of Medical Sciences, Swami
Rama Himalayan University
Jolly Grant, Dehradun
248140, Uttarakhand
Yawning is a very ubiquitous yet very poorly
understood phenomenon. Even though with
advancements in science, the scientific
community has been able to decode the mechanisms
and mysteries behind most of the physiological
functions of the body, but we still do not have
clear answers to this common activity that all
of us experience numerous times on a daily
basis. It is the enigma surrounding yawning that
makes it all more intriguing. A lot of
hypotheses and theories have been proposed since
the times of Hippocrates. With more modern
neuroimaging methods and bioassays available
now, more meticulous inquiry is being
increasingly made to elucidate a rational and
scientifically sound physiological basis of
yawning. A comprehensive and exhaustive study of
articles and research work available on the
internet on the subject was made through various
search engines such as Google Scholar, PubMed,
etc. This article attempts to provide in a
nutshell the available information and knowledge
on the subject and discuss its plausibility and
the future direction of research in this
field.
Le bâillement est un
phénomène omniprésent mais
mal compris. La communauté scientifique a
été en mesure de décoder
certains de ses mécanismes mais les
mystères derrière la plupart ses
fonctions physiologiques n'ont toujours pas de
réponses claires à cette
activité commune que nous vivons tous de
nombreuses fois sur un base quotidienne. C'est
cette énigme qui entoure le
bâillement qui le rend encore plus
intriguant.
De nombreuses hypothèses et
théories ont été
proposées depuis l'époque
d'Hippocrate. Avec des méthodes de
neuroimagerie et des bioessais plus modernes
disponibles maintenant, des recherches plus
approfondies, trop peu nombreuses, sont
menées pour élucider une base
physiologique rationnelle et scientifiquement
solide du bâillement. Une étude
complète et exhaustive des articles et
travaux de recherche disponibles sur internet
sur le sujet a été
réalisée via différents
moteurs de recherche tels que Google Scholar,
PubMed, etc. Cet article tente de fournir une
synthèse des informations et
connaissances disponibles sur le sujet et d'en
discuter sa plausibilité et l'orientation
future de la recherche dans ce domaine.Le
bâillement est un phénomène
omniprésent mais mal compris. La
communauté scientifique a
été en mesure de décoder
certains de ses mécanismes mais les
mystères derrière la plupart ses
fonctions physiologiques n'ont toujours pas de
réponses claires à cette
activité commune que nous vivons tous de
nombreuses fois sur un base quotidienne. C'est
cette énigme qui entoure le
bâillement qui le rend encore plus
intriguant.
Introduction
Yawning is a ubiquitous phenomenon in our
daily lives. It is such a common occurrence that
sometimes we are not even aware of it. Inspite
of this till date, "yawning" still remains
shrouded in a veil of mystery with no clear
understanding of as to why or what are the
mechanisms behind this activity. Provine, who is
considered as the pioneer of yawning research,
remarked in the late 1980s that "yawning may
have the dubious distinction of being the least
understood and common human
behavior."[1] Yawning is a behavior that
is observed across an evolutionarily diverse
array of animals from fishes and birds to
mammals and from the fetal to the old stages of
life. In human beings, yawning has been observed
as early as 12 weeks of fetal life.[2]
It is an phylogenetically old yet ontogenically
new and stereotyped motor behavior that has not
undergone much changes over the course of
evolution. And any trait that has survived
evolution is bound to have some significance for
survival. It is also important to learn about
the different mechanisms behind yawning because
excessive yawning has been associated with
certain conditions like narcolepsy, uremia, side
effects of medications that are used to treat
depression or anxiety such as selective
serotonin reuptake inhibitors or even various
forms of encephalopathy. In this review, we will
try to explore the various mechanisms behind
this seemingly ubiquitous phenomenon. The first
documented account of yawning dates back to 400
BC where Hippocrates wrote in "de flatibus
liber" (a treatise on wind) that "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."[3] Although as we
shall see subsequently in this article in the
absence of any teleological or scientific
evidence, this notion was later discredited by
the researchers in the late twentieth century,
but the idea prevailed for a long time. A
unanimously acceptable mechanism or teleological
explanation to the phenomenon of yawning remains
to be established, but various theories have
been proposed by different groups of researchers
over the last four decades. The present article
tries to provide a narrative review of the
existing knowledge we have on this subject.
Functional Anatomy of Yawning
Yawning is a stereotyped, reflexive motor
activity which consists of a deep respiratory
effort associated with extension of the neck and
wide expansion of the jaw and subsequent
contraction of the tongue. This may be
associated with raising of the arms and muscular
clenching of the extremities.[4] The
respiratory act comprises three distinct phases:
(1) prolonged and deep open-mouth inhalation,
(2) a brief acme, and (3) followed by a shorter
exhalation.[5] It is also often
associated with lacrimation, either due to
pressure on the lacrimal glands or of nervous
stimulation or both.[6] It is a complex
yet very highly coordinated motor activity
bringing together a flexion followed by an
extension of the neck, a wide dilatation of the
laryngopharynx with strong stretching of the
diaphragm and antigravity muscles. And it is
highly stereotypical because no environmental
input changes the sequence of movements.
Therefore, it often appears to be a
semi-involuntary act, which once initiated
cannot be suppressed, but its manifestations can
be modified.[7] The stereotypical nature
of the yawn is consistent with the physiological
property of reflexes being stereotypical. One of
the indispensable concepts in neurophysiology is
the notion of "moto-programs" which are
sequences or algorithms fundamental to genesis
of any motor activity. These have been
attributed to certain "central pattern
generators" in the central nervous system (CNS).
It is now known that humans have certain
built-in motor programs, which means for that
particular activity, the sequence is fixed from
beginning to end once it is started.[8]
The nature and as well as the duration of a yawn
is almost consistent with a mean of just under 6
seconds.[1] [9
Theories of Yawning
Various theories have been put forward
behind yawning. Some try to answer the purpose
while others attempt to explain the mechanisms
behind it. And both homeostatic roles and
communicative role have been suggested. They
range from respiratory, arousal, and
thermoregulatory to its role as a component of
action repertoire of advanced empathic and
social skills.[10]
Respiration and Yawning
Because the act of yawn itself consists of a
prominent respiratory pattern, the earliest
reason proposed behind it was hypoxia. It has
been held commonly that yawning is triggered
when blood or brain oxygenation is insufficient,
either due to hypoxia or due to hypercapnia. In
fact as early as 1755, a noted author on
medicine in the eighteenth century, Johan de
Gorter, described in one of his books De
Perspirationeinsensibili that yawning acts as a
mechanism to accelerate blood flow and improve
oxygenation of the brain in response to cerebral
hypoxia.[11]
Yawning was thought to remove "bad air" from
the lungs and increase circulation in the
brain.[12] It was more of a teleological
argument and prevailed for almost two centuries.
However, now it has been refuted by majority of
the scientific communities. Blood levels of O2
and CO2 show little correlation with
yawning.[13] It was also observed in a
study in the late 1980s that the yawning
frequency was not affected by air mixtures
containing either more than normal CO2 or even
pure O2. However, more recent work in animal
models lend some support in this hypothesis.
Microinjections of L-glutamate, cyanide, and a
nitric oxide-releasing compound (NOC12) into the
medial parvocellular subdivision of
paraventricular nucleus of the hypothalamus
(PVN) in anesthetized, but spontaneously
breathing rats produced a stereotypical yawning
response. The authors suggested that the neurons
in this area of the hypothalamus could have an
oxygen-sensing mechanism, and diffusible NO
could be a paracrine agent involved in the
genesis of yawning response.[14] Yawning
is assumed to subserve important respiratory
functions. Hyperinflation of the lungs as in
yawning is an important stimulus for surfactant
synthesis in the lungs.[15] This is
especially important for infants and might
explain its presence even in fetal life. Yawning
also enhances the dynamic lung compliance of
lungs, that is, greater change in volume is
possible per unit change of transpulmonary
pressure. Additionally, it also improves the
venous return to the heart.
Arousal and Yawning
The conditions during which yawning has been
commonly observed are immediately before sleep,
awakening from fully complete sleep, weariness,
lack of stimulation, boredom, or any monotonous
task. Medical conditions, such as multiple
brainstem ischemic strokes, frontal lobe tumors,
etc., could also cause excessive yawning.
Increased frequency of yawning has also been
observed in people intoxicated by Psilocybin
mushrooms.[6] All these scenarios
described above have one common feature: lowered
state of critical consciousness which implies a
reduced state of normal, active awareness of
being related to environment. It was suggested
in the late 1980s that yawning actually is a
complex arousal defense reflex from its close
temporal occurrence with activities causing
boredom or loss of interest, fatigue, and sleep.
The center of this reflex was proposed to be the
reticular formation of the brainstem,[9]
which we now know is the seat of the
consciousness and also houses the various neural
circuits implicated in sleep-wake
states.[8] [16] Even in infants
and children (aged 6&endash;34 months), the most
common context of yawns as recorded by their
mothers was on awakening after morning or
afternoon naps, suggesting its close temporal
association with sleep and
wakefulness.[17] This proposition was
later supported by observations in studies on
human subjects where physiological variables
associated with aroused state like an increased
heart rate, increased skin conductance and _
waves on electroencephalogram were studied in
relation to yawning. The _-waves on EEG are most
marked when the person is awake but relaxed and
the eyes are closed.[16] [18]
This correlates with the experiential feeling of
comfort or relaxation during a yawn. Studies in
the last decade have yielded that EEG changes
found postyawning were consistent with those
observed intake of caffeine, which is a known
stimulant of CNS.[19] [20] In
2011, a group of researchers showed that heart
rate significantly increased at the peak of a
yawn (p < 0.001), 10 seconds (p = 0.002) and
15 seconds (p < 0.001) after yawning as
compared with the resting values.[21]
Also, the stretching of the muscles around the
jaw and neck during could also compress the
carotid bodies and baroreceptors which are
located in the major blood vessels of the
region. This would trigger a downstream
alteration in the circulation by altering the
resting vasomotor tone on the
arteries.[6] [15] This might
possibly increase cerebral blood flow too,
contributing to enhanced alertness.
The Ear and Yawning
The eustachian tube is a channel that
connects the middle ear cavity with the pharynx.
This plays vital role when there is a change of
air-pressure on either side of the tympanic
membrane as in rapid ascent or descent, as
observed in take-off or landing of aeroplanes,
or diving, for example. The pressure difference
causes the tympanic membrane to bulge outward in
the former and pulled inward in the latter
scenarios, often causing discomfort and pain in
many people.[22] Yawning causes an
opening and closing of the pharyngeal end of the
eustachian tube, thus equilibrating the
pressure. Therefore, the mechanics associated
with yawning can help relieving these
symptoms.
Thermal Homeostasis and Yawning
There is yet another proposed function of
yawning is maintaining of thermal homeostasis,
especially the temperature of the head.
Researchers have proposed that yawning "cools
the brain." Studies in clinical settings
suggested that an increased occurrence of
yawning is observed in pathological states where
there was a sudden increase in the core
temperature of the body as in epilepsy,
migraine, multiple sclerosis, etc. The episodes
of symptoms subsided following
yawning.[23] [24] [25]
The authors have even contemplated considering
pathological yawning as a part of the
symptomatology of these diseases. Further
evidence in this regard was provided by a series
of animal experiments in mice and parakeets
where the cortical brain temperature was more
before and less after yawning.[26]
[27] In an interesting study done on
human volunteers using warm-pack and ice-pack
applied to the forehead, the researchers
observed that there was an increase in yawning
when warm packs were applied.[28] The
premise of this heat-loss theory can be
understood by considering the various concepts
of heat dissipation from the body. Heat can be
lost when there is an increased blood flow which
takes away the heat from the core to the surface
or when there is an enhanced loss of air from
the body as deep breathing.[16] Although
brain is one of the most metabolically active
organs of the body; however, it still remains to
be proved conclusively that higher metabolic
rates can increase the internal temperature of
the region. This is one of the questions that
the authors could not explain. The contraction
and relaxation of a variety of the muscles of
the face and neck during a yawn, increases the
facial blood flow which aids in dissipation of
heat. Concomitant stretching of the lower
extremities often observed while yawning
contracts muscles like the soleus, the
"peripheral heart" which in turn increases the
venous return to the right chambers of the
heart, thus increasing the cardiac output and
consequently increasing cerebral blood
flow.[29] Heat is also lost as yawning
by itself is an act of deep and prolonged
respiration. Interestingly much before we had
these modern methods of quantifying metabolism
or blood flow, a similar theory was also
proposed by an Italian physician Santorio
Santori in as early as 1634. He proposed an
analogy between yawning and limb extension after
sleep with that of a rooster that flapping its
wings before it starts to sing. Both of these
activities, he had suggested increased
perspiration.[30]
Emotional Yawning
A specific type of yawning has also been
observed in relation to certain emotional states
and described by ethologists as "emotional
yawns." Although not much comprehensive in its
explaining in humans, this theory states that
yawn is generated by the paleomammalian brain
and helps to pacify after stress. Observations
in its favor have been drawn mainly from
observations in dogs and caged chimpanzees,
yawning more during stressful times. A type of
yawning has also been associated with sexuality
in dominant male macaques, who yawn repeatedly
before mating, as if to assert their dominance
in the group. And interestingly, this type of
yawning disappears following castration and
reappears if testosterone is
injected.[31]
Is There a Biochemical Basis?
Evidence of a possible biochemical basis was
put forward primarily from animal experiments,
primarily in the last decades of the previous
century. Dopaminergic and Cholinergic agonists,
ACTH-MSH and oxytocin, were observed to produce
yawning in rats. Intraventricular injection of
ACTH, _-MSH, and oxytocin was found to induce
yawning and stretching in these animals.
Dopaminergic and cholinergic antagonists were
found to inhibit the same, thereby suggesting a
possible role of these two compounds
too.[7] [32] [33] One of
the prominent biochemical theories of yawning is
Thompson's Cortisol hypothesis which proposes
that cortisol levels are elevated during yawning
episodes. Evidence in favor of this hypothesis
was provided when researchers found higher
levels of stress hormones particularly cortisol,
was recorded in the saliva of human subjects
following yawning.[6] With regard to
neurochemistry of yawning, the most
comprehensive model is centered around PVN of
the hypothalamus. It suggests that oxytocinergic
neurons originating there and projecting to
extra hypothalamic brain areas mediate the
expression of yawning in animals in most
circumstances. Activation of these neurons in
the PVN by dopamine receptor agonists,
excitatory amino acids, and oxytocin results in
yawning and their inhibition by opioids, for
example, endogenous opioids like enkephalins
prevent the behavioral
expression.[34]
Decoding the Contagiousness of a Yawn:
The Mirror Neuron System
The social contagiousness of a yawn is one
of the most common experiences of our daily
lives. Whether we see other people actually
yawning or videos of people yawning or even read
and hear repeatedly about yawning, it seems to
be transmitted to us and we too tend to yawn
very often. In fact, it would not be surprising
if the reader of this article gives out a yawn
or two by the time he or she finishes reading
it. There are two basic ways by which yawning
can be elicited: thoughtful preoccupation and
subconscious or unconscious
imitation.[29] This particular and
rather peculiar property of a yawn is now
considered to be an evolutionarily derived skill
of social empathy.
A study published in 2011 on yawning in 109
healthy adult volunteers of various
nationalities in their natural work environments
concluded that social bond greatly influenced
the bouts of yawning between the yawner and the
observer (in which it was triggered as a
response). It significantly increased from
strangers, acquaintances, close friends to kin
(p < 0.001). The authors concluded that
yawning and social empathy are closely
linked.[35] More studies exploring this
social aspect have provided further evidence.
Yawning episodes were significantly lesser in
schizophrenic patients[36] and in
autistic children as compared with age and
sex-matched controls when similar stimuli like
yawning videos were shown to them.[37]
Both of these scenarios depict patients in whom
social skills and understanding are deficient.
Researchers have also suggested that even in
healthy children, contagious yawning can occur
in children only after 4 to 5 years of age
because until this age, neural mechanisms
implicated in social skills are still under the
process of development.[38] A study done
on chimpanzees yielded some interesting results.
A group of 23 adult chimpanzees were observed
for contagious yawning while viewing the videos
of yawning movements of the mouth of same
species and different species, that is, humans.
They authors observed that yawning responses
were more in the former case. Although, the
small sample size was a major limitation in the
study. Nonetheless, the study points out, at
least qualitatively, that yawning must have a
role in social communication, even in other
mammals.[39]
Neuroimaging studies investigating the
physiological basis of yawning reported that
higher functional magnetic resonance imaging
activations in response to contagious yawning
have been observed in posterior cingulate
area,[40] bilateral superior temporal
sulcus,[41] or ventro-medial prefrontal
cortex.[42]
The neural basis of yawning is now
attributed to a system of neurons in the brain
called as "mirror neurons."[41]
[43] Mirror neurons are one of the most
enigmatic set of neurons that hold the key to
evolution of human civilization. They represent
a distinctive class of neurons that discharge
both when an individual executes a motor act and
when he observes another individual performing
the same or a similar motor act. These neurons
were first discovered in monkey's
brain.[44] The human mirror-neuron
system consists of a network involving the
following areas: supplementary motor area,
primary somatosensory cortex, inferior parietal
cortex, and ventral premotor area. Additionally,
neurons having mirror properties have also been
discovered in Broca's area, Wernicke's area,
Fusiform Gyrus, Angular gyrus, and Primary motor
cortex.[44] [45] These system of
neurons are now known to be the fundamental seat
of human emotions like empathy at the cellular
level.[46] [47] [48]
Thus, this provides the physiological basis of
the social contagiousness of occurrence of
yawning.
Recent Trends: Is There a Link with
Cortical Motor Excitability?
A research team at the University of
Nottingham investigating in the field of
cognitive neuropsychology have rather come up
with interesting results. They conducted a study
on 36 volunteers showing them video clips of
another individual yawning and were told to
either resist yawning or allow themselves to
yawn. They were observed and videoed throughout.
Transcranial magnetic stimulation was
concomitantly used to quantify motor cortical
excitability and physiological inhibition for
each participant. They demonstrated that the
participants who resisted yawning had increased
the urge to yawn and altered how yawns were
expressed (i.e., complete yawns or stifled
yawns). They made two important observations.
First, that during yawning there is an increased
excitability of the cells of primary motor
cortex and/or decreased physiological
inhibition. And even suggested a possible link
with a wide range of clinical conditions where
echophenomena is observed like epilepsy,
dementia, autism, and Tourette syndrome and also
have similar physiological attributes like
increased cortical excitability. And second, the
propensity of contagious yawning is highly
individualized.[49]
Yawning Modifiers
The occurrence of contagious yawning and the
factors which might trigger yawning have already
been discussed above. They could range from
alterations in sleep-arousal system to emotional
factors. However, one of the latest works shows
that the occurrence of a yawn could be modified
experimentally by changing the temperature
around the neck. A recent study published in
2019 in which participants were asked to hold a
warm (46°C), cold (4°C), or room
temperature (22°C) pack firmly to their
neck, just over their carotid arteries, for a
period of 5 minutes prior to watching a
contagious yawning stimulus reported interesting
findings. More than 80% of the participants
reported the urge to yawn with warm packs and
less than half (48.5%) with the cold packs. This
study further supports the thermoregulation
hypothesis associated with yawning. While other
research works as discussed in the previous
section have also proposed that the
physiological tendency of yawning is highly
individualized.[50]
Conclusion
The phenomenon of yawning has fascinated the
human beings for ages and the truth is, the
complete neurobiology behind it is still
unknown.[51] The unique, universal,
ephemeral, and stereotypical qualities of
yawning have invited boundless speculation about
its evolution, function, and significance from
the scientific community. With more and more
evidences and experiments with newer methods
like neuroimaging, older concepts have changed
and newer theories about various aspects have
emerged. However, its full neurophysiological
mapping is yet to be completed.
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