Once
born, each of us will yawn an average 250,000
times before we breathe our last
!
The yawn is a stereotyped and often
repetitive motor act characterized by gaping of
the mouth accompanied by a long inspiration of
breath, a brief acme, and then a short
expiration of breath.
Introduction
Stretching and yawning (known as
pandiculation when they occur together) are
under-researched features of behavior.
Ethologists agree that almost all vertebrates
yawn (Deputte, 1974). Yawning is morphologically
similar in reptiles, birds, mammals and fish.
These behaviors may be ancestral vestiges
maintained throughout evolution with little
variation (phylogenetic old origins). Systematic
and coordinated pandiculations occur in a
similar pattern and form across all animals, and
consistently occur during behaviors associated
with cyclic life rhythms: sleep-arousal, feeding
and reproduction. Pandiculation appears as one
undirected response to an inner stimulation,
underlying the homeostasis of these three
behaviors (Provine, 2005; Walusinski &
Deputte, 2004).
Relatively sedentary species that sleep very
little, such as many herbivores, yawn
infrequently; species that sleep 8 or 12 h and
alternate between active and inactive periods
(e.g., predatory carnivores and primates) yawn
much more frequently following a circadian
rhythm. In humans, daily frequency of yawning
varies between 5 and 15 times per day. The
diurnal distribution of yawning frequency is
illustrated by higher frequency upon waking and
before sleep (Baenninger et al., 1996).
In his 1755 book De perspiratione
insensibili, Johan de Gorter was the first to
describe yawning as accelerating blood flow,
supposedly to improve the oxygenation of the
brain, in response to cerebral anaemia. Well
into the 20th century, there were regular
references to this notion, even though it had
never been demonstrated. The inaccuracy of this
hypothesis was formally shown by Provine, Tate
and Geldmacher in 1987. They had their subjects
inhale air with higher than normal levels of CO2
(3-5% vs. <0.5%). In response, the subjects'
breathing rates increased, but they did not
yawn. Likewise, when the subjects inhaled pure
oxygen, there was no inhibition of spontaneous
yawning at normal rates. Hence yawning is not a
physiological reflex to improve cerebral
oxygenation.
Neurophysiology
A good number of clinical and
pharmacological arguments indicate that yawning
involves the hypothalamus (particularly the
paraventricular nucleus, PVN), the bulbous and
pontic regions of the brainstem, with frontal
region connections in primates and to the
cervical medulla (Argiolas & Melis, 1998).
The PVN is an integration centre between the
central and peripheral autonomic nervous
systems. It is involved in a number of functions
ranging from feeding, metabolic balance, blood
pressure and heart rate, to sexual behavior and
yawning. In particular, a group of oxytocinergic
neurons originating in this nucleus and
projecting to extra-hypothalamic brain areas
(e.g., hippocampus, medulla oblongata and spinal
cord) controls both yawning and penile erection
(Kita et al., 2006).
Activation of these neurons by dopamine and
its agonists, excitatory amino acids
(N-methyl-D-aspartic acid), oxytocin itself, or
by electrical stimulation leads to yawning;
conversely their inhibition by
gamma-amino-butyric acid (GABA) and its agonists
or by opioid peptides and opiate-like drugs
inhibits both yawning and sexual response. The
activation of these neurons is secondary to the
activation of nitric oxide synthase, which
produces nitric oxide. Nitric oxide in turn
causes, by a mechanism that is as yet
unidentified, the release of oxytocin in
extra-hypothalamic brain areas (Sato-Suzuki,
1998). Other compounds modulate yawning by
activating central oxytocinergic neurons: sexual
hormones, serotonin, hypocretin and endogenous
peptides
(adrenocorticotropin-melanocyte-stimulating
hormone).
Oxytocin activates cholinergic
neurotransmission in the hippocampus and the
reticular formation of the brainstem.
Acetylcholine induces yawning via the muscarinic
receptors of effectors from which the
respiratory neurons in the medulla, the motor
nuclei of the Vth,VIIth, IXth, Xth, and XIIth
cranial nerves, the phrenic nerves (C1-C4) and
the motor supply to the intercostal muscles. An
arousal response accompanied by yawning behavior
can be evoked by electrical and chemical
stimulation of the hypothalamic paraventricular
nucleus (PVN) in rats, although the mechanism
responsible for the arousal response accompanied
by yawning evoked by PVN stimulation is still
unknown.
Development in humans
At the beginning of the third month, the
embryo becomes a fetus with the occurrence of
the first oral and pharyngal motor sequences
under the control of the neurological
development of the brainstem which coordinates
the respiratory, cardiac and digestive
regulations. Circuits that generate organized
and repetitive motor patterns, such as those
underlying feeding, locomotion and respiration
belong to the Central Pattern Generators in the
medulla (CPG) which are genetically determined,
subserving innate motor behaviors essential for
survival. As an example, yawning occurs as early
as 12 weeks
after conception and remains relatively
unchanged throughout life (Walusinski, 2005;
Piontelli, 2010). Its survival without
evolutionary variations postulates a particular
importance in terms of developmental needs. The
ability to initiate motor behavior generated
centrally and linked to arousal and respiratory
function is a property of the brainstem
reticular formation, which has been remarkably
conserved during the phylogeny of vertebrates
including agnathans, fishes, amphibians,
reptiles, and birds. Thus, yawning and
stretching have the traits of related
phylogenetic old origins.
Yawning and thermoregulation (the lastest
and debatable hypothesis)
As reviewer, Gallup adds his new theory:
consistent with the role of the hypothalamus and
the PVN, evidence from diverse sources suggests
that yawning may be a thermoregulatory mechanism
(Gallup & Gallup, in press). Multiple
sclerosis, epilepsy, schizophrenia, treatment
for opiate withdrawal, sleep deprivation,
migraine headaches, stress and anxiety, and
central nervous system damage are all related to
thermoregulatory dysfunction and each of these
conditions is associated with atypical yawning.
Excessive yawning appears to be symptomatic of
conditions that increase brain and/or core
temperature, such as central nervous system
damage, sleep deprivation, and specific
serotonin reuptake inhibitors. Drugs that lead
to hypothermia (e.g., opioids) inhibit yawning.
Nasal breathing and forehead cooling, which have
been identified as specific brain cooling
mechanisms, diminish the incidence of yawning
(Gallup & Gallup, 2007).
There is no work indicating that cerebral
activity modifies the internal temperature of
the brain in a variable way according to the
level of attention. Parmeggiani (2007) has
reported changes in brain temperature during the
ultradian sleep cycle in several mammalian
species. The temperature decrease in NREM sleep
appears as a normal effect of thermoregulation
operating at a lower set point temperature than
in wakefulness. In contrast, the increase in
brain temperature related to REM sleep appears
paradoxical from the viewpoint of normal
thermoregulation. The problem of the physiologic
mechanisms underlying this temperature change
remains unresolved. Changes in brain temperature
are in general relevant to both the energy
metabolism of the brain and the function of the
preoptic-hypothalamic thermostat. It is obvious
that brain homeothermy is altered essentially by
quantitative imbalances between metabolic heat
production and heat loss. Heat loss from
systemic heat exchangers, affecting carotid
blood temperature through the systemic venous
return to the heart (systemic brain cooling), is
the most important determinant of brain
temperature in primates. Concerning humans, in
particular, there is no consensus as to whether
a mechanism for selective brain cooling plays a
significant role. The arguments advanced by
Gallup & Gallup by which yawning decrease
body temperature are physically possible only if
yawning effectively increases perspiration. The
thermoregulatory hypothesis is interesting, and
hypotheses are needed but they should be called
hypotheses or theories, not conclusions or
results, as long as convincing evidence is
missing (Elo, 2010).
Although the origin and function of yawning
has been subject to speculation for centuries,
the first complete review of the experimental
evidences for each of these hypotheses can only
now be read (Guggisberg, Mathis et al,
2010).
Contagiousness of yawning
Although yawning often procures a sense of
well-being for the yawner, attempring to mask
this behavior is standard practice. Many
worldwide cultural beliefs and myths portray it
as socially and singly offensive
(Meenakshisundaram, 2008 in press). Hominids
have the unique capacity to be receptive to the
contagiousness of yawning (echokinesis would be
a more accurate term). Yawning appears to
trigger a sort of social coordination function
(arousal synchrony) and reflects the capacity to
unconsciously, automatically be influenced by
the behavior of others, supporting the
hypothesis that contagious yawning shares the
neural networks involved in empathy.
Echokinesis only occurs in situations of
minimal mental stimulation (public transport,
for example); people are not susceptible to this
phenomenon during prolonged intellectual effort.
Using functional magnetic resonance imaging
(fMRI), Schürmann et al. confirmed that
whilst observation of facial gestures in another
person caused activation of mirror neurons in
motor areas of the human brain (left posterior
inferior frontal cortex), there was no such
activation during echokinetic yawning. These
ethological and neurophysiological elements
demonstrate that, strictly speaking, echokinetic
yawning is not simply motor imitation.
Recognition of human faces involves specific
dedicated neurons in the temporal lobe. The
inferior temporal region (IT) allows immediate
overall recognition of faces, both their
identity and their expression, apparently
through its own autonomous, non-hippocampal
memory. As for the superior temporal sulcus
(STS), it is specifically activated during
perception of eye and mouth movements, which
suggests its implication in the visual
perception of emotions, once again by the
activation of mirror neurons. These neurons mime
the expression perceived, helping the observer
to understand it. Schürmann et al.
demonstrated that the STS is activated during
echokinetic yawning. This activation, automatic
and involuntarily, is transmitted to the left
amygdala, the posterior cingulate cortex and the
precuneus.
These structures are thought to play a role
in differentiating emotions expressed by the
human face and, especially, in evaluating the
sincerity of the sentiment expressed. Using
fMRI, Platek et al. found a correlation between
personality traits and the activation of
neuronal circuits beyond the STS. « In
contrast to those that were unaffected by seeing
someone yawn, people who showed contagions
yawing identified their own faces faster, did
better at making inferences about mental states,
and exhibited fewer schizotypal personality
characteristics. These results suggest that
contagious yawning might be related to
self-awareness and empathic processing».
Subjects considered empathetic, who were very
susceptible to echokinetic yawning, activated
the amygdala and the cingulate cortex, whereas
schizotypal subjects, who were not susceptible
to this type of yawning, did not activate these
structures. Neurophysiological studies of
empathy show similar zones of activation (STS,
insula, amygdala, cingulate cortex).
These data imply that contagious yawning may
reside in brain substrates which have been
implicated in self-recognition and mental state
attribution, namely the right prefrontal cortex
(Platek, 2003, 2005; Schürmann, 2005).
Consistent with this view, autistic children who
are characterized by impaired mental state
attribution do not show contagious yawning
(Senju et al., 2007). Giganti and Ziello (2009)
support the hypothesis of a link between
contagious yawning and social abilities and the
existence of different processes underlying
spontaneous and contagious yawning. In the
interpersonal contact with individuals with
schizophrenia we can often experience impaired
empathic resonance. Haker H, and Rössler W
(2009) try to determine differences in empathic
resonance-in terms of contagion by yawning and
laughing-in individuals with schizophrenia and
healthy controls in the context of
psychopathology and social functioning.
They conclude Individuals with schizophrenia
showed lower contagion rates for yawning and
laughing but it may be argued that the treatment
by neuroleptic drugs reduce drastically
spontaneous and contagious yawning by
themselves.
Pathology
On Tuesday, Oct.23, 1888, Jean-Martin
Charcot presented, during one of his celebrated
Tuesday gatherings at La
Salpêtrière, the case of a young
woman inconvenienced by 8 yawns a minute, that
is 480 per hour! He qualified this as a form of
hysteria, despite his examination revealing
binasal hemianopsia, right-side cheirobrachial
skin insensitivity to all stimuli and loss of
smell. Given our contemporary knowledge, this
points to a pituitary adenoma.
The disappearance of yawning may be due to
an extrapyramidal syndrome, to the use of opioid
drugs or high doses of caffeine, but is rarely a
cause for complaint. The family-medicine
practice shows that excessive yawning is a
source of embarrassment in social circles. There
are multiple causes of excessive yawning, that
is, a cluster of 10 to 30 yawns, many times a
day. Of short duration, they may predict a
vasovagal reaction or neurovegetative disorders
(dyspepsia, migraine-like syndromes). All
insults to the intra-cranial central nervous
system or the hypothalamo-hypophyseal region may
be involved: tumors with intracranial
hypertension, infections, temporal epilepsy,
strokes, etc. For example, we coined the term
"parakinesia brachialis oscitans" to describe
cases of hemiplegia where the onset of yawning
coincides with involuntary raising of the
paralysed arm. We argued that a lesion in the
internal capsule affecting an inhibitory pathway
liberates certain subcortical structures that
coordinate the massive inspiration of yawning
and the motor control associated with
quadrupedal locomotion (Walusinski, 2005).
The development of psychotropic drugs has
given rise to a rich iatrogenic pathology:
serotoninergic agents, apomorphine,
acetylcholinesterase inhibitors, sismotherapy
and, opiate withdrawal are triggers of yawn
clusters. Excessive sleepiness with excessive
yawning should suggest examination for an
obstructive sleep apnea syndrome. Finally, after
after ruling out all other causes, some patients
may be suffering from a type of chronic motor
tic disorder, associated with yawn clusters, and
treated with haloperidol (Walusinski,
2009).
Selective serotonin reuptake inhibitors
(SSRI) have significant side effects from
stimulation of 5-HT2A, 5-HT2C and 5-HT3, from
noradrenergic receptor stimulation, as well as
from interactions at other receptors including
muscarinic, histaminergic, and postsynaptic
alpha1-adrenergic. Complex neurotransmitter
systems make pin-pointing an exact mechanism of
yawning induction difficult and conflicting data
exist regarding the role of specific
neurotransmitters. Yawning as side effect was
described with paroxetine, escitalopram,
duloxetine. The excessive yawning was not
accompanied with drowsiness. The error would be
to believe in the aggravation of the depression
and to increase doses of SSRI treatment. This
side effect disappeared completely once
treatment was terminated
(Gutiérrez-Álvarez, 2007).
Conclusion
Yawning and pandiculation are a universal
behaviour amongst vertebrates, closer to an
emotional stereotypy than a reflex.
Phylogenetically ancient and ontogenetically
primitive, they exteriorize homeostatic
processes of systems controlling wakefulness,
satiety and sexuality in the diencephalon. An
arousal response accompanied by yawning behavior
can be evoked (Baenninger, 1997; Walusinski,
2006).
Suggested by:
Mr. Abdellatif Nemri, Department of
biological sciences, University of Montreal,
Canada
Invited by:
Dr. Eugene M. Izhikevich, Editor-in-Chief of
Scholarpedia, the free peer reviewed
encyclopedia
Action editor:
Dr. Eugene M. Izhikevich, Editor-in-Chief of
Scholarpedia, the free peer reviewed
encyclopedia
Assistant editor:
Mr. Abdellatif Nemri, Department of
biological sciences, University of Montreal,
Canada
Reviewers
Dr. Paul Wicks, King's College London,
London, UK
Dr. Gordon G. Gallup, State University of
New York at Albany, NY
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