Yawning and pandiculation are a universal
behaviour amongst vertebrates, closer to an
emotional stereotypy than a reflex.
Phylogenetically ancient and ontogenetically
primitive, they exteriorise homeostatic
processes of systems controlling wakefulness,
satiety and sexuality in the diencephalon.
Western and Eastern cultures ascribe different
meanings to these elements of non-verbal
communication, closely related to empathy. We
present a comparative study of popular and
medical views on the subject, in France and
India, revealing that perceptions of yawning are
not very advanced, more closely resembling
beliefs than scientific knowledge. Perhaps
medical training will one day incorporate the
study of this daily behaviour, common to all
human beings.
Since Antiquity, yawning has held as little
interest for philosophers, psychologists and
physiologists, as it has for teachers, moralists
and physicians. And yet, few things are as
common as yawning. Everyone yawns 5 to 10 times
a day. Yawning is a recognized behaviour in
almost all vertebrates from birds to humans, one
which starts in the womb and continues until
death. Although yawning often procures a sense
of well-being for the yawner, attempting to mask
this behaviour is standard practice.
Modern neuroscience is still looking for a
complete explanation of its intimate mechanisms.
But above all, its exact physiological purpose
remains a subject of debate; some see yawning as
a mechanism for stimulating wakefulness
[1], while others contest this view and
instead link yawning to the effects of a
homeostatic sleep factor accumulating throughout
the waking hours [2].
In this paper, we offer a broad-based
cultural and medical overview of the related
conceptions and myths through comparison of the
popular and medical views of Arabic, Western and
Indian cultures. This will help us support the
idea that yawning should be covered during
medical studies, along with sleep and arousal
disorders.
Beliefs
Arab countries
In 1923, Pierre Saintyves [3]
surveyed cultural beliefs related to the meaning
of yawning. According to Saintyves, Islam sees
yawning as a sign of Satan entering the body,
and sneezing as a sign of his leaving the body.
Assas-bou-Malek and others all date this opinion
back to the Prophet: "The Prophet said that
Satan endeavours to distract the faithful in
prayer. This is Allah's way of testing them. One
way Satan distracts the faithful is by
dominating their thoughts, infiltrating their
minds during prayer. Another way is by making
them yawn to divert attention away from their
prayers. The Prophet told us that yawning is
prompted by Satan and gave us the order to avoid
it whenever possible. When it becomes
inevitable, we must close our mouth with our
hand."
We recently came across this question on a
website: "I am a 22-year-old devout practising
Muslim with a problem I hope to overcome with
Allah's help and your advice. As soon as I begin
my prayers, I start yawning involuntarily. And
this continues even when I recite the Throne
Verse. I really don't know why I'm yawning
dozens of times, over and over, during a single
prayer. I hope you can shed some light on my
problem."
Saintyves also writes: "According to Ibn
Battal, attributing yawning to Satan means he
wants us to yawn and takes pleasure in it; he
enjoys this disfiguring behaviour because it
makes men look ridiculous." As to putting a hand
over the mouth, this gesture applies when the
mouth is already open, as well as when it is
still closed, "because Satan enters…".
Instead of the hand, a piece of clothing or any
other object may be used. The fear of Satan
entering the body is linked to the fear of
possession, which explains why this gesture is
demanded of the faithful during prayer
[4]. W. Seuntjens call this idea : the
demonic rationale of yawning etiquette
[5]. Moroccans would place their hand in
front of their gaping mouth because otherwise,
it was belived, the devil would urinate into
their mouth.
In India
In India, "bhuts" (spirits) are believed to
prefer entering the body through the mouth.
Yawning is therefore dangerous, because it
entails two kinds of risks: either bhuts will
penetrate the body through the throat, or a part
of the soul might escape. Since it would be very
difficult to recapture, the recommended practice
is to put a hand in front of one's mouth and say
"Narayan!" (Good God!), or snap one's fingers to
scare the bad spirit away [3].
In Ancient Mayan civilization, yawning was
thought to indicate subconscious sexual desires.
In the same way, W. Seuntjens argues an
hypothesis that yawning has an erotic side
[5]. He found that both the "yawn" and
the "stretch" of the stretch-yawn syndrome are
semantically and etymologically associated with
"desire" and "longing for". In several proverbs
and sayings yawning, and especially contagious
yawning, is interpreted as a clue of something
more than just sympathy, that is, as a sign of
being in love. Yawning was both linked with
acedia-boredom and with luxuria (lechery) and
passion. As a non-verbal behavior the yawn was
found to figure in the courtship process. That
this is not a purely recent or western
phenomenon was illustrated by passages from
ancient Indian literature [6].
In Europe
Around 590 AD, during the times of Pope
Gregory the Great, a bubonic plague epidemic
raged through Europe, decimating the population
and inspiring numerous superstitions: "Yawning
was fatal then, and the habit of signing the
cross in front of the mouth originated during
the times of the plague. [...] There was
a plague they called inguinal, because a bubo
appeared in the groins, causing men to die
suddenly in the streets, in their houses, at
play, during a meal. Their souls left their
bodies when they sneezed or yawned. This is why
we said 'God bless you' to those who sneezed.
Those who yawned made the sign of the cross over
their mouths" [5]. Even the sceptical
Michel de Montaigne conced that he made the sign
of the cross before his mouth while yawning,
given evidence for the education's power. In
Austria, in the case of a yawning baby who was
not able to perform the sign of the cross, an
older person would perform this gesture in front
of the infant's mouth in order to prevent
illness ans bad luck [5].
It is possible that the love of perfumes in
the royal European courts in the 17th and 18th
centuries had its origins in the necessity to
conceal poor body hygiene. Placing one's hand in
front of the mouth during yawning was helpful in
hiding appalling oral conditions and reducing
the expiration of nauseating odours. In a 2004
editorial for the British Medical Journal, G
Dunea [7] was surprised to see medical
students yawning frequently as they waited for
their lecturer; moreover, 67.5% of the time they
did not cover their mouths with their hands. He
suggested this allowed students to avoid
bacterial contamination of their palms,
ironically adding that it is undoubtedly better
to let others marvel at your tonsils than to
risk injuring your elbow!
In medicine
In his treatise on wind, De flatibus liber,
Hippocrates [8] noted that "the
continual yawning of apoplectics proves that air
is the cause of apoplexies", thereby confirming
his theory that "wind is the cause of all
diseases". In 1739, Hermann Boerhaave, in his
Praelectiones academicae [9], explains
that "yawning and pandiculation favour the
equitable distribution of spiritus in all the
muscles and unblock the vessels of which sleep
or rest may have slowed the functions", and that
their action fights "against the excessive
pre-eminence of the flexor muscles and returns
everything to its place". In his 1755 book De
perspiratione insensibili, Johan de Gorter
[10] 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. Even someone as knowledgeable and
inquisitive as JM Charcot repeated this maxim
without any critical analysis in his
Leçons du Mardi à la
Salpêtrière in 1888. The inaccuracy
of this hypothesis was formally shown by
Provine, Tate and Geldmacher in 1987
[11]. 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.
Phylogenesis, ontogenesis,
ethology
The existence of yawning in reptiles
confirms the primitive phylogenetic origins of
this behaviour. Its survival without any notable
evolutionary variations is an indication of its
functional importance, as confirmed by its early
ontogenetic manifestation. It coincides with the
first type of sleep involving hypotonia, which
evolves towards REM sleep between weeks 12 and
15 of pregnancy [12]. Ethology supports
the idea that almost vertebrates yawn, whether
heterotherms or homeotherms, whether herbivores,
frugivores, insectivores or carnivores, whether
they inhabit water, land or air. Probably
giraffes, whales and dolphins do not yawn; the
physiology of their sleep is not completely
understood. It seems that they be lacking of
durable REM sleep and their sleep occurs in one
by one hemisphere.
Physiology
Living organisms, particularly vertebrates,
exhibit varied behaviours which are essential to
their survival and characterised by cyclical
recurrence. This is the case for the three
behaviours fundamental to life and its
transmission: alertness (ability to survive
predators while still needing to sleep to
maintain brain homeostasis), feeding (energy
capture) and sexuality (perpetuating life).
Yawning and pandiculation are morphologically
identical and apparently associated with each
transitional state of the infradian, circadian
and ultradian rhythms which characterise them.
Rather than the result of a passive adaptation
to environmental conditions, an animal's
behavioural transitions are dictated by internal
stimuli characteristic of homeostatic
adaptations, generated in particular by the
hypothalamus (suprachiasmatic nuclei,
paraventricular nuclei). These internal
biological clocks permit a precise balancing act
between metabolic needs (satiety), survival of
the species (copulation) and environmental
conditions (tonic adaptation to weight and
movement). Yawning and pandiculation are
associated with transitions between wakefulness
and sleep, occurring at the onset of hunger or
satiety and with the ebb and flow of emotional
states secondary to living in hierarchical
social groups [13].
Yawning and pandiculation exteriorise the
activity of the motor centres of the brainstem
(V, VII, IX, X, XI, XII) and of the spinal cord,
under the control of the hypothalamic
paraventricular nucleus (PVN). The PVN is a
point of integration between central and
peripheral autonomic systems. Amongst other
things, it plays a role in metabolic balance
(osmolarity, energy), blood pressure and heart
rate, and sexuality. Yawning and pandiculation
can be triggered by injections (apomorphine,
hypocretins, etc.) or inhibited after electrical
lesion in the parvocellular zone of the PVN
[14]. A group of oxytocin neurons
situated in this zone and projecting to the
hippocampus, the brainstem (locus ceruleus) and
the spinal cord control yawning and erection.
The stimulation of these neurons by dopamine or
its agonists, such as excitatory amino acids
(NMDA), histamine and oxytocin itself, triggers
yawning and erection, whereas GABA and opioids
have an inhibitory effect [15,16,17]. A
specific role for the dopamine D3 receptor in
this behavior has yet to be elucidated. Collins
et al. report that dopamine D2/D3 agonists
elicit dose-dependent yawning behavior in rats,
resulting in an inverted U-shaped dose-response
curve. The induction of yawning is a D3
receptor-mediated effect, whereas the inhibition
of the yawning observed at higher doses is due
to competing D2 receptor activity.
[18].
Some thoughts on human pathology
On Tuesday, Oct.23, 1888, Jean-Martin
Charcot presented, during one of his
celebrated Tuesday gatherings at La
Salpêtrière, the observation 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 (when a tumor has grown around the
chiasma, it compresses the chiasma from both
sides, thus mainly affecting the laterally
located, uncressed fibers derived from the
temporal halves of the two retinas, which are
responsible for perception in the nasal
hemifield of each eye), this points to a
potential pituitary adenoma although he does not
give any information on possible loss of the
sense of smell and her menstrual status.
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 [19,20,21].
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
[22]. 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 excess of
yawns needs to search for an obstructive sleep
apnea syndrom. Finally, after After ruling out
the other causes, it seems possible to
individualise a particular type of chronic motor
tic disorder, associated with yawn clusters,
and treated with haloperidol.
Current knowledge and
beliefs about yawning
It is interesting to contrast current views
of yawning held by the physicians in France and
India, and then compare them to beliefs amongst
the general French or Indian public. We have
compared the data gathered in 1998 in France,
partially published in a journal read by the
French family physicians [23], and those
of the present study in India. In France 150
patients of a private practice (public) were
questioned during one week, whatever it may be
the consulting cause and only 5 family
physicians agreed to answer. In India, 150
anonymous questionnaire was distributed to rural
population and doctors qualified in modern
medicine and registered under Indian Medical
Council were considered and requested to fill
out all the questions (see table).
In all parts of the world, and regardless of
the level of medical knowledge, yawning is
associated with the idea of tiredness, boredom,
and lack of sleep or non-restorative sleep. Due
to their capacity to decode emotions expressed
by behaviour and facial expressions, humans add
an additional non-verbal meaning to the
physiological role of yawning. In any culture, a
yawning person sends the signal that he or she
is bored and expresses lack of interest. Western
culture associates an unfavourable connotation
and lack of respect with this behaviour.
In France, women and men are considered to
be yawn equally often; whereas in India, a
larger proportion of the people questioned
thought men yawned more often than women, which
is incorrect [24].
Curiously, 24% of the laypeople and 28 % of
the physicians, questioned in India, have
doubted the existence of yawning in animals. The
French, known for their close companionship with
dogs and cats, did not have doubts about whether
their pets yawned, but rarely knew that birds
and fish yawn as well. Oddly, many of them
thought that their yawning could trigger yawning
in their dogs. On the contrary, yawning induced
by echokinesis has only been found in great apes
and humans, and appears to be species-specific.
Modern neurophysiology explains this phenomenon
as activity in the right parietal-temporal
cortex, comparable to that observed during
empathy [25]. Echokinesis thus seems
impossible between canines and hominids. As
such, anthropomorphism can be seen in this
popular French belief [26].
All people reported appreciating the brief
pleasure associated with a successful yawn. It
is quite common for them to complain about
unsatisfactory yawning when they don't
experience the short period of relaxation that
follows, like a moment of ecstasy. Relaxation
and yoga techniques are well suited to bring
about this state of harmony [27].
Strangely, 40% of the Indian laypeople
questioned did not experience this sensation of
well-being. 55% of public and doctors felt
better after yawning. Paradoxically, 33% of the
physicians reported they know that yawning could
signal illness, versus 7% of the laypeople
questioned. This paradox may be explained by the
lack of knowledge released by the university. In
France a majority of physicians appear unable to
answer !.
Regardless of the continent, a large
proportion of the physicians is unaware that
medicine has the therapeutic to reduce the
frequency and number of yawns, compared to a
similar percentage of the general public without
any opinion (74% versus 73%). Studies have shown
that coffee reduces the number of yawns, as do
neuroleptics, baclofen (GABAergic) and
opioids.
Amongst both physicians and non-physicians,
irrespective of culture, it is well known that
women yawn more during pregnancy. This is
explained by progesterone's modulation of D3
dopamine receptors in the PVN [28].
Indians also believe that breastfeeding women
yawn more. This tendency is clearly explained by
the crucial role of oxytocin in triggering a
yawn, but the French tend not to notice it,
perhaps because French mothers have regrettably
lost interest in breastfeeding
[28].
In India unlike in France, the general
public prefer chewing something (ancestral
practice advocated by Indian folk medicine) to
try to avoid exteriorising a yawn, whereas
physicians prefer clenching their teeth.
Everyone knows that stretching or pandiculation
favours yawning rather than preventing it.
In France as in india, amongst physicians as
well as laypeople, the notion that yawning
improves the supply of oxygen to the brain is
widespread despite its inaccuracy, indicative of
a belief without critical foundations, rather
than validated scientific knowledge.
In France as in India, physicians still know
little about yawning. The most conducive times
for this behaviour &endash; upon waking, before
sleep and when hungry &endash; are known.
Likewise, the association of yawning with
vasovagal events or hypoglycemia is relevant.
Very few Indian or French practitioners evoke
stimulation to explain the physiological role of
yawning. There is little knowledge of iatrogenic
causes, even though they most frequently explain
excessive yawning, linked to serotonergic
antidepressants [21,30]. There is little
awareness of fetal yawning, which can be
observed with ultrasound, despite the negative
implications of its absence (delayed functional
maturation in the brainstem, for example).
Little is known about pathological yawning even
though it is frequent during migraines, and in
sleep apnoea, temporal lobe epilepsy, stroke,
pituitary disorders, and in
hyperactivity/attention deficit disorder.
Whether French or Indian, 100% of the
physicians questioned said yawning was never
discussed during their medical studies. Less
than 5 hours are devoted to sleep in France
during 8 year training period and only 2.5 hours
in India of 5 year training period even though
we spend a third of our lives in sleep. Yawning,
a daily behaviour at every age, is not even
considered!
The fact we know so little about this daily
activity, which like any physiological behaviour
has its own pathology, and the fact this
ignorance is equally as common amongst
physicians and laypeople can only be met with
surprise. Moving away from folk knowledge, akin
to believe in magic, and towards scientific
understanding might require integrating the
study of yawning into medical training.
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