Department of Physiology,
Gian Sagar Medical College, Ramnagar, Patiala,
India
Although yawning is a commonly witnessed
human behavior, yet it has not been taught in
much detail in medical schools because, until
the date, no particular physiological
significance has been associated with it. It is
characterized by opening up of mouth which is
accompanied by a long inspiration, with a brief
interruption of ventilation and followed by a
short expiration. Since time immemorial, yawning
has been associated with drowsiness and boredom.
However, this age old belief is all set to
change as the results of some newer studies have
pointed out that yawning might be a way by which
our body is trying to accomplish some more
meaningful goals. In this review, we have tried
to put together some of the important functions
that have been proposed by a few authors, with
the hope that this article will stimulate the
interest of newer researchers in this hitherto
unexplored field.
INTRODUCTION
Yawning consists of an involuntary wide
opening of mouth with maximal widening of jaw,
together with a long and deep inhalation through
the mouth and nose, followed by a slow
expiration, associated with a feeling of
comfort. The average duration of the yawn is 5
s.[1] Additionally, stretching of the
limbs also frequently accompanies yawning in
humans.[2] Yawning has long been thought
to be a sign of boredom and is commonly
interpreted as disrespectful when carried out in
the presence of others. It is also contagious as
seeing, hearing, reading or even thinking about
yawning can trigger yawns.[3]
Remarkably little interest has been paid to
yawning in research, even though it is an
everyday phenomenon.[4] Modern science
is still on the lookout for a complete
explanation of the mechanisms and the purpose
which yawning accomplishes, and the debate about
its usefulness is still ongoing.[5]
Through this review, we have tried to give a
brief insight into the various theories that
have been proposed by different authors
world-wide, so as to explain the possible
physiological significance of this seemingly
useless act.
YAWNING AND AROUSAL
Evidence suggests that drowsiness is the
most common stimulus of yawn. Boredom occurs
when the main source of stimulation in a
person's environment is no longer able to
sustain their attention. This induces drowsiness
by stimulating the sleep generating system. At
this moment, the mind has to make an effort to
maintain contact with the external
environment.[1] Vick and
Paukner[6] observed the yawning pattern
variations in a group of 11 captive chimpanzees
with respect to their daily activities. It was
seen that while the majority of the yawns were
displayed in close proximity to some sort of
activity (e.g., play bouts, feeding, sexual
contexts, etc.), only a few were connected to
sleepiness (e.g., just before sleeping or
immediately upon awakening). A major limitation
of this study which might affect the yawning
rates and patterns might have been the presence
of human observers in close proximity to the
primates.
Various studies have indicated an increase
in arousal level after yawning as reflected by a
significant change in the various physiological
variables. Corey et al.[7] investigated
the physiological effect of yawning in a group
of 48 students (mean age 18.94 ± 1.51
years) and found that there was a significant
rise in the heart rate at the peak of yawning (P
< 0.001), 10 s post-yawning (P = 0.002) and
15 s post-yawning (P < 0.001) as compared to
baseline values. It was also reported that this
rise in heart rate lasted atleast until 5 s
since there was no significant difference in the
heart rates at the peak of yawning and at 5 s
post-yawning (P = 0.049). A significant increase
was also seen in the skin conductance, at the
peak of yawning and at 5 s post-yawning
intervals as compared to baseline levels (P <
0.01). Barry et al.[8] examined the
effect of single oral dose of caffeine on
resting state arousal levels in a group of 18
healthy university students (mean age 21 years)
and reported that caffeine intake resulted in a
significant increase in the skin conductance
levels and frequency of alpha waves of
electroencephalogram. These results were found
to be similar to those obtained in yawning
subjects, by other researchers. Since caffeine
is a well-known stimulant of the nervous system,
thus it was argued that yawning, like caffeine,
might also play a role in arousal reflex of
brain.
The arousal occurring after yawning is being
considered to be due to the mechanical
stimulation of carotid body. The strategic
location of this structure results in its
stimulation due to the compressions and
movements caused by yawning. The carotid bodies
are highly vascularized, and their compressions
may thus affect their shunt system, thereby
leading to release of hormones such as adenosine
and catecholamines, which subsequently mediate
the arousal response.[9]
More frequent yawning is associated with
viewing uninteresting repetitive stimuli rather
than viewing interesting stimuli.[10]
Majority of the yawning episodes have been
recorded during activities requiring minimal
interaction, such as attending lectures,
studying, driving, and watching television. The
opposite has been reported with activities that
are of a faster and more interactive nature,
such as cooking, cleaning, washing, and talking.
This further supports the notion that yawning
sub-serves arousal and is implicated in higher
brain activation following yawn
episodes.[11]
YAWNING AND BRAIN COOLING
Recently, another physiological function of
yawning has been proposed, that is, it regulates
the temperature of the brain. It has been
postulated that yawning might "cool" down the
brain when its temperature
increases.[12] An evidence for this
proposition comes from a research in which the
prelimbic cortical brain temperature recordings
were continuously monitored in rats (Rattus
Norvegicus) during the 3 min prior to and
following a yawn, it was seen that cortical
temperatures were significantly raised until the
onset of yawn, followed by a significant fall
and return to baseline in the next 3 min after
yawning.[13]
In addition, studies in both animal and
human models provide a growing evidence that
yawning occurs before, during and after
instances of abnormal thermoregulation, heat
stress and hyperthermia. One of this
studies[14] was carried out in parakeets
(Melopsittacus undulatus), who were chosen due
to their relatively large brain size. In this,
the authors observed that a rise in the ambient
temperature was associated with a significant
increase in the incidence of yawning.
Additionally, yawning also became more frequent
as the ambient temperature rose to within
0.5°C of the parakeet body temperature,
indicating the occurrence of a breech in the
thermal homeostasis at this point. Accordingly,
it was proposed that temperature has a decisive
role in yawning. However, a leading concern was
the presence of some uncontrolled factors, such
as the differences in the individual drowsiness
levels of parakeets, as well as an absence of a
direct comparison with controls, both of which
might have affected the outcome of the
study.
The effect of alteration of the brain
temperature on the frequency of contagious yawns
was investigated by Gallup and
Gallup.[15] In a separate study in which
they induced yawning in the subjects by showing
them videos of yawning persons. The effect of
placing a warm pack or an ice pack on the
foreheads of these subjects on their yawning
frequency was also noted simultaneously. It was
observed that the cold pack was associated with
a decrease in contagious yawning while the warm
pack increased the frequency of yawning. This
was interpreted as evidence of the role of brain
thermoregulatory mechanism in the genesis of
yawning. However, this experiment did not
control the confounding factors. For instance,
having an ice pack on one's forehead might
itself be responsible for the arousal effect
while a warm pack would tend to induce
relaxation and drowsiness. Thus, it is not
possible to distinctly distinguish between the
effects of temperature and sleepiness in this
study.
The physiological consequences of yawning
are analogous to those which are needed to
effectively cool the brain, such as increase in
the peripheral and cerebral blood
flow.[16,17] The contraction and
relaxation of facial muscles during a yawn,
increases the facial blood flow which
subsequently aids in dissipation of heat through
emissary veins. The gaping of mouth and deep
inhalation of cool air during a yawn also alters
the temperature of blood going from the lungs to
the brain via convection. Tearing from the eyes,
which some people experience, at the peak of
yawn may likewise play a role in dissipation of
heat from skull.[14]
Patients with clinical disorders such as
multiple sclerosis, epilepsy, migraine, stress,
anxiety, head trauma, and stroke experience
excessive yawning which is followed by temporary
cessation of their symptoms. This is because
these conditions lead to an increase in the body
core temperature, thereby resulting in abnormal
thermoregulation, which the body then tries to
correct transiently by way of
yawning.[18-22]
YAWNING AND SOCIAL EMPATHY
Yawning has a well-known contagious effect
in humans and this effect is now frequently used
to induce yawning for research purposes. The
susceptibility to contagious yawning correlates
with empathic skills in healthy
humans.[23,24] Various clinical,
psychological and neurological clues link the
yawn contagion with empathy. Millen and
Anderson[25] conducted a two part study
on infants and preschool children to investigate
whether they also showed susceptibility to
contagious yawning like older children and
adults or not. In the first part of the study,
20 mothers were asked to record the occurrence,
time, and context of every yawn that occurred in
their children (aged 6-34 months) on a logbook,
over a 1 week period. A total of eight logs were
returned and analyzed. It was observed that the
most common context of yawns was on awakening
after morning or afternoon naps (31.7%).
Furthermore, none of the mothers made any
reference to any possible contagious yawning
episode. In the second part of study, 22 infants
and toddlers were observed for contagious
yawning while viewing the video clips of their
yawning mothers. These clips were inserted
within a series of images of unfamiliar
individuals who were either smiling or yawning.
It was seen that 16 children did not yawn at all
throughout the entire study, while two children
yawned once during the presentation and the rest
of the four children yawned once,
post-presentation. On the basis of these
observations, the authors proposed that infants
and preschool children appear largely immune to
contagious yawning, even if the stimulus is an
emotionally significant one. This is in marked
contrast to older children and adults. The small
data group analyzed was recognized as a major
limitation in this study by the authors. The
latter also maintain that some discrepancies
might also have arisen if the parents may have
missed some of their child's yawns. Therefore,
contagious yawning can be induced in children
only after 4-5 years of age, as below this age
group, the neural mechanisms required to
understand the mental state of others are still
under development.[26]
Extensive evidence indicates that the
susceptibility of contagious yawning is reduced
in patients who are suffering from disorders
that affect the ability of social interaction.
Haker and Rössler[27] investigated
the changes in yawning patterns in a group of 43
schizophrenic outpatients, after presenting them
with video sequences of yawning, laughter, and
neutral faces. On comparing the results with
those obtained in an age and sex matched group
of healthy controls, they observed that
schizophrenic individuals showed significantly
lower contagion rates for yawning as well as
laughter. Similarly, in another study carried
out by Senju et al.[28] analysis of
yawning patterns was carried out in a group of
24 children with autism spectrum disorder and
results were compared with a control group of 25
healthy children. Both groups were observed
closely while viewing yawning videos or control
video clips (of mouth opening) in a random
sequence. It was observed that yawning videos
induced lesser yawns in autistic children as
compared to healthy ones (P = 0.01), but the
control video clips showed no significant
difference between the two groups in the no. of
yawns (P > 0.1). Also, in the healthy
children, yawning videos elicited more yawns as
compared to control videos (P = 0.038) while
children with autism did not show any
significant difference between yawning and
control videos (P > 0.1).
Different neuroimaging studies also support
the empathic basis of contagious yawning.
Significantly higher functional magnetic
resonance imaging activations in response to
contagious yawning have been observed in
posterior cingulated area,[24] bilateral
superior temporal sulcus[29] or
venteromedial prefrontal cortex.[30]
Although all these areas are divergent, but they
seem to be a part of a distributed neural
network related to empathy and social
behavior.[26]
Recently, the mirror neuron system of the
brain, a collection of neurons in the right
posterior inferior frontal gyrus has been
suggested to be involved in contagious
yawning.[29,31] Mirror neurons are
considered to be important for perception and
understanding of motor actions, which is a
pre-requisite for "true-imitation," that is, the
exact copying of a goal directed
behavior.[32]
The results of a study conducted by Norscia
and Palagi[33] have provided evidence
for the fact that the social bond associated
with empathy affects the yawn contagion in
humans in terms of occurrence, frequency and
latency. In this study, a total of 109 adults
(>16 year old) of various nationalities, were
observed closely in their natural settings
(e.g., in workplaces, restaurants, etc.). All
the yawns that were triggered by a person
(yawner) and by the potential responder
(observer) who was in possible audio/visual
contact with the yawner were recorded. A total
of 613 bouts of yawning were observed, out of
which only 480 were analyzed, since only they
could be definitely assigned as being triggered
in an observer by a specific audio-visual
contact with a yawner, within a 3 min time slot.
It was seen that the social bond had a strong
significant effect on yawn contagion (P <
0.001) since the latter showed a definitive
empathic gradient, increasing from strangers
<acquaintances <close friends <kin. The
importance of the social bond in shaping the
yawn contagion demonstrates that empathy and
yawning are strongly correlated.
The link between empathy and contagious
yawning is further supported by the data
collected by Campbell and de Waal.[34]
In this study, 23 adult chimpanzees were
observed for contagious yawning while viewing
the videos of yawning and control movements of
the mouth of ingroup (same species) or outgroup
(different species, i.e., humans) individuals.
The ingroup videos were shown before the
outgroup videos to all the subjects. It was
ensured that all the subjects paid similar
attention to both types of videos. Each
chimpanzee was exposed to the videos for a total
of 20 min on one or more days, depending upon
his interest and cooperativeness, to eliminate
the effect of stress. Also, none of the test
subjects were able to see the other chimpanzees
while viewing the videos. It was observed that
the subjects yawned more frequently in response
to ingroup yawn videos than to ingroup control
videos (P = 0.002) while no difference was
observed in the rate of yawning between the
outgroup yawn and control videos (P = 0.175).
Also, the yawning response was more to the
ingroup yawn video as compared to the outgroup
yawn video (P = 0.012). Even though, the authors
do maintain that their results suggest a
possible relationship between yawning and
empathy, yet they also admit a few limitations
of their study. One of these is the smaller size
of the study sample and the other might be
attributed to the social behavior of the
chimpanzees', that is, even though there are
only chimpanzees in the ingroup videos, yet even
these "ingroup individuals" might actually be
recognized as "outgroup individuals," especially
if the chimpanzees in the videos and the ones
being tested belong to separate groups. This may
be due to the fact these animals are territorial
and form small coteries, which are aggressive to
neighboring ones. Such a kind of behavior is
absent in humans since the latter do not always
view strangers as belonging to an outgroup.
It is thus concluded that yawning may be a
part of action repertoire of empathic and
communicative processes in adult humans and some
other mammals which provide for a strong social
role of yawns in these species.[12]
YAWNING AND EAR PRESSURE
Yawning relieves the ear discomfort and
hearing problems that are commonly experienced
by people during rapid altitude changes in
airplanes and elevators. This is achieved by
opening of the eustachian tubes due to the
contraction and relaxation of tensor tympani and
stapedius muscles. This observation has led to
another proposition that yawning might actually
serve as a "defence reflex" of the ear, which is
triggered either by rapid altitude changes or by
other conditions that lead to trapping of air in
the middle ear, and is helpful in equalising the
air pressure in the middle ear with the outside
air pressure. An crucial experimental evidence
that provides support to the above proposition
comes from the work of Winther et
al.[35] In this study, a contrast dye
kept at the nasopharyngeal orifice of the
eustachian tube was found to reflux into the
middle ear cavity, in four out of a total of six
healthy volunteers, during yawning. The contrast
material was detected in middle-ear by
computerized tomographic scan of the temporal
bone.
However, since the eustachian tube can also
be opened by swallowing and Valsalva manoeuvre,
thus yawning, by itself, does not appear to
offer an indispensable evolutionary advantage of
releasing middle ear pressure. The latter effect
thus does not seem to be the primary purpose of
yawning.[12]
YAWNING AND BRAIN HYPOXIA
For the past several centuries, a commonly
held notion associated with yawning is that it
is triggered when blood or brain oxygenation is
insufficient, that is, when oxygen (O2) levels
decrease and carbon dioxide (CO2) concentration
rises. Yawning is thought to remove "bad air"
from the lungs and increase O2 circulation in
the brain.[36]
However, this belief has been discarded in
wake of the results of a recent study in which
the yawning frequency was unaffected in subjects
who breathed air mixtures containing either more
than normal CO2 or even pure
O2.[37]
CONCLUSION
In 1986, Provine, the pioneer of yawning
research wrote that "Yawning may have the
dubious distinction of being the least
understood, common human behavior."[2]
Today, more than 20 years later, this may well
still be the scenario as we are yet to find a
definitive solution to this age old
conundrum.
Yawning research is intriguing because the
ubiquity of this phenomenon across most of the
vertebrate classes and even in a 20 week old
human fetus,[9] suggest that considering
it merely as an act of boredom and drowsiness is
unjustified and that it may have a definitive
underlying physiological importance which needs
to be meticulously explored. However, till we
get a conclusive answer, it is safe to assume
that yawning could represent a para-linguistic
signal that may have multiple functional
outcomes across various species.
REFRENCES
1. Askenasy JJ. Is yawning an arousal
defense reflex? J Psychol. 1989;123:609-21.
[PubMed: 2558182]
2. Provine RR. Yawning as a stereotyped
action pattern and releasing stimulus. Ethology.
1986;72:109-22.
3. Provine RR. Yawning. Am Sci.
2005;93:532-9.
4. Simonds AK. Curbside consult: Why do
people yawn? West J Med. 1999;170:283.
[PMCID: PMC1305587] [PubMed:
18751145]
5. Walusinski O. Popular knowledge and
beliefs. Front Neurol Neurosci. 2010;28:22-5.
[PubMed: 20357458]
6. Vick SJ, Paukner A. Variation and context
of yawns in captive chimpanzees (Pan
troglodytes) Am J Primatol. 2010;72:262-9.
[PMCID: PMC2936766] [PubMed:
20014109]
7. Corey TP, Shoup-Knox ML, Gordis EB,
Gallup GG., Jr Changes in physiology before,
during, and after yawning. Front Evol Neurosci.
2011;3:7. [PMCID: PMC3251816]
[PubMed: 22319494]
8. Barry RJ, Rushby JA, Wallace MJ, Clarke
AR, Johnstone SJ, Zlojutro I. Caffeine effects
on resting-state arousal. Clin Neurophysiol.
2005;116:2693-700. [PubMed:
16221568]
9. Matikainen J, Elo H. Does yawning
increase arousal through mechanical stimulation
of the carotid body? Med Hypotheses.
2008;70:488-92. [PubMed: 17709210]
10. Provine RR, Hamernik HB. Yawning:
Effects of stimulus interest. Bull Psychon Soc.
1986;24:437-8.
11. Kasuya Y, Murakami T, Oshima T, Dohi S.
Does yawning represent a transient arousal-shift
during intravenous induction of general
anesthesia? Anesth Analg. 2005;101:382-4.
[PubMed: 16037148]
12. Guggisberg AG, Mathis J, Schnider A,
Hess CW. Why do we yawn? Neurosci Biobehav Rev.
2010;34:1267-76. [PubMed: 20382180]
13. Shoup-Knox ML, Gallup AC, Gallup GG,
McNay EC. Yawning and stretching predict brain
temperature changes in rats: Support for the
thermoregulatory hypothesis. Front Evol
Neurosci. 2010;2:108. [PMCID:
PMC2965053] [PubMed: 21031034]
14. Gallup AC, Miller ML, Clark AB. Yawning
and thermoregulation in budgerigars
(Melopsittacus undulatus) Anim Behav.
2009;77:109-13.
15. Gallup AC, Gallup GG., Jr Yawning as a
brain cooling mechanism: Nasal breathing and
forehead cooling diminish the incidence of
contagious yawning. Evol Psychol.
2007;5:92-101.
16. Askenasy JJ, Askenasy N. Inhibition of
muscle sympathetic nerve activity during
yawning. Clin Auton Res. 1996;6:237-9.
[PubMed: 8902321]
17. Greco M, Baenninger R. Effects of
yawning and related activities on skin
conductance and heart rate. Physiol Behav.
1991;50:1067-9. [PubMed: 1805271]
18. Postert T, Pöhlau D, Meves S,
Nastos I, Przuntek H. Pathological yawning as a
symptom of multiple sclerosis. J Neurol.
1996;243:300-1. [PubMed: 8936365]
19. Yankovsky AE, Andermann F, Dubeau F.
Post-ictal forceful yawning in a patient with
nondominant hemisphere epilepsy. Epileptic
Disord. 2006;8:65-9. [PubMed:
16567329]
20. Jacome DE. Compulsive yawning as
migraine premonitory symptom. Cephalalgia.
2001;21:623-5. [PubMed: 11472391]
21. Witterseh T, Wyon DP, Clausen G. The
effects of moderate heat stress and open-plan
office noise distraction on SBS symptoms and on
the performance of office work. Indoor Air.
2004;14(Suppl 8):30-4. [PubMed:
15663458]
22. Cattaneo L, Cucurachi L, Chierici E,
Pavesi G. Pathological yawning as a presenting
symptom of brain stem ischaemia in two patients.
J Neurol Neurosurg Psychiatry. 2006;77:98-100.
[PMCID: PMC2117389] [PubMed:
16174652]
23. Smith EO. Yawning: An evolutionary
perspective. Hum Evol. 1999;14:191-8.
24. Platek SM, Mohamed FB, Gallup GG., Jr
Contagious yawning and the brain. Brain Res Cogn
Brain Res. 2005;23:448-52. [PubMed:
15820652]
25. Millen A, Anderson JR. Neither infants
nor toddlers catch yawns from their mothers.
Biol Lett. 2011;7:440-2. [PMCID:
PMC3097853] [PubMed: 21123252]
26. Saxe R, Carey S, Kanwisher N.
Understanding other minds: Linking developmental
psychology and functional neuroimaging. Annu Rev
Psychol. 2004;55:87-124. [PubMed:
14744211]
27. Haker H, Rössler W. Empathy in
schizophrenia: Impaired resonance. Eur Arch
Psychiatry Clin Neurosci. 2009;259:352-61.
[PubMed: 19377866]
28. Senju A, Maeda M, Kikuchi Y, Hasegawa T,
Tojo Y, Osanai H. Absence of contagious yawning
in children with autism spectrum disorder. Biol
Lett. 2007;3:706-8. [PMCID: PMC2391210]
[PubMed: 17698452]
29. Schürmann M, Hesse MD, Stephan KE,
Saarela M, Zilles K, Hari R, et al. Yearning to
yawn: The neural basis of contagious yawning.
Neuroimage. 2005;24:1260-4. [PubMed:
15670705]
30. Nahab FB, Hattori N, Saad ZS, Hallett M.
Contagious yawning and the frontal lobe: An fMRI
study. Hum Brain Mapp. 2009;30:1744-51.
[PubMed: 18937281]
31. Arnott SR, Singhal A, Goodale MA. An
investigation of auditory contagious yawning.
Cogn Affect Behav Neurosci. 2009;9:335-42.
[PubMed: 19679768]
32. Rizzolatti G, Craighero L. The
mirror-neuron system. Annu Rev Neurosci.
2004;27:169-92. [PubMed: 15217330]
33. Norscia I, Palagi E. Yawn contagion and
empathy in Homo sapiens. PLoS One.
2011;6:e28472. [PMCID: PMC3233580]
[PubMed: 22163307]
34. Campbell MW, de Waal FB.
Ingroup-outgroup bias in contagious yawning by
chimpanzees supports link to empathy. PLoS One.
2011;6:e18283. [PMCID: PMC3071812]
[PubMed: 21494669]
35. Winther B, Gwaltney JM, Jr, Phillips CD,
Hendley JO. Radiopaque contrast dye in
nasopharynx reaches the middle ear during
swallowing and/or yawning. Acta Otolaryngol.
2005;125:625-8. [PubMed: 16076711]
36. Schiller F. Yawning? J Hist Neurosci.
2002;11:392-401. [PubMed: 12557656]
37. Provine RR, Tate BC, Geldmacher LL.
Yawning: No effect of 3-5% CO2, 100% O2, and
exercise. Behav Neural Biol. 1987;48:382-93.
[PubMed: 3120687]
