Yawning is a stereotyped behavior that
enhances blood flow to the skull, and the
resulting counterflow has been hypothesized as a
mechanism for brain cooling. Studies have shown
that yawns are strongly associated with
physiological and pathological conditions that
increase brain temperature, and that they are
followed by equivalent decreases in brain
temperature. However, measured reductions in
cranial or facial temperatures following yawning
have yet to be reported, to our knowledge. To
accomplish this, we used a subline of
Sprague-Dawley rats that yawn at a much greater
rate (20 yawns/h) than do outbred Sprague-Dawley
rats (2 yawns/h).
Results
Using an infrared camera, we effectively
evaluated thermal changes in the cornea and
concha of these rats before, during, and after
yawns. The maximum temperature in both regions
significantly decreased 10 s following yawns
(concha: _0.3 °C, cornea: _0.4 °C),
with a return to basal temperatures after 20
s.
Conclusions
This study is the first clear demonstration
of yawning-induced thermal cooling on the
surface of the face, providing convergent
evidence that this behavior plays a functional
role in thermoregulation. As other studies have
demonstrated that yawning is capable of reducing
cortical brain temperature, our current data
support the idea that yawning functions as a
thermoregulator, affecting all structures within
the head.
Thanks to J.R. Eguibar for the picture
Background
Yawning is an innate behavior characterized
by a stereotyped motor pattern. Wide opening of
the mouth and wide dilation of the pharynx and
larynx is followed by deep inspiration that ends
abruptly with a short expiration. Neck
musculature then shrinks and returns to basal
levels [1, 2]. Understanding the
physiological significance of yawning is
important because spontaneous yawning is
ubiquitous in vertebrates [3], with
reports identifying atypical yawning as a
symptom or side-effect of several neurological
diseases or medications [4]. Many
hypotheses have been proposed regarding the
potential physiological functions of yawning;
however, they often lack clear physiological
evidence [5]. While much of the
scientific community believed that yawns serve a
respiratory function, experimental procedures
performed on humans have demonstrated that
yawning and breathing are controlled by separate
mechanisms [6]. However, other causes
such as fatigue, boredom, and sleepiness have
been proposed as causes of increased yawning
frequency [4]. One recent theory that
has gained recent experimental support proposes
that yawning is a brain cooling mechanism
[7&endash;9].
In homeotherms, brain temperature is
determined by three variables: the rate of
arterial blood flow, the temperature of arterial
blood, and the amount of metabolic heat
production [10]. The physical action of
yawning can alter the first two variables.
Yawning produces significant changes in
circulation, including accelerating heart rate
by up to 10 additional beats per minute [11,
12]. The deep inhalation and powerful jaw
stretching during a yawn also favors increases
in blood flow to the skull [13], and the
extended contraction of the lateral pterygoid
muscle during yawning acts to squeeze blood from
the associated plexus [14]. Therefore,
the gaping of the jaw and deep inhalation
increase arterial blood flow to the brain and
enhance venous return, thus acting to remove
hyperthermic blood from the skull and
simultaneously introduce cooler blood coming
from the lungs and extremities. Increased facial
blood circulation and associated changes in the
ventilation rate are two well-known mechanisms
that cool brain temperature [15,
16].
The deep inhalation of air that accompanies
yawning may also provide counter-current heat
exchange by cooling venous blood draining from
the nasal and oral orifices that is in close
contact with arterial blood supply [16].
Consistent with this view, recent studies in
human and non-human primates [8, 17]
have shown that pharyngeal cooling rapidly and
selectively decreases brain and tympanic
temperature by cooling the carotid arteries
[17]. Furthermore, anatomical
investigations in humans have revealed that the
thin sinus walls flex when pterygoid musculature
contracts during yawning, indicating that the
posterior wall of the maxillary sinus serves as
an origin for both medial and lateral pterygoid
muscle segments [18]. This powerful
flexing of the sinus walls has been proposed to
ventilate the human sinus system similarly to
what occurs in birds [19], providing a
second mechanism through which yawning functions
in human cerebral cooling. Accordingly, yawning
could reduce brain temperature by ventilating
the sinus system and promoting the evaporation
of the sinus mucosa [20]. The salivation
and tearing that accompany yawning could be a
third mechanism for cooling, aiding in heat loss
through evaporation [8].
Importantly, yawning appears to be
constrained to a narrow range of ambient
temperature (i.e., a thermal window). Numerous
reports have confirmed and replicated the
specific thermal window for various species. For
heat to dissipate; ambient temperatures must be
lower than the body temperature of the subject
animal. Thus, as predicted, in warmer
environmental situations, yawning did not cool
the brain [7&endash;9, 20]. Consistent
with models of thermoregulation, variation in
ambient temperature elicits predicted
fluctuations in yawning frequency in a number of
species, including budgerigars [21],
rats [22], white-faced capuchin monkeys
[23], and humans [20, 24].
Initial rises in temperature within this
window trigger yawning and other
thermoregulatory cooling mechanisms such as
panting and behavioral adjustments to reach
thermoneutralization. However, as external
temperatures continue to rise beyond the thermal
window, yawning decreases because
counter-current heat exchange becomes less
effective. Similarly, yawning is also reduced at
extremely cold temperatures, as thermoregulatory
cooling responses are no longer necessary
[24].
Direct measures of internal temperature in
rats and humans have shown that brain and oral
temperature rise immediately before the onset of
yawns, with corresponding decreases in
temperature being observed directly following
these events [9, 25]. One interpretation
is that yawns are triggered by elevated
temperature inside the skull, and that the
physiological consequences of yawning discussed
above result in temperature reduction.
Consistent with this view, heightened core body
temperature following handling-stress has been
shown to be correlated with earlier onset and
higher frequency of yawning in birds
[26], and experimental manipulations
designed to promote brain cooling have been
shown to diminish yawning frequency in humans
[7]. Furthermore, a number of medical
conditions and drugs affect yawning and
brain/core temperature in reciprocal patterns.
Conditions associated with rises in temperature
present with increased yawning, while those
associated with lower temperatures present with
diminished yawning [8]. However, whether
yawning reduces the temperature on the surface
of the head or in the face remains unclear.
Selective breeding of Sprague-Dawley rats
has generated a subline with a higher incidence
of spontaneous yawning [27], which is a
useful tool for the physiological study of
yawning. Yawning frequency (20 yawns/h) in these
high-yawning (HY) rats is an order of magnitude
higher than in other Sprague-Dawley rats (2
yawns/h) [27&endash;29]. Thus, HY
animals allow us an efficient means to evaluate
internal and environmental variables that
modulate yawning frequency. Indeed, HY rats were
used to determine that yawning has a circadian
oscillation pattern that includes significantly
increased yawning frequency when transitioning
from light periods to dark periods [30].
Under constant light conditions, the circadian
rhythm of yawning is disorganized, suggesting
that this behavior is not endogenously generated
[31]. However, restricting food access
to just 2 h per day produced a highly
significant increase in yawning frequency. This
is because food access can be a predictor of
food availability and can produce an
anticipatory yawning peak [31].
High-yawning rats allow us to analyze the
role of smell on contagious yawning
[32]. HY rats are also more sensitive to
cholinergic and dopaminergic agents that
increase yawning frequency [33, 34], and
to adrenocorticotrophic hormones and oxytocin
neuropeptides [29, 35], indicating a
higher sensitivity of these sublines to
environmentally and pharmacologically induced
yawning.
Based on past findings regarding yawning and
thermoregulation, the present study used a
thermographic imaging camera to measure
temperature changes associated with spontaneous
yawning that occurred in the cornea and concha
of HY rats. The concha is a good candidate
structure because the ears dissipate more heat
than other head regions and act as a thermal
buffer mechanism in many mammalian species.
Similar structures such as the cornea play
critical roles in thermoregulation, and are
frequently called thermal dissipaters because
they are responsible for heat exchange and they
regulate surface temperature [36,
37].
During yawning, the upper airways are
ventilated, and this possibly cools the blood in
the facial artery, which travels around the
mouth and nasal cavities, making terminations
around the eye and cooling these structures
[7]. Thus, the two anatomical areas that
we selected are good candidates for directly
detecting temperature change in areas not
covered by fur.
Discussion
The use of infrared thermal imaging provides
an effective means of tracking behavioral
thermoregulation through changes in surface
temperature [36, 37]. This is the first
study to document fluctuations in facial
temperature that are temporally locked to
yawning, revealing that temperatures in the
cornea and concha consistently rise leading up
to yawning events as shown in Fig. 5b (_10 s)
and then decrease below baseline levels shortly
thereafter (10 s). These results are consistent
with previous research measuring changes in
brain temperature surrounding yawns in rats
[25], and provide further evidence
supporting the idea that yawning functions to
cool the head and cortical surface
[7&endash;9].
Previous reports indicate that yawns are
triggered by rises in brain and body temperature
[21, 25, 38], which is consistent with
the pattern of temperature change we observed
preceding yawns. This is illustrated in Fig. 5b,
in which 10 s before a yawn occurs, there is a
small increase in the concha temperature that
drops significantly during and 10 s after
yawning. This is likely because this area is
more exposed to thermal influences, as has
already been demonstrated in other species
[36, 37]. Because rat brain temperature
is consistently higher than that of the arterial
blood supplying the brain [39],
increases in arterial blood flow and enhanced
venous return that result from the act of
yawning (i.e., wide opening of the mouth and
deep inhalation) could explain the cooling we
observed within 10 s of yawning. Heat convection
by blood depends on several variables, including
the volume and velocity of blood flow in the
vessels [40]. For example, increased
blood-flow velocity can result in a twofold
increase in heat transmission by tissue
[41], and specific reductions in brain
temperature have been observed because of
increased localized blood flow [42].
Therefore, the decreased temperatures that we
observed at the corneal and conchal surfaces are
consistent with various models of bio-heat
transfer that take perfusion rates into account
[43&endash;46].
We must emphasize that the main heat
regulator in rats and mice is the tail. However,
facial surface area is also a well-known heat
dissipater [47, 48]. Indeed, in humans,
the eyeball&emdash;and in particular the cornea,
iris, and sclera&emdash;are structures with high
temperature conductivity because they often have
higher temperatures than the environment
[49]. Therefore, these eye structures
function as thermal dissipaters that work
through heat convection, and even evaporation,
because tears allow the transmission of heat
from inside the cranium to the surface of the
eye [49].
The decreases in surface temperature at the
cornea and concha sites correspond with
previously documented changes in brain-tissue
temperature following yawning events in rats.
Shoup-Knox et al. [25] showed that
temperature in the prelimbic cortex rise sharply
just before yawns and then begin to drop after
about 18 s, with maximum cooling occurring at
about 60 s following this transition. This time
course is much longer than what we observed
externally on the eye and the ear, and metabolic
heat production from neuronal activity inside
the skull should interact with other structures
and blood flow that can be responsible, at least
in part, for the delayed responses. Together,
these observations provide a consistent timeline
for a functional role of yawning in cooling the
brain, with temperature reductions at external
surfaces preceding those at internal brain
tissue. It is valid, therefore, to mention that
both phenomena share common mechanisms and are
temporally linked. Additional experiments are
necessary to establish a causal
relationship.
Cooling of external surfaces in the head
might also contribute to cooling of internal
tissues. In humans, the ophthalmic vein, like
other emissary veins, has been reported to play
an important role in cerebral cooling and may
even reverse blood flow depending on the
temperature conditions of the environment.
Therefore, during hypothermia, blood travels
from the brain to the surface of the face,
whereas during hyperthermia the opposite pattern
occurs [50]. Because yawning in rats and
humans has already been demonstrated to be
triggered by increases in brain and oral
temperature [25, 38], cooling of
external surfaces such as the eye and ear could
directly alter brain temperature. Our
observations of a mean reduction of _0.32
°C in the cornea and _0.48 °C in the
concha are consistent with the reduction of just
over _0.11 °C in the cerebral cortex of
rats following yawns observed in a previous
study [25]. The differences can be
explained by the heat gain/loss ratio that
follows circulation in blood vessels, as well as
by differences in the quantity of blood supply
to the brain and face, which are governed by
different vascular tones and by evaporation in
the paranasal sinuses [51]. Importantly,
the corneal surface immediately returned to
pre-yawning temperatures because blood in the
ophthalmic artery carries heat continuously from
inside the cranium, and in the case of the
concha, heat-loss primarily results from
convection and conduction mechanisms.
Importantly, Sato-Suzuki et al. [52]
showed that chemical or electrical stimulation
of the paraventricular nucleus of the
hypothalamus evoked yawning and shifted EEG
activity from delta to theta rhythms. They also
showed an association between a drop in blood
pressure and skin conductance supporting changes
in the sympathetic inhibitory responses. Our
results showed changes in the temperature of
facial structures due to changes in the blood
flow to the head. These changes are closely
associated with the loss of heat in the
oropharynx due to air flow, and support the
validity of the thermoregulatory role of
yawning.
Conclusion
Our results are consistent with a growing
number of comparative studies supporting the
thermoregulatory theory of yawning [9].
The use of HY rats in this study provides an
effective sample population for this
investigation because of their high frequency of
spontaneous yawning. However, further studies
using similar thermal imaging techniques are
needed to replicate these findings in other
lines or species with more typical yawning
patterns.
