The function of the paranasal sinuses has
been a controversial subject since the time of
Galen, with many different theories advanced
about their biological significance. For one,
the paranasal sinuses have been regarded as
warmers of respiratory air, when in actuality
these structures appear to function in cooling
the blood. In fact, human paranasal sinuses have
been shown to have higher volumes in individuals
living in warmer climates, and thus may be
considered radiators of the brain. The
literature suggests that the transfer of cool
venous blood from the paranasal sinuses to the
dura mater may provide a mechanism for the
convection process of cooling produced by the
evaporation of mucus within human sinuses. In
turn, the dura mater may transmit these
temperature changes, initiated by the cool
venous blood from the heat-dissipating surfaces
of the sinuses, to the cerebrospinal fluid
compartments. Furthermore, it has recently been
demonstrated in cadaveric dissections that the
thin bony posterior wall of the maxillary sinus
serves as an origin for both medial and lateral
pterygoid muscle segments, an anatomic finding
that had been previously underappreciated in the
literature. The present authors hypothesize that
the thin posterior wall of the maxillary sinus
may flex during yawning, operating like a
bellows pump, actively ventilating the sinus
system, and thus facilitating brain cooling.
Such a powered ventilation system has not
previously been described in humans, although an
analogous system has been reported in
birds.
Introduction
The brain is exquisitely sensitive to
temperature elevation and therefore must be
protected from overheating. Mammalian brain
temperature is controlled by three variables,
including the rate blood flows to the brain, the
temperature of the blood supply, and metabolic
heat production [1]. Mechanisms for
selective brain cooling (SBC) are well
documented in mammals and birds [2,3],
enabling these animals to maintain brain
temperature below the temperature of the rest of
the body during periods of hyperthermia. The
carotid rete (cranial retia mirabilia), a
specialized heat exchanger made up of a vascular
structure located at the base of the skull in
some mammals, facilitates countercurrent heat
exchange and contributes to SBC. Whether humans
demonstrate SBC is still under debate
[4,5].
The prospect of SBC in humans has been a
controversial topic because the vascular
architecture of humans is drastically different
from that of other mammals that have this
selective cooling capacity. In addition to
lacking a carotid rete, it has been suggested
that other anatomical a b s t r a c t
considerations in humans (i.e., sweating and
vasodilation via skin) make SBC an unnecessary
component in brain thermoregulation [6].
Despite these anatomical differences, however,
it has been argued that SBC still occurs in
humans during hyperthermia [7]. For
instance, the upper respiratory tract, face and
mucosal surfaces of the nose, cerebrospinal
fluid, tympanic cavity, and angular and emissary
veins have all been suggested as components of
an SBC system in humans [8]. In fact,
using measures of intracranial temperatures
between the frontal lobe and cribriform plate,
Mariak et al. (1999) have shown that cooling may
be achieved through the upper respiratory tract
[9]. Furthermore, other anatomical
considerations allow for the outermost layers of
the cortex to be locally cooled during sweating
[10]. Jessen (2001) has reviewed the
literature regarding SBC in humans, concluding
that while there is neither physiological
evidence nor anatomical potential for whole
brain cooling, partial or localized cooling is
possible.
Birds have a similar vasculature to some
mammals, possessing an ophthalmic rete, and they
too show a capacity for SBC. In fact, brain
temperatures are maintained close to 1 C below
core body temperatures and this is most
pronounced during flying and running
[1]. Similar to some mammals,
thermoregulatory behaviors in birds include
panting, a behavior that increases the rate of
evaporative water loss from the mouth and lining
of the throat, ultimately promoting evaporative
cooling during heat stress [11]. It is
interesting to note that the opening and closing
of the jaw in birds induces negative and
positive air pressure changes, which in turn
allow their sinus system to be actively
ventilated, acting as a bellows pump
[12]. This system is made possible by
the fact that the bird's sinus system is only
partially encased in bone and interweaves with
their jaw musculature. The significance of this
so-called ''suborbital sac'' is that it provides
a mechanism for actively ventilating the bird's
sinus (i.e., pumping air in and out).
Furthermore, the discovery of a dense venous
plexus surrounding the sinus suggests a
physiological role in thermoregulation as a
contributor to SBC [13].
In birds, movements of the lower jaw, such
as closing and opening the mouth, set up
positive and negative pressures in their
suborbital sac because of its intimate
relationship to the jaw muscles. These pressure
changes are transferred to the sinus and thus,
act like a bellows pump, as air passes to and
from between the nasal cavity and sinus. Aside
from panting, it is possible that other jaw
movements such as yawning may activate this
system during periods of heat stress. Consistent
with this view, recent research investigating
behavioral changes during ambient temperature
manipulations in budgerigars (Melopsittacus
undulatus) has shown that rising temperatures
increase the frequency of yawning [14].
A subsequent study demonstrated that this effect
was not simply to due to temperature change in
general, as the same range of decreasing
temperatures left yawning unaffected
[15]. Moreover, yawning was positively
correlated with panting and other
thermoregulatory behaviors during these
experiments [15].
It has been proposed that this powered
ventilation system is unique to birds, and is
not possible in humans, as human sinuses are
believed to be dead-air spaces with air exchange
occurring only very slowly through diffusion
[16]. The present authors challenge this
view, reviewing recent evidence suggesting that
the anatomy of the human paranasal sinus can be
actively ventilated during abduction and
adduction of the mandible.
Selective brain cooling and paranasal
sinuses
Irmak et al. (2004) hypothesize that SBC
protects the human brain from thermal damage in
a long-standing manner by allowing adaptive
mechanisms to adjust craniofacial morphology
[8]. These same authors also point out
that bigger paranasal sinuses in humans provide
more evaporative surfaces. The paranasal sinuses
had been regarded as humidifiers and as warmers
of respiratory air, when in actually these
structures function to cool the venous blood
within their vessels and are likely components
of a SBC mechanism in humans. The transfer of
cool venous blood from the paranasal sinuses to
the dura mater provides a mechanism for the
convection process of cooling produced by the
evaporation of mucus within these sinuses
[10]. In turn, the dura mater may
transmit these temperature changes to the
cerebrospinal fluid ventricles. The paranasal
sinuses have been shown to have higher volumes
in individuals living in hotter climates
[8], and thus may be considered
radiators of brain. Indeed, a higher volume of
paranasal sinuses would be more beneficial for
SBC in thermally challenging environments.
Previous research involving twenty cadaveric
dissections has revealed that the posterior wall
of the maxillary sinus serves as an origin for
both medial and lateral pterygoid muscle
segments (see Fig. 1) [17]; an anatomic
finding in humans that has previously been
underappreciated in the literature. The
maxillary sinus is the largest of the paranasal
sinuses, and this pneumatic cavity occupies the
greater part of the maxillary bone. The usual
capacity of this sinus is between 12 and 18 cc.,
with an average of approximately 15 cc. The
inner as well as most of the posterior and outer
walls are generally very thin and often in
places of ''papery delicacy'', as is the roof of
this sinus [18]. All of the paranasal
sinuses open into the nasal cavity, and the
mucous membrane lining the maxillary sinus is
continuous with that covering the lateral wall
of the nasal fossa.
As a result, the current authors postulate
that the thin sinus walls may flex when the
pterygoid musculature contracts during jaw
activity, such as yawning. This powerful flexing
may act to ventilate the human sinus system
similar to that described in birds. Therefore
the proposed ventilation process may assist in
controlling brain temperature and insuring the
maintenance of integrated functions of the
brain.
Yawning as a brain cooling mechanism
A growing body of literature has already
demonstrated a connection between yawning and
thermoregulation [19,20]. In particular,
it has been proposed that yawning may function
as a brain cooling mechanism in homeotherms
[21]. As a more direct test of this
hypothesis, recent research has used implanted
thermocoupled temperature probes in the
pre-limbic cortex of rats to track brain
temperature fluctuations surrounding spontaneous
yawning events [22]. Results show that
yawning was preceded in all instances by rapid
increases in brain temperature, with
correspondingly consistent decreases in brain
temperature and a return to baseline after each
yawn. In accord with these findings, recent
research has shown that under-wing body
temperature of budgerigars is negatively
correlated with yawn latency (i.e., hyperthermic
birds yawn sooner) following handling stress
[23]. Furthermore, a number of studies
have now documented either a positive or
curvilinear relationship between ambient
temperature and yawning frequency, including
reports on birds [14,15], rats
[24] and primates [25,26].
Research on humans is consistent with these
comparative studies, providing support that
rises in brain and/or body temperature trigger
yawning, and this may contribute to localized
cooling. In a recent case report of a patient
who suffered from frequent and debilitating
bouts of excessive yawning, oral temperature
recordings revealed that onset of these episodes
occurred during mild hyperthermia and were
followed by significant decreases in temperature
(see Fig. 2) [27]. Convergent support
comes from research showing that methods of
behavioral brain cooling (e.g., nasal breathing
and forehead cooling) effectively diminish the
incidence of yawning in humans [21,27].
Yawning also follows a circadian pattern in
humans [28], occurring often in the
evening, when brain temperature is at its peak,
and upon waking, when brain temperature begins
increasing from its lowest point [29].
Gallup and Gallup (2008) have reviewed
literature showing that a number of medical
conditions associated with thermoregulatory
dysfunction are also accompanied by frequent
yawning (e.g., epilepsy, multiple sclerosis)
[19].
Moreover, certain drugs that increase brain
temperature produce excessive yawning
[30], while drugs and neurotransmitters
that produce hypothermia diminish yawning
frequency [31&endash;33]. Similarly,
extensive research shows that yawning is under
the control of the hypothalamus [32], a
brain structure strongly linked to
thermoregulation [34]. Taken together,
this research suggests that yawning is
inherently connected with thermoregulatory
system, and may contribute to a SBC mechanism in
humans. Physiological cooling mechanisms that
influence blood supplying the brain include
convection, conduction and evaporation.
Previously, two main processes have been
described for how the physiological consequences
of yawning could alter brain temperature in
humans. First, yawning produces significant
changes in circulation, including acceleration
in heart rate [35] and elevation of
blood pressure [36]. More specifically,
powerful jaw stretching during yawning produces
increases in neck, head and facial blood flow
[37,38], and the deep inspiration during
yawning produces significant downward flow in
cerebrospinal fluid and an increase in blow flow
in the internal jugular vein [39].
Together, these processes may act like a
radiator removing hyperthermic blood from brain
while introducing cooler blood from the lungs
and extremities, thereby cooling cortical
surfaces through convection. Secondly, it is
hypothesized that yawning also provides a direct
heat exchange from deep inhalation of cooler
ambient air [14,15]. The air exchange
during yawning could cool venous blood draining
from the nasal and oral orifices into the
cavernous sinus, which surrounds the internal
carotid artery supplying blood to the rest of
the brain [10].
The discovery that the posterior wall of the
maxillary sinus serves as an origin for both
medial and lateral pterygoid muscle segments
[17] suggests yet another mechanism for
cerebral cooling by yawning in humans that has
not been previously described. Accordingly,
yawning would selectively reduce brain
temperature by ventilating the sinus system and
promoting the evaporation of sinus mucosa. In
addition, further cooling may result from
enhanced venous return through the interaction
of anatomical features closely linked with this
system. The pterygoid plexus, which is a network
of small veins within the lateral pterygoid
muscle, operates as a ''peripheral pump'',
aiding venous return by the pumping action of
the pterygoid muscle [40]. Likewise, the
emissary veins, which are believed to serve as a
radiator system for cooling the hominid brain
[41,42], connect the pterygoid plexus
with the cavernous sinus through the foramen
ovale and the foramen lacerum, and it has been
suggested that the powerful and extended
contraction of the lateral pteroigoids during
yawning acts to squeeze blood from this plexus
[43].
Conclusions
This newly described process adds to the
literature regarding the potential for SBC in
humans, though future research should be
conducted to confirm and quantify these actions.
The anatomical findings associated with the
paranasal sinuses in humans are consistent with
comparative research on SBC in other animals
(e.g., birds), and this system compliments
recent work showing that physiological changes
associated with yawning can have
thermoregulatory consequences. These findings
provide further support for the view that
excessive yawning may be a useful diagnostic
tool for identifying instances of
thermoregulatory dysfunction in humans
[19,27,44]. Lastly, this work not only
adds theoretical support to the possibility of
SBC in humans, but also suggests that yawning
may be an integral response facilitating this
process. Applications of this system include the
potential for it tobe efficaciously manipulated
in certain pathologic conditions.
