Over the past 5 years numerous reports have
confirmed and replicated the specific brain
cooling and thermal window predictions derived
from the thermoregulatory theory of yawning, and
no study has found evidence contrary to these
findings. Here we review the comparative
research supporting this model of yawning among
homeotherms, while highlighting a recent report
showing how the expression of contagious yawning
in humans is altered by seasonal climate
variation. The fact that yawning is constrained
to a thermal window of ambient temperature
provides unique and compelling support in favor
of this theory. Heretofore, no existing
alternative hypothesis of yawning can explain
these results, which have important implications
for understanding the potential functional role
of this behavior, both physiologically and
socially, in humans and other animals. In
discussion we stress the broader applications of
this work in clinical settings, and counter the
various criticisms of this theory.
Introduction
It was recently discovered that contagious
yawning frequency varies with seasonal climate
variation (Gallup and Eldakar, 2011).
Pedestrians in Tucson, Arizona, an arid desert
climate in the Western United States, completed
a survey in which they viewed a series of
yawning photos and answered questions about
their own yawning behavior while doing so. Two
independent samples of participants were
collected, one during the early summer when
temperatures averaged 37°C (equivalent to
human body temperature) and the other during the
winter when temperatures averaged 22°C
(equivalent to room temperature). Results showed
that pedestrians in the winter condition were
nearly twice as likely to yawn during the survey
and that even when accounting for variables such
as the amount of sleep the night before,
duration of time spent outside prior to being
surveyed, and relative humidity, ambient
temperature was the only significant predictor
of yawns. Specifically, participants were more
likely to yawn contagiously at lower ambient
temperatures across both seasonal conditions.
Furthermore, the proportion of individuals
yawning in the summer quickly dropped as the
length of time spent outside increased,
suggesting that yawns were suppressed following
an initial acclimation to sudden temperature
changes.
Although these results may seem unexpected,
they match the specific predictions of the
thermoregulatory theory that were initially
proposed over 5 years ago (Gallup and Gallup,
2007). Since then, a growing body of both
descriptive and experimental research has
demonstrated a clear and consistent association
between yawning and brain thermoregulation in
homeotherms (Gallup, 2010). Alongside the
repeated demonstration of predicted brain
temperature fluctuations surrounding yawning in
rats (Rattus norvegicus) (Shoup-Knox et al.,
2010; Shoup-Knox, 2011), a fundamental principle
of this theory concerns the specific predictions
associated with yawning frequency and ambient
temperature variation (i.e., the thermal window
hypothesis), which directly follow models of
body temperature regulation among homeotherms
(e.g., Scholander et al., 1950). Research on
humans, non-human primates, rats and birds shows
that yawning frequency is altered by
fluctuations in ambient temperature (Campos and
Fedigan, 2009: Cebus capucinus; Deputte, 1994:
Macaca fascicularis; Gallup et al., 2009, 2010b:
Melopsittacus undulatus; Gallup et al., 2011:
Rattus norvegicus; Gallup and Eldakar, 2011:
Homo sapiens), and in all cases the specific
correlation between temperature and behavior
remains consistent with the thermoregulatory
theory. Following an overview of this theory, we
briefly outline the clinical and medical
literature revealing a strong association
between abnormal yawning and thermoregulatory
dysfunction in humans (Gallup and Gallup, 2008;
Ghanizadeh, 2011). Lastly, we address the
attempts to dismiss or undermine the empirical
support of this theory (Elo, 2010, 2011;
Guggisberg et al., 2010, 2011; Walusinski, in
press) and show how they have remained
untenable.
The brain cooling hypothesis
The fact that yawning is elicited by
numerous stimuli has contributed to the lack of
consensus regarding its function (Miller et al.,
2012a), and new hypotheses for yawning continue
to emerge (e.g., Thompson Cortisol Hypothesis,
Thompson and Bishop, 2012). Perhaps the most
common belief is that yawning functions to
increase oxygen levels in the blood. However,
Provine et al. (1987) disproved this hypothesis
by showing that breathing heightened levels of
oxygen or carbon dioxide did not influence
yawning, although it did increase breathing
rates. They also demonstrated that physical
exercise sufficient to double breathing rates
had no effect on yawning. Therefore, contrary to
popular belief, yawning does not serve a
respiratory function and is controlled by a
separate mechanism from breathing.
A vast amount of literature suggests that
yawns function to stimulate or facilitate
arousal during state change (Baenninger, 1997;
also see state change hypothesis: Provine, 1986,
1996, 2005). Although there is conflicting
evidence from studies measuring an arousal
response accompanying yawning (e.g., Laing and
Ogilvie, 1988; Regehr et al., 1992; Sato-Suzuki
et al., 1998; Kita et al., 2000; Kasuya et al.,
2005; Guggisberg et al., 2007), across
vertebrate taxa yawning occurs in anticipation
of important events and during behavioral
transitions. Further research shows that yawning
precedes modified activity levels in humans and
non-human primates (Baenninger et al., 1996;
Giganti et al., 2002; Vick and Paukner, 2009:
Pantroglodytes). Evidence from endocrine,
neuotransmitter, and pharmacological mechanisms
also supports the view that yawning is an
important mediator of behavioral arousal levels
(Baenninger, 1997). Accordingly, it has been
proposed that yawning functions to modify levels
of cortical arousal during variable
environments. Branching from this theory, it has
recently been postulated that it is the effect
of yawning on brain thermoregulation that
produces these adaptive benefits of arousal and
mental efficiency (Gallup, 2010; Gallup et al.,
2011).
The thermoregulatory theory was initially
developed on the view that the physiological
consequences of a yawn could provide the
necessary components needed for effective brain
cooling in homeotherms (Gallup and Gallup,
2007). Specifically, it proposed that yawning
functions as a compensatory cooling mechanism.
These predictions have since been echoed in
continued research investigating the
physiological consequences of yawning in humans
(Shoup-Knox, 2011; Corey et al., 2012).
Consistent with this theory, pharmacological
research demonstrates that yawning is under the
control of the hypothalamus (Argiolas and Melis,
1998), a brain structure strongly linked to
thermoregulation (Cooper, 2002).
Mechanisms of thermoregulation and how
yawning cools the brain
Brain temperature of homeotherms is
determined by three variables: the temperature
of arterial blood flow, the rate of this blood
flow, and the metabolic heat production (Baker,
1982). The localized circulatory changes
accompanying yawning alter these first two
variables. Physiological cooling mechanisms that
influence blood supplying the brain include
convective heat transfer, thermal conduction,
and evaporative heat loss. To date, three main
processes have been described for how yawning
could cool brain temperature in mammals and
birds. Below we apply them specifically to
humans.
First, yawning produces significant changes
in circulation, including acceleration in heart
rate (Heusner, 1946) and elevation of blood
pressure (Askenasy and Askenasy, 1996). More
specifically, powerful jaw stretching during
yawning produces increases in neck, head, and
facial blood flow (Zajonc, 1985; Askenasy,
1989), and the deep inspiration during yawning
produces significant downward flow in
cerebrospinal fluid and an increase in blow flow
in the internal jugular vein (Schroth and Klose,
1992). The network of veins within the lateral
pterygoid muscle has been described to operate
as a peripheral pump, and the powerful and
extended contraction of these muscles during
yawning acts to squeeze blood from the
associated plexus (Bhangoo, 1974). Brain
temperature is consistently 0.2°C higher
than that of arterial blood supplying the brain
(Kiyatkin et al., 2002), and that on average,
0.66J of heat energy per minute per gram is
released from the brain through blood flow
(Yablonskiy et al., 2000). As a result, the
aforementioned processes during yawning act like
a radiator by removing hyperthermic blood from
brain and simultaneously 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 the
deep inhalation of cooler ambient air (Gallup et
al., 2009). The air exchange during yawning
would 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 (Zenker
and Kubik, 1996). Again, this would provide a
cooling effect through convection. Furthermore,
it has recently been discovered that pharyngeal
cooling rapidly and selectively decreases brain
temperature in primates, and tympanic
temperature in humans, by cooling the carotid
arteries (Takeda et al., 2012).
Third, it has recently been discovered that
the posterior wall of the maxillary sinus serves
as an origin for both medial and lateral
pterygoid muscle segments (Koritzer and Hack,
2002), which allows the thin sinus walls to flex
when the pterygoid musculature contracts during
jaw activity such as yawning. This powerful
flexing of the sinus walls has been proposed to
ventilate the human sinus system similar to that
described in birds (Sedlmayr and Witmer, 2001),
providing yet another mechanism for cerebral
cooling by yawning in humans. Accordingly,
yawning could reduce brain temperature by
ventilating the sinus system and promoting the
evaporation of the sinus mucosa (Gallup and
Hack, 2011).
The inhibition of yawning following nasal
breathing and forehead cooling
The first empirical support for the brain
cooling model came over 5 years ago when Gallup
and Gallup (2007) discovered that contagious
yawning can be modulated by different breathing
and forehead temperature manipulations in
humans. It has been well documented that
behaviors such as nasal breathing and forehead
cooling effectively result in brain temperature
reductions (Mariak et al., 1999; Harris et al.,
2007; Zenker and Kubik, 1996), and when
presented with a contagious yawning stimulus,
participants performing these behaviors showed a
reduced tendency to yawn. Thus, it was proposed
that cerebral cooling from these conditions
inhibited the mechanisms that normally trigger
contagious yawning. Consistent with this
interpretation, mechanical introduction of cool
air into the nasal cavity can lower brain
surface temperature (Harris et al., 2007), and
further research using intracranial
thermocouples demonstrated that nasal inhalation
can produce rapid reductions (0.1°C/min) in
frontal lobe brain temperature as well (Mariak
et al., 1999). Likewise, forehead cooling
reduces the temperature of the blood in
cutaneous and subcutaneous venous plexuses,
which is then transported through venous
communications into the venous plexuses of the
dura mater (Zenker and Kubik, 1996). Forehead
cooling also enhances dissipation of heat from
the skull, and the cooling of venous blood by
the skin can in turn cool the carotid arterial
blood supply to the brain through convective
heat transfer. More recently, these same methods
of brain cooling (i.e., nasal breathing and
forehead cooling) have been shown to either
prevent or delay bouts of excessive yawning in
patients suffering from thermoregulatory
dysfunction (Gallup and Gallup, 2010).
Predicted fluctuations in brain and oral
temperature surround yawning events in rats and
humans
The fundamental predictions of the
thermoregulatory theory are that yawning should
(1) be triggered by brain hyperthermia, and (2)
produce a measureable cooling effect (Table
?(Table1).1). To explicitly investigate the
relationship between yawning and brain
temperature, Shoup-Knox et al. (2010) took
continuous measures of prelimbic brain
temperature in rats using thermocoupled
temperature probes and paired these recordings
to confirmed yawning events. Consistent with
these predictions, yawning was triggered in
response to rapid increases in brain temperature
(0.11°C), and followed by equivalent
decreases in temperature immediately thereafter.
Furthermore, all increases in brain temperature
during this study of ³0.1°C corresponded to
yawning and stretching behavior, and all rapid
decreases in temperature of ³0.5°C occurred
during the first minute following yawns only.
Table 1 Table 1 Empirical tests of the brain
cooling hypothesis.
Shoup-Knox (2011) further strengthened this
relationship by measuring temperature changes in
both the prelimbic cortex and preoptic area of
the hypothalamus of rats before and after yawns.
Temperature recordings from the prelimbic cortex
replicated the relationship from previous
findings (Shoup-Knox et al., 2010). However, the
temperature relationship in the preoptic area
differed slightly. In particular, cooling
following yawns was delayed in the preoptic area
in comparison to the prelimbic cortex, and there
was no increase in temperature in the preoptic
area prior to yawns. Therefore, while both
internal and external brain tissues cooled after
yawns, only the cortex showed an increase in
temperature leading up to this response.
Predicted temperature fluctuations have also
been confirmed using non-invasive temperature
measures in humans. Gallup and Gallup (2010)
described two case studies of women suffering
from chronic bouts of yawning, in which one
could anticipate the onset of these bouts and
record her oral temperature before and after
each episode. Both patients complained of
unpredictable and uncontrolled yawning attacks
that lasted up to 45 min in length, occurring
between one to fifteen times per day. These
episodes involved repeated deep and overwhelming
yawns that caused their eyes to water and their
nose to run. Each yawn consisted of powerful
jaw, neck, and body stretching, and time spent
in between yawns included deep inhalations. Both
women also reported feeling cold during or after
each bout of excessive yawning, and often
experienced goose bumps and shivering as a
consequence. The woman who took oral temperature
recordings reported the onset of each bout
occurring during mild hyperthermia
(37.5°C), and that there was an average
decrease in temperature of 0.4°C
immediately following each episode (Gallup and
Gallup, 2010).
Thermal window hypothesis
Homeothermic species preserve a relatively
constant body temperature as ambient temperature
fluctuates, using a combination of autonomic and
behavioral mechanisms controlled by the central
nervous system (Bicego et al., 2007). According
to the thermoregulatory theory, the mechanisms
triggering yawning should also be controlled by
ambient temperature variation (Gallup and
Gallup, 2007, 2008). The predictions derived
from this theory, also known as the thermal
window hypothesis, follow other behavioral
models of temperature regulation among
homeotherms (Scholander et al., 1950).
Therefore, yawning should be influenced by both
the direction and range of ambient
temperature.
The thermal window hypothesis has three
primary predictions (Table2). First, yawns
should increase in frequency with initial rises
in ambient temperature. As ambient temperatures
rise, so do temperatures in the brain
(Shoup-Knox, 2011) stimulating thermoregulatory
mechanisms to control temperatures within a
normal range. Second, yawns should decrease as
ambient temperatures draw near or exceed body
temperature. Since the temperature of the
ambient air gives a yawn its cooling utility,
yawning at ambient temperatures above body
temperature would be counter productive, and
thus more effective evaporative cooling
mechanisms (e.g., sweating, panting) should be
triggered during extreme heat stress. A third
prediction states that yawning should diminish
when temperatures fall below a certain point,
because countercurrent heat exchange could
potentially cool the brain below optimal
homeostasis. The specific tests of the first two
predictions are outlined below, while the third
and final prediction has yet to be formally
investigated.
The thermal window hypothesis was first
tested in budgerigars, an arid zone parrot.
Gallup et al. (2009) measured yawning and other
thermoregulatory behaviors in three distinct
temperature conditions: control (22°C), an
increasing range (22&endash;34°C), and a
high range (34&endash;38°C). Consistent
with the theory, yawning was indeed more
frequent during the increasing range, but began
to decrease in frequency at the high temperature
range when evaporative cooling mechanisms became
more frequent (i.e., panting). These results
directly match Scholander et al.'s (1950) model
of temperature regulation among avian species.
Their model assumes that birds expend the least
amount of energy on temperature regulation in
the thermoneutral zone, which is the ambient
temperature range where respiration rates do not
change with temperature. Within this zone, heat
loss is generated with little direct energy
expenditure, typically through varying rates of
venous blood flow or by altering body posture.
Therefore, yawns could provide a metabolically
inexpensive means for cooling through
countercurrent heat exchange and by increasing
cerebral blood flow. Outside of this zone,
however, temperature regulation requires
increases in metabolism through shivering or
panting. For instance when ambient temperature
rises above the upper critical temperature, more
effective evaporative heat loss mechanisms are
increased (Scholander et al., 1950), while other
mechanisms are progressively reduced (i.e.,
yawning). Importantly, follow-up experiments in
budgerigars and rats show that yawning is
sensitive to both temperature range and
direction of change, and not merely elicited by
any change (see Gallup et al., 2010b, 2011 for
results and detailed discussion).
In the most recent test of this hypothesis,
which spurred this review, Gallup and Eldakar
(2011) demonstrated that contagious yawning
frequency in humans was sensitive to ambient
temperatures accompanying seasonal climate
variation. Explicitly testing the second
prediction of the thermal window hypothesis,
i.e., that yawning should decrease when ambient
temperatures draw near or exceed body
temperature, pedestrians were significantly less
likely to yawn in response to viewing images of
people yawning at especially hot temperatures
(37°C&emdash;human body temperature).
However, when ambient temperatures were cooler
during the winter condition (22°C),
pedestrians yawned at the same rate found in
laboratory studies at room temperature (Platek
et al., 2003). Ambient temperature was the sole
predictor of this difference across conditions,
while increasing time spent outside further
reduced contagious yawning in the summer heat.
For instance, individuals who yawned during in
the summer reported being outside for less than
5 min, while the average time spent outside of
those who did not yawn was over 19 min.
Evidence and applications
of the thermoregulatory theory in medicine and
clinical research
Sleep, yawning, and
thermoregulation
It is well documented in humans that yawning
occurs most often before sleep onset and after
waking (Provine et al., 1987), and similar
circadian effects have been demonstrated in
laboratory rats (Anias et al., 1984). Sleep and
body temperature vary inversely (Gilbert et al.,
2004), and in humans yawning frequently occurs
in the evening, when brain temperature is at its
peak, and upon waking, when brain temperature
begins increasing from its lowest point (Landolt
et al., 1995). By lowering brain temperature and
maintaining thermal homeostasis, the
thermoregulatory theory suggests that instead of
prompting sleep, yawning actually serves to
maintain focus and attention, thereby
antagonizing sleep.
Consistent with the thermoregulatory theory,
circadian modulation of body temperature alters
sleep propensity in humans (Kumar, 2004).
Subjective ratings of sleepiness correlate with
increases in skin temperature while lying down
(Krauchi et al., 1997) and with increases in
core body temperature when standing (Krauchi et
al., 2005). In addition, hot water consumption
increases body temperature as well as
sleepiness, while ice intake produces the
opposite effect (Krauchi et al., 2006).
Furthermore, prolonged sleep deprivation in rats
increases deep brain temperature (Everson et
al., 1994). Thus, as with yawning, variation in
body temperature is associated with
corresponding variation in sleepiness and
sleep-related fatigue. This research clears up
some misconceptions regarding cases of frequent
or excessive yawning, and thus has the potential
to provide critical insight to sleep
medicine.
Abnormal yawning and thermoregulatory
dysfunction
Despite the close association between
yawning, sleep, and thermoregulation, excessive
yawning is not always indicative of sleep
deprivation or sleep disorder and may in fact be
an important symptom of an individual's
inability to properly maintain thermal
homeostasis (Gallup and Gallup, 2008, 2009a,b;
Gallup, 2009). Conditions such as multiple
sclerosis, migraine headaches, epilepsy, stress
and anxiety, and schizophrenia have all been
linked to thermoregulatory dysfunction and are
often associated with instances of atypical
yawning. Excessive yawning is also symptomatic
of conditions that increase brain and/or core
temperature, such as central nervous system
damage, sleep deprivation, and specific
serotonin reuptake inhibitors. Conversely, drugs
and conditions that produce hypothermia or
decreases in temperature suppress yawning. How
thermoregulatory changes influence yawning in
humans: medical conditions, drug use and
behavior (modified from Gallup and Gallup,
2008).
It has therefore been suggested that
physicians could use excessive yawning as a
diagnostic tool for identifying instances of
abnormal thermoregulation (Gallup and Gallup,
2008). Not only is excessive yawning indicative
of thermoregulatory dysfunction (Gallup and
Gallup, 2010), but yawns can also provide
symptom relief in patients suffering from
conditions such as multiple sclerosis similar to
deliberate behavioral cooling methods (Gallup et
al., 2010a). For instance, cooling of the head
and neck has been shown to alleviate multiple
sclerosis symptoms (Ku et al., 1999) and
diminish yawning (Gallup and Gallup, 2007,
2010), supporting the view that yawns provide a
temporary brain cooling effect in these
patients. Together, this evidence supports the
view that frequent yawning associated with
various conditions and medications is an
adaptive response to counter intermittent brain
temperature rises.
Propranolol in yawning prophylaxis: a
case report
Aside from the previously described
behavioral cooling methods of nasal breathing
and forehead cooling (Gallup and Gallup, 2007,
2010), there has been no evidenced-based
treatment for excessive yawning. Recently,
however, Ghanizadeh (2011) describes a
compelling case study of how the use of
propranolol repeatedly extinguished extended
periods of frequent yawning in a middle-aged
male. Propranolol is a non-selective
beta-blocker used to treat hypertension and
anxiety, and one side effect is thermoregulatory
cooling (e.g., Brittain and Handley, 1967;
McSorley and Warren, 1978; Meythaler and
Stinson, 1994; Soszynski et al., 1996). For
instance, propranolol has been shown to reduce
centrally mediated hyperthermia in humans
following traumatic brain injury (Meythaler and
Stinson, 1994) and prevent increases in body
temperature triggered by psychological stress
(Soszynski et al., 1996). The above-mentioned
evidence supports the view that propranolol
reduces yawning frequency through its brain
cooling effects (Ghanizadeh, 2011). Research of
this nature deserves further attention in
clinical studies.
Yawning and fever
Another testable, and perhaps
counterintuitive, implication of the
thermoregulatory theory is that yawning should
diminish during pyrexia, or fever. As described
by Gallup and Gallup (2008, p. 12):
An elevation of body temperature can occur
either due to thermoregulatory failure
(hyperthermia), or from intact homeostatic
responses such as fever (Simon, 2007). It is
well-established that fever is an adaptive host
defense mechanism and an essential defensive
response to infection by pathogens (Soszynski,
2003). Consistent with this notion Mariak et al.
(1998) found that brain temperature during fever
is not selectively suppressed by any specific
thermolytic mechanisms, and research has shown
that attempts to treat fever can have harmful
effects on critically ill patients, leading to
an increase in mortality (Kluger et al., 1996;
Schulman et al., 2005). Therefore, the
mechanisms that trigger an increase in the
thermoregulatory set point (fever) in the
hypothalamus may, as a testable implication of
our model, override or turn off normal operating
thermal mechanisms such as yawning (also in the
hypothalamus) to fight the infection.
Additional features and
predictions of the thermoregulatory
theory
Yawning and boredom
Yawning is often interpreted as an
indication of boredom, lack of interest, and
sleepiness, and some have even hypothesized that
yawning is simply an expression of boredom,
unconcern, or indifference (Barbizet, 1958;
Baenninger and Greco, 1991). As described by
Shoup-Knox (2011), the thermoregulatory
hypothesis would alternatively suggest that
yawning is a symptom of one of several factors
influencing brain temperature, including
insufficient blood flow, time of day, and high
rates of metabolic heat production. It is
therefore predicted that similar to the
experience of feeling tired (see above), boredom
would also be accompanied by rises in brain
temperature.
Contagious yawning
Due to its contagious nature in a few
species of mammals and birds (recently reviewed
by Miller et al., 2012b), yawning may also have
a more derived social role in some group-living
vertebrates. Research on contagious yawning in
humans has focused on understanding how
individual social characteristics or cognitive
development influences its release (e.g.,
Anderson and Meno, 2003; Platek et al., 2003;
Senju et al., 2007; Millen and Anderson, 2010),
and a popular view is that contagious yawning is
related to empathy. For instance, it was
recently observed that humans are more likely to
yawn contagiously when they witness kin and
friends yawn, in comparison to acquaintances or
strangers (Norscia and Palagi, 2011). Since
contagion is disrupted by thermal influences
(Gallup and Gallup, 2007; Gallup and Eldakar,
2011), however, it is proposed that any derived
function of contagious yawning is tied to
cognitive processing since hyperthermia impairs
cognitive functioning (e.g., Racinais et al.,
2008).
Considering that yawning is triggered during
low states of vigilance (Guggisberg et al.,
2007) and produces changes in localized
circulation (Zajonc, 1985; Askenasy, 1989), the
spreading of this behavior to nearby
conspecifics has been proposed to enhance group
vigilance (Gallup and Gallup, 2007). Recent
evidence suggests that budgerigars both yawn and
stretch contagiously (Miller et al., 2012b) and
that the social transmission of these behaviors
is enhanced following environmental threats
(e.g., auditory disturbances) (Miller et al.,
2012a). Consistent with the view that contagious
yawning evolved to coordinate arousal, which in
turn would improve vigilance within the group,
the close behavioral coupling of yawning and
stretching among flock-mates may function in the
collective detection of, and response to, local
disturbances or threats.
Critiques of the
thermoregulatory theory
Despite overwhelming empirical evidence
supporting the thermoregulatory theory, some
individuals remain skeptical. While theories
benefit from criticism and scrutiny that drive
more rigorous scientific investigation,
unfounded criticisms can hinder progress and
delay future applications. Here we address the
critiques of the thermoregulation theory of
yawning, showing that they remain
untenable.
Yawning cannot cause significant
decreases in temperature (Elo, 2010,
2011)
Elo (2010, 2011) has repeatedly argued that
yawning cannot cause significant decreases in
temperature in the absence of sweating. This
conclusion, however, is based solely on
calculations referring to changes in the overall
body temperature in humans, and not to more
localized changes in the specific areas relevant
to yawning (i.e., the neck, face, and head). In
the case report under scrutiny (Gallup and
Gallup, 2008), two patients reported excessive
yawning attacks lasting upwards of 45 min in
length and immediately following these bouts it
was observed that oral body temperatures
significantly decreased. During these attacks
each yawn consisted of powerful jaw, neck, and
body stretching, and time spent in between yawns
included deep inhalations. Therefore, the
associated respiratory and cardiovascular
changes accompanying excessive yawning in these
patients could easily contribute to cooling of
the skull in the absence of perspiration (see
Gallup, 2011a).
Contrary to Elo's position, the
thermoregulatory theory has outlined well
documented and theoretically founded mechanisms
for which the physiological consequences of
yawning could produce selective brain cooling
(see above). Elo's position is also inconsistent
with research directly investigating the
relationship between yawning and brain
temperature changes in rats (Shoup-Knox et al.,
2010; Shoup-Knox, 2011). In particular, the
aforementioned reports on rats have shown that
isolated yawns produced significant localized
brain cooling in the prelimbic cortex and
preoptic area of the hypothalamus (Shoup-Knox et
al., 2010; Shoup-Knox, 2011). Therefore, the
conclusions of Elo (2010, 2011) are
invalid.
The association between yawning and
temperature can be explained by other factors
(Guggisberg et al., 2010)
In a recent review, Guggisberg et al. (2010)
concluded that the association between yawning
and temperature was not causal and could be
explained by other factors. They attempt to
discredit the results of Gallup and Gallup
(2007), which showed that methods of behavioral
brain cooling (i.e., nasal breathing and
forehead cooling) diminish yawning, by arguing
that it is impossible to differentiate the
effects of temperature and sleepiness (i.e.,
warmer forehead packs may increase yawning
because participants may become sleepy). This
argument, however, does not take into account
that nasal breathing does not affect sleepiness,
and that none of the participants yawned in
response to contagious stimuli when inhaling and
exhaling through their nose. Therefore, the
temperature/sleep confound described by
Guggisberg et al. (2010) is untenable.
Guggisberg et al. (2010) also suggest that
the association between yawning and rising
ambient temperatures reported by Gallup et al.
(2009) may be related to rapidly changing vs.
stable temperatures, or due to uncontrolled
factors such as differences in drowsiness. It
has since been shown, however, that yawning is
sensitive to both temperature range and
direction of change, and not merely elicited by
any change (Gallup et al., 2010b, 2011). For
instance, yawning in rats is triggered by
deviations in thermal homeostasis, and not
simply unstable temperatures. In addition,
according to Guggisberg et al. (2010) the
association between warm temperature and sleep
would predict that yawning should be more
frequent when ambient temperatures are held high
since this would produce an increase in
drowsiness or fatigue. However, these
expectations run contrary to the thermal window
hypothesis, as well as the evidence. Both
experimental and descriptive research shows that
yawning is significantly reduced at high
temperatures, and that this is not an artifact
of increased sleep or rest (Gallup et al., 2009,
2011; Gallup and Eldakar, 2011).
The thermoregulatory theory does not
demonstrate any yawn-induced effects (Guggisberg
et al., 2011)
According to Guggisberg et al. (2011),
contagion is the only effect that is induced by
yawning. These authors state that physiological
explanations of yawning fail to show a
yawn-induced effect, which is argued to support
their notion that the "origin and function" of
yawning is social (Guggisberg et al., 2010). On
the contrary, however, yawn-induced cooling
effects have been documented and are outlined
throughout this review (Table ?(Table1).1). In
addition, Corey et al. (2012) has more recently
provided clear evidence of yawn-induced effects
on a number of aspects of human physiology.
Furthermore, the results from Gallup and
Eldakar (2011), as well as Gallup and Gallup
(2007), challenge the social/communication
hypothesis as an explanation for the origin of
yawning. Contagious yawning was the dependent
variable in both of these studies and was
significantly, and independently, inhibited by
extreme ambient temperatures and methods of
behavioral brain cooling. Therefore, counter to
the position of Guggisberg et al. (2010, 2011),
yawn-induced contagion effects appear to be at
least partially mediated by underlying
thermoregulatory physiology.
Importantly, neither social contagion nor
thermal effects can deny the other. It has been
shown that you can change sensitivity to
contagion, but it may also be possible to lose a
bit of thermoregulatory control under strongly
contagious situations. It is critical, however,
that any hypothesis on yawning can take into
account the existing empirical literature. The
social/communication hypothesis fails explain
how the "communication" purportedly involved in
yawning somehow breaks down at high ambient
temperatures or when individuals breathe through
their nose.
The delay in brain cooling following a
yawn is too long (Guggisberg et al.,
2011)
In discussion of the brain cooling effects
in rats following yawning and stretching
(Shoup-Knox et al., 2010), Guggisberg et al.
(2011) argue that even when considering the time
for venous blood drain and thermal convection to
occur, the delay observed before brain
temperature began to fall is too large to be
explained by yawning. In particular, they state,
"The thermometer seems to have been placed close
to the dura and therefore should have rapidly
captured a blood flow induced temperature
change" (p. 1303). This argument ignores the
fact that yawning occurred during rapid
increases in brain temperature (~0.1°C). It
is simply unreasonable to suggest that there
should not be a slight delay in cooling via
increases in blood flow. Not only would there be
a delay in reducing a stable temperature, but
this would be even greater when counteracting
already rising temperatures. Furthermore, the
mechanisms of counter-current heat exchange and
evaporative effects are not discussed and would
require a certain delay before reducing brain
temperature. Guggisberg et al. (2011, p. 1303)
also state, "… the brain continued to warm
up with the same speed as before until
~20&endash;40 s after the yawns and stretches of
the observed rats." This is simply not an
accurate depiction. Shoup-Knox et al. (2010)
actually showed that prelimbic temperatures
began to decrease at an average of 18 s
following each isolated yawn, while
stretch-induced decreases in prelimbic
temperature took 38 s (over twice as long).
Furthermore, the rate of increase did in fact
slow during this transition. The position of
Guggisberg et al. (2011) also fails to account
for the discrepancy in cooling effects between
yawning and stretching, while the
thermoregulatory theory clearly explains this.
In short, the argument by Guggisberg et al.
(2011) is untenable.
The thermoregulatory theory overlooks the
existence of fetal yawning (Walusinski,
in press)
In a review of the theories on the function
of yawning, Walusinski (in press) states the
thermoregulatory theory has "overlooked" the
existence of fetal yawning. Consistent with the
view that yawning is phylogenetically old, the
onset of this behavior occurs quite early in
uterine development (11 weeks gestation in
humans) (de Vries et al., 1982). Counter to the
views of Walusinski (in press), however, this
evidence has indeed been taken into account
within the framework of the thermoregulatory
model (see Gallup et al., 2009). According to
the argument presented by Walusinski (in press),
any behaviors that occur in utero should serve
identical functions following birth. Thus,
because the mother controls thermoregulation of
the fetus, Walusinski believes that brain
cooling cannot be the function of yawning
thereafter. Contrary to this view, however, many
important postnatal behaviors begin to appear
prenatally (e.g., breathing movements,
swallowing and eye movements) before they
develop their externally intended functional
significance (Nijhuis, 2003). In other words,
any functions that prenatal behaviors may have
are not necessarily going to match the
function(s) to these behaviors following birth.
Therefore, the existence of fetal yawning
neither supports nor opposes the
thermoregulatory theory.
Walusinski (in press) also argues that the
thermoregulatory theory could not provide an
accurate explaination for yawning in homeotherms
because it "overlooks" yawning in poikilotherms
(i.e., cold-blooded animals). According to this
position, he believes there should be a single
function to yawning across all vertebrate
species. In other words, if poikilotherms such
as fish, amphibians, and reptiles yawn, and this
is presumably unrelated to maintaining optimal
brain temperature, then this behavior should not
function in brain thermoregulation among
homeotherms either. There are four primary
weaknesses in this argument.
First, the discussion of brain cooling in
relation to poikilotherms has been mentioned in
papers related to the thermoregulatory model
(e.g., Gallup et al., 2010b, 2011), and in fact
is has been suggested that yawning could play a
role in behavioral thermoregulation in these
species as well (Gallup et al., 2010b). Yawning
is behavioral mechanism of cooling and
poikilotherms are particularly dependent on
behavioral cooling. Furthermore, many
poikilotherms experience the problem of
trade-offs in heating, i.e., they benefit from
warmer temperatures for digestion but such
sustained temperatures may be too high for
neural tissue. Exactly what and how yawning
cools would depend on the morphology of the
brain or areas particularly sensitive to
overheating in each species. To our knowledge,
no good comparative studies have been
performed.
Second, it is important to point out that
poikilotherms may not even yawn in the same way
that birds and mammals do (see Rasa, 1971;
Dullemeijer and Povel, 1972, for explanations of
this action pattern in fish and snakes).
Baenninger (1987) argues that although
amphibians and reptiles open their mouth widely
on occasion, this does not necessarily represent
yawning.
Third, even if poikilothermic animals do
yawn like homeotherms, and yawning were to serve
disparate functions from thermoregulation in
these species, this does not remove the
possibility that yawning has derived
thermoregulatory functions in birds and mammals
(discussed in Gallup, 2011a,b,c). This type of
argument would be similar to positing that since
poikilotherms do not yawn contagiously that we
should not expect contagion to be present in
homeotherms either, yet we certainly do.
Evolution is a cumulative process, which has
additive effects on traits over time. Thus it is
entirely possible that following the evolution
of homeothermy, yawning developed brain
temperature consequences in birds and mammals
(outlined above), which could have then altered
selection of this behavior via pressures of
thermoregulation in unstable environments.
Fourth, yawning is elicited by numerous
stimuli and it has already been suggested that
yawning probably serves multiple functions
across vertebrates (Gallup, 2011b). As already
mentioned, one clear example of this is the
distinction between spontaneous and contagious
yawning. Therefore, the mere presence or absence
of yawning in poikilotherms can neither be used
as support for nor against the thermoregulatory
theory. Rather, a more thorough investigation of
yawning in poikilotherms is needed.
Conclusions
Unlike many hypotheses on yawning, the
thermoregulatory theory has stood up to rigorous
testing as well as various critiques. Not only
do predicted brain and localized body
temperature fluctuations surround yawning
events, but yawns are also triggered or
inhibited by environmental factors such as
ambient temperature manipulation and medical
conditions and drugs/medications that directly
affect thermoregulation. When the above evidence
is taken together (Table ?(Table4),4), the most
parsimonious explanation is that yawning is a
thermoregulatory mechanism in homeotherms. This
evidence has important applications for the
current understanding of yawning in medicine and
clinical research, and attempts to diminish the
significance of this theory could have
detrimental effects in delaying treatments and
diffusing both basic and practical knowledge. To
date, no other theory can explain why contagious
yawning in humans would vary with seasonal
temperature ranges.
