Yawning
and stretching predict brain temperature changes
in rats: support for the thermoregulatory
hypothesis
Melanie L. ShoupKnox, Andrew C. Gallup,
Gordon G. Gallup Jr. and Ewan C. McNay
Department of Psychology,
University at Albany, NY USA
Department of Biological
Sciences, Binghamton University, NY USA Center
for Neuroscience Research, University at Albany,
NY USA
Recent research suggests that yawning is an
adaptive behavior that functions to promote
brain thermoregulation among homeotherms.To
explore the relationship between brain
temperature and yawning we implanted
thermocoupled probes in the frontal cortex of
rats to measure brain temperature before, during
and after yawning.Temperature recordings
indicate thatyawns and stretches occurred during
increases in brain temperature, with brain
temperatures being restored to baseline
following the execution of each of these
behaviors. The circulatory changes that
accompany yawning and stretching may explain
some of the thermal similarities surrounding
these events.These results suggest that yawning
and stretching may serve to maintain brain
thermal homeostasis.
INTRODUCTION
Yawning has been documented in all five
classes of vertebrates, suggesting an ancient
phylogeny and an essential basic function
(Baenninger, 1987), yet the adaptive
significance of yawning has yet to be determined
(Provine, 2005), and is likely multifunctional
across species. A satisfying yawn involves
gaping of the mouth, eye closure and watering,
salivation, and is often accompanied by
stretching (Provine, 1986, 2005). Contrary to
popular opinion, yawning is not affected by
changes in blood oxygen or carbon dioxide
levels. Provine et al. (1987b) showed that
neither inhalation of heightened levels of
oxygen or carbon dioxide nor physical exercise
influenced yawning. Therefore, it seems that
yawning does not serve a respiratory function,
and that yawning and breathing are controlled by
separate mechanisms. Baenninger (1997) suggested
that yawning functions to stimulate or
facilitate cortical arousal during state change.
Consistent with this hypothesis, yawning occurs
in anticipation of important events and during
behavioral transitions or changes in activity
levels across vertebrate taxa. 'While this
account may explain the hedonic quality and
unprompted nature of yawning, the particular
physiological mechanism mediating such arousal
has not been identified. Matikainen and Elo
(2008) suggested that arousal could be
facilitated by muscular stimulation of the
oxygen sensing carotid body during a yawn, but
this hypothesis has not been tested.
Recent research suggests that yawning may
contribute to brain thermoregulation among
homeotherms (reviewed by Gallup, 2010). In
humans, medical and physiological literature
shows that conditions such as multiple
sclerosis, migraine headaches, epilepsy, stress
and anxiety, and schizophrenia are all linked
with thermoregulatory dysfunction and are often
associated with instances of atypical yawning
(Gallup and Gallup Jr., 2008; Gallup et al.,
2010). One clinical report shows excessive
yawning during periods of mild hyperthermia, and
body temperature is reduced below baseline
levels following yawning bouts (Gallup Jr. and
Gallup, 2010). Frequent yawning is symptomatic
of conditions that increase brain and/or core
temperature, such as central nervous system
damage (Krantz et al., 2004; Cattaneo et al.,
2006) and the use of selective serotonin
reuptake inhibitors (Chen and Lu, 2009). Other
drugs that increase brain temperature frequently
produce excessive yawning, while drugs that lead
to hypothermia inhibit yawning (Argiolas and
Melis, 1998). Likewise, dopamine D2 agonists
induce hypothermia at high doses, and this
corresponds with decreased yawning in rats
(Collins et al., 2007). Experimental research on
one bird species (Melopsittacus undulatus), has
shown that yawning occurs more frequently during
rising ambient temperatures (Gallup et al.,
2009), and is correlated with other
thermoregulatory behaviors such as panting and
wing venting (Gallup et al., 2010). Similarly,
an observational report of behavioral
thermoregulation in capuchins (Cebus capucinus)
has shown that yawning occurs more frequently in
high ambient temperatures (Campos and Fedigan,
2009). Consistent with these reports, Deputte
(1994) documented that yawning among macaques
(Macaca fascicularis) was positively correlated
with ambient temperature while outside, and that
rising temperatures correlated with an increase
in yawning frequency while animals were lying
down.
The homeothermic brain operates most
efficiently within a limited temperature range
and is regulated by mechanisms that maintain
optimal temperature during periods of
hyperthermia (Cabanac, 1993). In humans, brain
temperature averages approximately 37°C,
with circadian fluctuations of up to
±0.5°C (Landolt et al., 1995). Brain
temperature is primarily determined by metabolic
heat production, temperature of the blood
supply, and rate of blood flow. Physiological
cooling mechanisms affecting the blood supply to
the brain include convection, conduction, and
evaporation. Convection occurs after sweat,
mucosal, tear, or saliva evaporation cools
cutaneous and subcutaneous venus plexuses in the
oral, nasal, and paranasal cavities (Zenker and
Kubik, 1996), as well as in the ophthalmic veins
during hyperthermia (Caputa et al., 1978;
Dekiunder et al., 1991; Hirashita et al., 1992).
Intertwined venous and arterial rete structures
enable heat transfer from warm incoming blood to
cooled venous blood. Increased blood flow during
body stretching, neck and facial stretching, or
increased heart rate variability (Greco and
Baenninger, 1991; Guggisberg et al., 2007)
during yawning may further increase convective
brain cooling (Zajonc, 1985; Askenasy, 1989).
Heat dissipation through the upper airways
allows for additional evaporative cooling.
Introduction of cool air into the nasal cavity
can effectively lower brain surface temperature
(Harris et al., 2006), and during periods of
induced mild hyperthermia, nasal breathing
produces a rapid (0.1°C per minute) drop in
frontal lobe temperature of up to 0.8'C (Mariak
et al., 1999). During a yawn, deep inhalation
may similarly invoke evaporative cooling of the
venous blood draining from the nasal and oral
orifices into the cavernous sinus. This process
would effectively cool the area surrounding the
internal carotid artery, which supplies blood to
the rest of the brain. Nasal breathing (in the
absence of jaw closure) inhibits the incidence
of yawning in humans (Gallup and Gallup Jr.,
2007), suggesting that yawning may be suppressed
when the brain is sufficiently cooled by nasal
cavity airflow.
Taken together, these results suggest that
yawning may activate multiple mechanisms
involved in maintaining/reinstating brain
thermal homeostasis. According to this model,
spontaneous yawning is most likely to occur in
response to brain hyperthermia, promoting
thermal homeostasis by decreasing brain
temperature. Because yawning is often
accompanied by neck or arm stretching (Provine
et al., 1987a; Daquin et al., 2001; Provine,
2005), stretching may also occur in response to
increases in brain temperature independently of
yawning. The present study represents a
preliminary investigation of the relationship
between changes in brain temperature associated
with yawning and stretching events in rats
(Rattus norvegicus). An indwelling thermocoupled
probe was used to continuously record brain
temperature in the prelimbic cortex of awake,
freely moving rats before, during, and after
instances of spontaneous yawning and
stretching.
DISCUSSION
This is the first report of a systematic
association between yawning, stretching and
brain temperature. Increased brain temperature
occurred prior to, and was predictive of the
onset of yawning and / or stretching, while
decreases in brain temperature always followed
the execution of each of these behaviors.
The current study is an initial step in
exploring the thermal consequences of yawning
and stretching. Although we gathered data on 13
yawns, 14 stretches and 8 yawn-stretch
combinations there are limitations associated
with our relatively small sample of animals. As
a correlational study, it is possible that the
observed rise in brain temperature may not
trigger yawns or stretches per se, but instead
may be an inherent property of the yawn/stretch
process.
Pre-yawning and pre-stretching processes,
such as changes in blood flow or fluctuations in
hormones and/or neurotransmitters, may
contribute to the observed increase in brain
temperature. If so, these data would be
consistent with prior suggestions that yawning
and stretching are associated with arousal
during state change through increased blood flow
(Greco and Baenninger, 1991) to the cavernous
sinus surrounding the internal carotid artery
(Matikainen and Elo, 2008), which then supplies
cooled blood to cortical structures. Decreases
in brain temperature following a yawn may be the
physiological mechanism mediating cortical
arousal (Baenninger, 1997). Because we measured
brain temperature from a shallow cortical
structure, future research in this area should
gather either independent or simultaneous
measurements from deeper structures, including
the hypothalamus, which regulates body
temperature.
We feel confident that our findings are not
a result of movement artifacts during the act of
yawning or stretching. Guide cannulae were
secured in place by cranial screws and dental
cement Temperature changes of this steady,
systematic nature were not observed during
periods of activity other than yawning or
stretching. Furthermore, as shown in Figure 1,
the changes in temperature that portend the
occurrence of yawning/stretching occur well in
advance of the act itself, and the changes in
temperature that follow the act continue for
several minutes afterward.
Consistent with the thermoregulatory
hypothesis, our findings suggest that both
yawning and stretching may be responses to, or
symptoms of transient brain hyperthermia. These
behaviors may be acting either independently or
in tandem to counter intermittent increases in
brain temperature and promote thermal
homeostasis. Differences in the nature of these
behaviors, however, suggest that stretching may
facilitate more widespread cooling compared to
direct brain and head cooling associated with
yawning. Future studies could investigate this
by simultaneously measuring core body and brain
temperature during yawning and stretching. The
hypothesis that yawning acts to cool the brain
(Gallup and Gallup jr., 2007) is powerful
because it integrates much seemingly diverse
information about yawning from a variety of
species, and it can also be used to generate
testable predictions regarding the endogenous
and exogenous conditions that affect
yawning.
The association between yawning and sleep
can be further understood from a
thermoregulatory viewpoint. Length of sleep
varies inversely with body temperature, and
yawning frequently occurs before sleep onset in
the evening when brain temperature is at its
peak, and upon waking when brain temperature
begins increasing from its lowest point (Provine
et al., 1987a; Landolt et al., 1995). Prolonged
sleep deprivation in rats has been shown to
increase deep brain temperature (Everson et al.,
1994), and excessive yawning is symptomatic of
exhaustion/sleepiness. In humans, 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). Hot water consumption increases body
temperature as well as sleepiness, while ice
intake produces the converse (Krauchi et al.,
2006). Therefore, if variation in body
temperature is associated with corresponding
variation in sleepiness, our data may help
explain why people often yawn when they are
tired (Zilli et al., 2007). Unlike yawning,
however, stretching is more likely to occur in
the morning than the evening (Provine et al.,
1987a), perhaps to promote more widespread
arousal.
Given the ubiquitous nature of yawning, it
is likely multifunctional across species. One
potentially fruitful distinction for making
predictions about the function of yawning may
come from examination of the classification of
homeothermic (birds, mammals) versus
poikilothermic vertebrates (fish, amphibians,
reptiles). Thus far, research illustrating the
association between yawning and thermoregulation
has been limited to the study of homeotherms,
including experimental studies of birds, rats,
and humans, and observational reports on
non-human primates. Yawning may also play a role
in behavioral thermoregulation among
poikilotherms, however, the function of yawning
in these species may be fundamentally different.
Coupled with existing evidence supporting a
connection between yawning and changes in
internal and external temperatures, it is
possible that yawning may also be a method of
behavioral thermoregulation in a wide range of
other species. Among homeotherms, ecological
factors such as the need for water conservation
could affect the way yawning is used to
alleviate thermal stress, as has been suggested
for budgerigars (Gallup et al., 2009). There
could be differences in the function or
frequency of yawning between homeothermic
species adapted to unique thermal environments.
In addition, this report documents equally
strong temperature changes associated with
stretching and yawning in rats, yet previous
experimental studies in birds and rats have
failed to show a relationship between
thermoregulation and stretching (Gallup et al.,
2009, 2010). Much like yawning, however, further
research is needed to examine the impact of
stretching on behavioral thermoregulation across
species.
In closing, the present results suggest that
excessive yawning may be a useful diagnostic
tool for identifying instances of
thermoregulatorydysfunction in humans (Gallup
and Gallup Jr., 2008). Recent case studies have
shown methods of behavioral cooling to postpone
or eliminate symptoms of excessive yawning
(Gallup Jr. and Gallup, 2010), and at least one
report now highlights specific symptom relief
from yawning in patients suffering from abnormal
thermoregulation due to multiple sclerosis
(Gallup et al., 2010). Therefore, the
association between yawning and temperature
change deserves further attention in clinical
studies.
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