Yawning appears to be involved in arousal,
state change, and activity across vertebrates.
Recent research suggests that yawning may
support effective changes in mental state or
vigilance through cerebral cooling. To further
investigate the relationship between yawning,
state change, and thermoregulation, 12
Sprague&endash;Dawley rats (Rattus norvegicus)
were exposed to a total of 2 h of ambient
temperature manipulation over a period of 48 h.
Using a repeated measures design, each rat
experienced a range of increasing (22 C fi 32
C), decreasing (32 C fi 22 C), and constant
temperatures (22C; 32C).
Yawning and locomotor activity occurred most
frequently during initial changes in
temperature, irrespective of direction, compared
to more extended periods of temperature
manipulation. The rate of yawning also
diminished during constant high temperatures (32
C) compared to low temperatures (22 C). Unlike
yawning, however, stretching was unaffected by
ambient temperature variation. These findings
are compared to recent work on budgerigars
(Melopsittacus undulatus), and the ecological
selective pressures for yawning in challenging
thermal environments are discussed. The results
support previous comparative research connecting
yawning with arousal and state change, and
contribute to refining the predictions of the
thermoregulatory hypothesis across
vertebrates
Introduction
Phylogenetically old, yawning or yawn-like
behaviors have been observed in all classes of
vertebrates (Craemer 1924; Luttenberger 1975;
Baenninger 1987; Gallup et al. 2009), suggesting
important and basic functions. It is physically
similar across classes, and comparatively it has
been characterized as an extended gaping of the
mouth, followed by a more rapid closure (Provine
1986; Baenninger 1987). Provine (1986) first
proposed the 'state change hypothesis' based on
the observations that yawning was associated
with behavioral transitions. The general
hypothesis was then extended to suggest that
yawning facilitates a number of behavioral
shifts, e.g. from boredom to alertness and
changes from one activity to another (Provine
1996, 2005).
Through a thorough analysis of the
behavioral correlates, temporal contexts,
physiological mechanisms, and phylogenetic and
ontogenetic aspects, Baenninger (1997) concluded
that yawning might stimulate arousal during
state change. For instance, comparative research
shows that vertebrates yawn in anticipation of
important daily events and behavioral
transitions or during changes in activity
levels. A recent report on captive chimpanzees
(Pan troglodytes) provides strong support for
this hypothesis, showing that locomotion
increases after yawning (Vick & Paukner
2009). Consistent with an arousing effect of
yawning, it is also common when there are
stressful events, threats, and increases in
anxiety (Baenninger 1997; Gallup & Gallup
2008). Perhaps the most regular periods of state
change and locomotor activity occur during
transitions between sleep and wakefulness, and
the most frequent instances of yawning in humans
occur prior to the onset of sleep and just after
waking (Provine et al. 1987; Baenninger et al.
1996; Zilli et al. 2007). Yawning appears to
have a circadian pattern in other animals as
well; peaks in yawning frequency among
laboratory rats occur during light to dark
transitions, as activity increases (Anias et al.
1984).
The deep inhalation and constriction and
relaxation of facial muscles during a yawn are
hypothesized to modify levels of cortical
arousal through enhanced cerebral blood flow
(Askenasy 1989). Contrary to expectations from
the arousal hypothesis, however, a recent study
of electroencephalographic changes (EEG)
describe no arousing effect (as measured by
alpha power and activity) 10 s after yawning in
patients suffering from excessive daytime
sleepiness (Guggisberg et al. 2007). It is
entirely possible, however, that yawning may
increase alertness and vigilance over a longer
time, and in ways that are not detected by EEG.
For instance, yawning may increase arousal
through the mechanical stimulation of the
carotid body (Matikainen & Elo 2008).
Likewise, recent research suggests that
yawning may have a thermoregulatory function,
and in particular may serve to cool the brain
(Gallup & Gallup 2007), thus maintaining
mental efficiency and vigilance through thermal
homeostasis. Shoup-Knox et al. (2010) recently
explored the relationship between brain
temperature and yawning by implanting
thermocoupled probes in the prelimbic cortex of
rats (Rattus norvegicus) to measure changes in
brain temperature before, during and after
yawning. Results showed yawning was preceded in
all instances by rapid increases in brain
temperature, but as soon as yawning occurred,
brain temperatures began to decrease and there
was a return to baseline following each yawn
(Shoup-Knox et al. 2010). It is proposed that
yawns may provide a metabolically inexpensive
means of cooling by increasing venous blood
flow, removing warmer blood from the brain and
reducing temperature through convection.
During hyperthermia in humans, blood flow is
increased from the skin to the cranial cavity,
and this change is essential for proper cooling
of the brain (Cabanac & Brinnel 1985). It is
also hypothesized that the gaping of the mouth
and deep inhalation during a yawn cools 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 (Gallup & Gallup 2007).
Comparative research from birds, rats, and
humans shows that yawning is followed by
reductions in brain and body temperature, is
suppressed by other methods of behavioral
cooling, and is influenced by the direction and
range of ambient temperature (reviewed by Gallup
2010b; in press). Consistent with the view that
yawning is a thermoregulatory behavior, recent
research has revealed a strong negative
correlation between body temperature and the
latency to yawn following a stressor in
budgerigars (Melopsittacus undulatus) (Miller et
al. 2010). This hypothesis complements those of
arousal and state change, suggesting that the
cooling component of yawning may facilitate
these processes by reinstating brain thermal
homeostasis.
The thermoregulatory hypothesis
generates numerous testable predictions. One is
that yawning will occur in a 'thermal window',
or a narrow range of ambient temperatures
(Gallup & Gallup 2007). According to this
model, the temperature of the air gives the yawn
its utility. The model predicts that yawns
should increase in frequency as ambient
temperatures approach body temperature, diminish
as temperatures continue to rise, and cease when
ambient temperatures reach or exceed body
temperature because they would no longer result
in cooling. Among homeotherms, ambient air
temperature provides an accurate index of the
rate of heat transfer away from the body. During
a rise in ambient temperature, the body is
increasingly unable to lose heat, stimulating
thermoregulatory mechanisms to control internal
temperatures. Likewise, when temperatures fall
below a certain point, and the brain is not
overheated, further cooling is not beneficial.
Experimental work with budgerigars has recently
tested the first prediction of the thermal
window hypothesis (Gallup et al. 2009, 2010).
Budgerigars yawned more frequently during
increasing ambient temperatures (22&endash;34
C), but as temperatures continued to rise and
were held near body temperature (34&endash;38
C), yawning rate diminished as more effective
heat loss behaviors became prevalent (Gallup et
al. 2009).
A follow-up study demonstrated that
temperature change alone was not sufficient to
influence yawning in budgerigars, as decreases
across a similar range of ambient temperature
(34&endash;24 C) failed to produce associated
increases in yawning frequency (Gallup et al.
2010). Thus, in this species, the physiological
trigger for yawning appears to be related to
increasing body temperatures rather than the
detection of changing external temperatures.
Deputte (1994) was the first to describe an
association between yawning and ambient
temperature in primates. In macaques (Macaca
fasciularis), yawning was positively correlated
with ambient temperature, and rising ambient
temperature was correlated with heightened
yawning while lying down (Deputte 1994). Recent
naturalistic research on capuchins (Cebus
capucinus) showed patterns consistent with these
findings; yawning occurred significantly more
often when ambient temperatures were high and
humidity low (Campos & Fedigan 2009; for a
reply see also Gallup 2010a).
Given that fluctuations in ambient
temperature can produce changes in state and
activity, temperature manipulation provides an
interesting avenue to further investigate the
relationship between yawning, state change, and
thermoregulation across vertebrate species. The
present study examined the incidence of yawning,
associated behaviors (e.g. stretching), and
activity in rats as a function of the range and
direction of ambient temperature change. To our
knowledge, this is the first study to
experimentally investigate these associations in
a mammalian species. As in our recent studies in
budgerigars, we exposed rats to varying ambient
temperatures, manipulating the direction and
range of ambient temperature in a controlled
thermal chamber. Animals experienced rapid
changes in temperature of each direction
(low-increasing: 22 C fi 27 C; high-increasing:
27 C fi 32 C; high-decreasing: 32 C fi 27 C;
low-decreasing: 27 C fi 22 C), as well as
periods of constant temperatures (cool: 22 C;
warm: 32 C).
Based on the results of Gallup et al. (2010)
in budgerigars, we hypothesized that temperature
manipulation would produce changes in yawning
frequency, but that high-increasing ambient
temperatures would generate the highest rates of
yawning. We also predicted that lowest yawning
rates would occur during low-decreasing
temperatures. According to the predictions based
on the thermal window, we expected yawning rates
to be diminished in the constant high
temperature condition in comparison to the low
temperature condition. Although stretching is
commonly associated with yawning and arousal and
the two co-occur under many conditions
(Baenninger 1997), we predicted that they would
be disassociated in this experiment. Provine et
al. (1987) first reported a disassociation
between yawning and stretching in humans,
showing that yawns are accompanied by stretches
more so in the morning than in the evening.
In addition, our past research using ambient
temperature manipulation completely decoupled
these behaviors in budgerigars, significantly
impacting yawning rates while leaving stretching
unafunaffected (Gallup et al. 2009, 2010). These
results suggest differences in the functionality
of these behaviors. Therefore, we also
hypothesized that the frequency of stretching
would not vary across different thermal
environments, and that the rate of yawning and
stretching would not be correlated during
thermally challenging conditions. Lastly, we
hypothesized that initial rapid changes in
ambient temperature would increase arousal and
alertness, and potentially produce highest
locomotor activity.
Discussion
Among rats, yawning appears to be an initial
response to loss of thermal homeostasis. Results
indicate that initial changes in ambient
temperature, irrespective of direction, trigger
increased yawning and locomotor activity. As
temperature change was extended, however,
yawning frequency and activity began to drop or
return to baseline. During the sustained
directional changes in temperature, most yawning
occurred during low-increasing temperatures,
while the fewest yawns occurred during
lowdecreasing temperatures. When temperatures
were held constant, yawning rates were nearly
completely inhibited during high temperatures
(32 C), while locomotor activity was unchanged.
Unlike yawning and locomotor activity,
stretching frequency was unrelated to ambient
temperature variation. In addition, correlations
between yawning and stretching diminished during
thermally challenging, higher temperature
conditions, particularly when temperatures were
held constantly high (32 C). These results
support previous research identifying yawning
with arousal, activity, and state change, and
also contribute to a growing literature
connecting yawning and thermoregulation.
Similar to recent research on budgerigars
(Gallup et al. 2009, 2010), this report reveals
that ambient temperature manipulation influences
yawning in rats. The triggers appear, however,
to differ between the two species. Yawning
appears to be related to increases in body
temperature in budgerigars, whereas in rats it
appears to be more closely associated with the
detection of changing external temperatures.
Water conservation is likely to influence how
yawning is used to alleviate thermal stress, as
has been suggested for budgerigars (Gallup et
al. 2009). Thus different ecological conditions
are likely to alter the way yawning occurs among
homeothermic species. Budgerigars live in hot
and dry climates and experience wide daily
fluctuations in ambient temperature. They may be
better adapted to dealing with initial changes
in ambient temperature in the absence of yawning
(e.g. through increased circulation and heat
dissipation, or using other forms of behavioral
thermoregulation).
For instance, they are adapted to living at
higher temperatures and conserving water, and
they can escape heat and solar radiation by
flocking to shade. The elevated frequency of
yawning among budgerigars at highincreasing
temperatures may be a product of the
metabolically inexpensive nature of a yawn in
comparison to more costly evaporative cooling
behaviors (e.g. panting Ú gular fluttering) that
take over at sustained high temperatures.
Similarly, yawning has been witnessed at high
ambient temperatures in capuchins (Campos &
Fedigan 2009), which are also adapted to water
scarcity and live in seasonally hot tropical dry
forest. In addition, the predictions of the
thermal window rely on the relationship between
ambient and body temperatures and birds have
higher body temperatures than mammals. Nocturnal
rodents may be more sensitive to acute changes
in temperature, and thus yawning is triggered
during initial deviations of thermal
homeostasis. Likewise, yawning may not be
involved in more extended behavioral cooling
because water conservation is not as critical.
As evidence for this, during higher ambient
temperatures rats begin evaporative cooling
behaviors (e.g. grooming) shortly after being
exposed to thermally challenging conditions
(Roberts et al. 1974). Extended periods of
grooming were not witnessed within the narrow
temperature range of this study.
Similarities between these two species
exist, however, as yawning becomes less frequent
in both rats and budgerigars when temperatures
are held near body temperature, and when
temperatures are low and decreasing. These
results are consistent with the predictions of
the thermal window framework, and with
predictions that yawning is an initial and
compensatory cooling mechanism (Gallup &
Gallup 2007). In the current study, the near
complete inhibition of yawning at constant high
temperatures (32 C), and the increase in yawning
in the highdecreasing condition (32&endash;27 C)
may reflect a sensitive mechanism for
maintaining thermal homeostasis. The predictions
of the thermal window hypothesis rely on the
specific relationship between ambient and body
temperatures. At constant high temperatures,
yawning may fail to produce effective cooling
because the difference between ambient and body
temperature is too small (4 C), and therefore it
is inhibited. As ambient temperatures begin to
fall, however, this provides a setting in which
yawning regains utility.
This may also explain why, unlike in
budgerigars (which have higher body
temperatures), yawning rate was not greater
during high-increasing temperatures
(27&endash;32 C) among rats. Future research
could explore this comparatively by exposing
animals of different resting body temperatures
to a wider range of ambient temperatures. In
addition, although it has already been shown
that brain temperature fluctuations are
correlated with yawning events in rats during
constant ambient temperatures (Shoup-Knox et al.
2010), future research should examine the
incidence of yawning in response to core body
temperature changes. Likewise, studies of
yawning and thermoregulation in poikilotherms
are badly needed to understand the evolutionary
history of this behavior.
Our observations reveal that ambient
temperature fluctuation also produced clear
changes in locomotor activity levels during the
experiments. Following acclimation and periods
of constant ambient temperature, initial changes
in temperature triggered increased yawning and
locomotion among rats. These findings are
consistent with research on both humans and
chimpanzees, showing that yawning is related to
modified activity or increased locomotion
(Baenninger et al. 1996; Giganti et al. 2002;
Vick & Paukner 2009). Following continued
temperature change in either direction, both
yawning and locomotor activity fell
precipitously, suggesting that yawning is not
solely associated with drowsiness or rest.
Instead, these findings support a wide range of
comparative research showing a more general
relationship between yawning, state change, and
arousal (Provine 1996, 2005; Baenninger 1997).
Homeothermic species are able to preserve a
relatively constant body temperature as ambient
temperature fluctuates, using a combination of
autonomic and behavioral mechanisms controlled
by the central nervous system (reviewed by
Bicego et al. 2007). Among rats, yawning may be
an adaptive response to early signs of thermal
change, providing an increase in alertness and
vigilance through cerebral
thermoregulation.
Under thermally non-stressful conditions,
stretching is associated with yawning in rats
(Gessa et al. 1967) and a number of other
species (Baenninger 1997), and both are believed
to be involved in arousal. On the other hand,
past research on humans suggests that yawning
and stretching may serve different functions
(Provine et al. 1987), and it is likely that
yawning is multifunctional. For instance, human
stretching is accompanied by yawning, and after
waking yawning and stretching co-occur, but
yawns are less frequently accompanied by
stretches at night before sleeping (Provine et
al. 1987). Our results are consistent with this
view, showing that stretching behavior was not
affected by ambient temperature variation.
Likewise, stretching was correlated with
yawning only in a subset of the thermal
conditions, specifically during the increasing
and constant low temperatures. By separating
these commonly associated behaviors, ambient
temperature manipulations provide insight into
their adaptive function. Although yawning and
stretching have some similar physiological
consequences (increased circulation), the
regional differences in these effects are likely
to have considerable implications for the
purpose of each. Powerful stretching of jaw
muscles during a yawn are believed to
specifically increase local facial and cerebral
blood flow (Askenasy 1989), while body
stretching is likely to have more global
effects. In addition, unlike stretching, yawning
is accompanied by a deep inhalation of air.
Consistent with the thermoregulatory
hypothesis, yawning is significantly altered by
ambient temperature variation, while stretching
remains unaffected. These findings parallel
those of Gallup et al. (2009, 2010) for
budgerigars, suggesting that stretching is not
involved in thermoregulation. In summary, the
range of ambient temperature variation used in
this study produced significant changes in
yawning and locomotor activity among rats.
Overall, this research provides novel support
for the arousal and state change hypotheses
while also refining the predictions of the
thermoregulatory hypothesis. It is important
that these hypotheses are not considered
mutually exclusive, but closely integrated
mechanisms for regulating behavior. That is, the
thermoregulatory benefits resulting from yawning
may provide the mechanism by which increased
arousal is achieved.
Future research should continue to
comparatively investigate the association
between yawning and ambient temperature
variation. Although the effect of temperature
change on yawning is hypothesized to vary across
species, these differences should be predicted
by underlying physiology and the unique
evolutionary histories and ecological
adaptations to thermal stress.
