The existence of yawning across a diverse
array of species has led many researchers to
postulate its neurological significance. One
hypothesis, which has garnered recent support,
posits that yawns function to cool the brain by
flushing hyperthermic blood away from the skull
while simultaneously introducing a cooler
arterial supply. The current study tested this
hypothesis by examining how manipulations aimed
at modifying carotid artery temperature, which
in turn directly alters cranial temperature,
influences contagious yawning in humans.
Participants held either a warm (46 °C),
cold (4 °C) or room temperature (22
°C) pack firmly to their neck, just over
their carotid arteries, for a period of five
minutes prior to watching a contagious yawning
stimulus. Thermographic imaging verified that
these manipulations produced predicted changes
in temperature at the superomedial orbital area,
a region previously used as a noninvasive
measure of brain temperature (i.e., the brain
temperature tunnel). As predicted by past
research, both the urge to yawn and overall yawn
frequency significantly diminished in the
cooling condition (p < .05). Less than half
(48.5%) of the participants in the cooling
condition reported the urge to yawn, while this
urge was expressed by the vast majority of
participants in the warming condition (84.8%).
Moreover, there was a threefold difference in
the mean number of yawns per participant between
the cooling and warming conditions (0.364
compared to 1.121). These findings are
consistent with previous research indicating
that yawns function as a compensatory brain
cooling mechanism.
L'existence de bâillements
repérés dans un large
éventail d'espèces a conduit de
nombreux chercheurs à postuler une
signification neurologique. Une
hypothèse, qui a recueilli un soutien
récent, postule que les bâillements
servent pour refroidir le cerveau en chassant le
sang hyperthermique du crâne tout en
introduisant simultanément un apport
artériel plus froid. La présente
étude a testé cette
hypothèse en examinant la manière
dont les manipulations visant à modifier
la température de l'artère
carotide, qui à leur tour modifie
directement la température
crânienne, ont une incidence sur le
bâillement contagieux chez l'homme. Les
participants ont tenu un sac chaud (46 °
C), froid (4 ° C) ou à la
température ambiante (22 ° C)
fermement sur leur cou, juste au-dessus de leurs
artères carotides, pendant une
période de cinq minutes avant de regarder
des enregistrements vidéos de
bâillements, afin d'en déclencher
par contagion.
L'imagerie thermographique a permis de
vérifier que ces manipulations
produisaient les changements de
température prévus au niveau de la
région orbitale super-médiale, une
région précédemment
utilisée comme mesure non invasive de la
température cérébrale.
Comme prévu par des recherches
antérieures, le besoin de bâiller
et la fréquence globale de
bâillements ont considérablement
diminué dans les conditions de
refroidissement (p <0, 05). Moins de la
moitié (48, 5%) des participants en
période de refroidissement ont
signalé l'envie de bâiller,
à l'inverse de ce qui a été
exprimé par la grande majorité des
participants en période de
réchauffement (84, 8%).
De plus, le nombre moyen de
bâillements par participant était
trois fois plus important entre les conditions
de refroidissement que de réchauffement
(0,364 contre 1,121). Ces résultats sont
cohérents avec les recherches
précédentes indiquant que les
bâillements fonctionnent comme un
mécanisme accesoire de refroidissement du
cerveau.
1. Introduction
Yawning is a complex and reflexive motor
action pattern that ap- pears to be
evolutionarily conserved across vertebrates.
Recent comparative research suggests an
important neurophysiological function to this
response, as interspecies variability in yawn
duration robustly correlates with measures of
brain size and neuron density among mammals
[22,23]. To date, however, there remains
no consensus regarding its adaptive significance
[11,25,33].
Human neuroanatomical and physiological
investigations support a role of yawning in
enhanced intracranial circulation [44]
and brain cooling [5,19]. In particular,
the brain cooling hypothesis posits that yawns
are triggered by rises in cranial temperature,
and that both the circulatory and respiratory
outcomes of this motor action pattern function
to counteract these changes and promote thermal
homeostasis [17]. According to this
hypothesis, the extended muscular contractions
and deep inhalation of ambient air that
characterize yawns induce cooling of the brain
via convective heat transfer, thermal conduction
and evaporative heat loss (reviewed by
[14]). These physiological changes
associated with yawning could facilitate
instances of state change [39] and
cortical arousal [2] that follow this
behavior.
The first empirical support for the brain
cooling hypothesis came from research on human
subjects demonstrating an inhibition of
contagious yawning by methods of behavioral
brain cooling (i.e., nasal breathing and
forehead cooling) [17]. Subsequent
studies in both humans and non-human animals
exhibited predicted changes in brain temperature
[40,41], cranial surface temperature
[6,24], and oral temperature following
yawns [15]. Further comparative studies
have revealed the importance of ambient
temperature in controlling the expression of
this behavior (e.g., [7,20,36]).
Moreover, even fever has been shown to influence
yawn frequency in a pattern predicted by this
hypothesis [16,35]. Nonetheless, the
brain cooling hypothesis is not universally
accepted (see [8,9,26]), and some
researchers have pro- posed that yawning may
simply occur conjointly with natural changes in
brain temperature rather than functioning in
thermoregulation [33]. The current
experiment was designed to address this issue by
in- directly manipulating brain temperature
among human subjects to witness its effect on
yawning. Brain temperature in homeotherms is
controlled by the temperature of the arterial
blood flow to the brain, the rate of arterial
blood flow to the brain, and metabolic heat
production within the brain [4]. Here,
we aimed to temporarily manipulate the first
variable by having human subjects hold varying
temperature packs directly to the surface of the
neck above their carotid arteries prior to
viewing a contagious yawning stimulus. Although
the temperature of the arterial blood supply is
not equivalent to brain temperature (e.g.,
[31,32]), comparative research has
demonstrated that the arterial blood perfusing
the brain is the major determinant of cerebral
temperature in primates [30]. In
addition, the temperature of blood within the
carotid arteries has been shown to predict
internal brain temperature across diverse
species (e.g., [10,34,37]). Based on the
brain cooling hypothesis, and past research
employing similar procedures to modify cranial
temperature in human subjects [17], it
was predicted that cooling of the skin just
above the carotid arterial blood supply would
diminish yawning, while conversely warming of
this tissue would in- crease this response.
Contagious yawning was used as a proxy for
spontaneous yawning since it can be reliably
triggered in the laboratory [38] and
studies have repeatedly demonstrated that
variables altering spontaneous yawns also
control yawn contagion (e.g.,
[7,17,36]).
4. Discussion
The brain cooling hypothesis of yawning has
garnered recent empirical support (reviewed
[14]), and has shed light on previous
un- characterized connections between abnormal
or frequent yawning and thermoregulatory
dysfunction in humans [18]. To date, the
majority of past studies linking yawning with
changes in brain/skull temperature have been
correlational in nature. That is, yawns have
been shown to be preceded by rises in
temperature, and followed by decreases in
temperature (e.g., [15,40,41]). As a
result, some researchers have proposed that
yawns may simply coincide with natural changes
in brain temperature, and that fluctuations in
brain temperature do not actually trigger yawns
[33]. This study extended upon this
previous work by manipulating the temperature of
the neck just above the arterial blood supply to
the brain and observing changes in yawn
frequency thereafter.
In partial support of the brain cooling
hypothesis, results show that manipulations
aimed at modifying arterial blood temperature
significantly altered contagious yawning among
humans. In particular, applying a cold pack (4
°C) to the neck just over both carotids
reduced the surface temperature of the BTT and
significantly diminished both the urge to yawn
and overall yawn frequency in this study. These
findings replicate previous research
manipulating forehead temperature [17],
whereby contagious yawning was markedly lower in
the cooling condition. Similar reductions in
yawn contagion occur when ambient temperatures
fall below a thermal neutral zone [36].
Given that brain temperature is largely
influenced by the temperature of arterial blood
supply [4], the decreases in temperature
produced by the cold condition appeared to
inhibit the mechanisms controlling this
response. This can be viewed in the same way
other cooling mechanisms (e.g., sweating) cease
when internal temperatures fall below thermal
homeostasis.
No differences emerged between the warm and
room temperature conditions, which also mirrors
earlier research manipulating forehead
temperature [17]. Although the warm
temperature condition (46 °C) of the
current study produced an increase in
temperature at the BTT, associated increases in
yawning were not statistically different from
the room temperature condition. This particular
result is not entirely consistent with the brain
cooling hypothesis, which predicts that rises in
brain temperature should trigger yawning.
However, it has been posited that yawning serves
as a compensatory, rather than primary, cooling
mechanism, and thus it could be that the
elevation in cranial temperature produced by the
warm condition (~0.25°C) exceeded the
threshold for which yawning would be effective.
For example, recordings from free-moving rats
show that yawns are preceded by rises in brain
temperature of only 0.12°C [41],
which is less than half the magnitude produced
in this current study. Similar effects have been
observed across large deviations in ambient
temperature [12]. A range of comparative
studies have shown that initial rises in ambient
temperature trigger an increase in yawn
frequency, but that yawns then decrease in
frequency back to baseline levels as
temperatures approach or exceed body temperature
because counter-current heat exchange is no
longer effective [7,13,20,21]. These
findings are also consistent with the
perspective that yawning operates as an initial
and compensatory response to slight deviations
in thermal homeostasis. As temperatures continue
to elevate, heat dissipation becomes more
difficult and more effective regulatory
mechanisms are triggered [20]. Future
research could specifically test these
predictions by comparing yawning across a range
of different warm temperature conditions while
simultaneously tracking other well-documented
thermoregulatory cooling responses. In addition,
further studies could examine how temperature
manipulations to areas of the body more distant
from the skull (e.g., the forearm or abdomen)
influence yawn frequency.
The overall findings from this report are
consistent with previous research indicating
that yawns function as a compensatory brain
cooling mechanism. However, it remains unknown
whether the temperature manipulations to the
neck were sufficient to alter either arterial or
brain temperature. Although the reported
thermographic recordings revealed predicted
changes in temperature at the BTT, intracranial
temperatures were not obtained. Nonetheless,
this report adds to a growing list of
experimental findings demonstrating that the
mechanisms controlling yawning, including
spontaneous and contagious forms, are sensitive
to temperature.
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