The ultimate function of yawning continues
to be debated. Here, we examine physiological
measurements taken before, during, and after
yawns in humans, in an attempt to identify key
proximate mechanisms associated with this
behavior. In two separate studies we measured
changes in heart rate, lung volume, eye closure,
skin conductance, ear pulse, respiratory sinus
arrhythmia, and respiratory rate. Data were
depicted from 75 s before and after yawns, and
analyzed at baseline, during, and immediately
following yawns. Increases in heart rate, lung
volume, and eye muscle tension were observed
during or immediately following yawning.
Patterns of physiological changes during yawning
were then compared to data from non-yawning deep
inhalations. In one study, respiration period
increased following the execution of a yawn.
Much of the variance in physiology surrounding
yawning was specific to the yawning event. This
was not the case for deep inhalation. We
consider our findings in light of various
hypotheses about the function of yawning and
conclude that they are most consistent with the
brain cooling hypothesis.
INTRODUCTION
Yawning has been recorded in all five
classes of vertebrates, and is phylogenically
old, implying that it is an evolved mechanism
that serves an important adaptive function
(Baenninger, 1987). Yawning consists of opening
the mouth, deep inspiration, a short period of
apnea, followed by expiration (Walusinski and
Deputte, 2004). In humans and other animals,
yawning frequency has been shown to be dependent
upon circadian rhythms (Zilli et al., 2007).
Studies of yawning have generated varying
explanations regarding its ultimate function and
proximate mechanisms (Guggisberg et al.,
2010).
One commonly held notion is that yawning
functions to modify levels of oxygen and carbon
dioxide in the blood. However, when measured in
a controlled environment, yawning frequency was
not affected by manipulating levels of oxygen
and carbon dioxide (Provine et al., 1987). The
same study demonstrated that while exercise
doubled breathing rate, indicating a strong
increase in oxygen requirements, yawning
frequency remained unaffected.
A more recent hypothesis proposes that
yawning facilitates arousal (Baenninger, 1997;
Walusinski, 2006). Evidence for this hypothesis
comes from the elevated occurrence of yawning
before important events or during behavioral
transitions (Baenninger, 1997). Matikainen and
Elo (2008) proposed a proximate mechanism to
support this theory, suggesting that yawning
mechanically stimulates the carotid artery,
promoting an increase in cortical arousal via
neck compressions that accompany yawning. The
carotid body is highly vascularized and
compressions may increase circulation, resulting
in stimulation by hormones such as adenosine or
catecholamines (Matikainen and Elo, 2008).
The occurrence of contagious yawning has led
some researchers to conclude that the primary
purpose of yawning is to provide a means of
inner-species social communication (Guggisberg
et al., 2010), suggesting that yawning may be a
catalyst for conveying empathetic feelings, or
messages to a member of ones species. This
hypothesis fails to account for several
important aspects of yawning; including the
proximate behaviors associated with yawning such
as stretching, eye and mouth watering, mouth
gaping, eye closure, or deep respiration, and
the fact that contagious yawning occurs only in
a few species, and frequently occurs in
solitude. A recent review of this theory,
suggests that the social implications of yawning
are most likely a derived feature, and that the
ultimate function is likely physiological due to
its phylogenic history (Gallup, 2011).
Another hypothesis that has received recent
support posits that yawning is a brain cooling
mechanism (Gallup and Gallup, 2007, 2008). The
brain cooling hypothesis stipulates that yawning
is triggered by an increase in brain
temperature, and that the physiological
reactions following a yawn promote a return to
brain thermal homeostasis. Many thermoregulatory
mechanisms have been observed in animals, and
possible routes of human brain cooling have been
suggested (Zenker and Kubik, 1996). Recent
research directly measured cortical temperature
in rats and found a distinctive association
between brain temperature and yawning
(Shoup-Knox et al., 2010). By continuously
monitoring cortical temperatures during the
3-min prior to and following a yawn, these
researchers found a significant increase in
temperature leading up to the onset of a yawn,
followed by a significant decrease in
temperature and return to baseline in the 3-min
following the yawn.
While the ultimate function of yawning
remains debated, the current study measured and
evaluated the physiology associated with
spontaneous yawning. Presented here are two
studies which evaluated a variety of
physiological measurements before, during, and
after a yawn. Previous attempts to measure
physiology include examinations of skin
conductance (Baenninger and Greco, 1991; Greco
and Baenninger, 1991), heart rate (Heusner,
1946; Greco and Baenninger, 1991), and
vasoconstriction (Heusner, 1946).
Greco and Baenninger (1991) found increased
variability in heart rate and inconclusive skin
conductance changes associated with yawning.
Heusner (1946), however, found an increase in
beats per minute and an accompanying
vasoconstriction, but her results were gathered
from a small number of subjects and were not
tested statistically. Our goal is to identify
replicable patterns of physiological change
associated with yawning to better inform
theories of an ultimate function. Our first
study examined archival physiological data, and
focused on the impact of yawning on heart rate,
eye closure, lung volume, and respiration rate.
Additionally, we examined the effects of yawning
on sympathetic and parasympathetic activity by
measuring skin conductance and respiratory sinus
arrhythmia (RSA). The second study more closely
controlled measurements of heart rate, skin
conductance, lung volume, respiration rate, and
facial temperature, and provided a reliable
control variable, in the form of deep
inhalations.
GENERAL DISCUSSION
Together, these two studies demonstrate and
replicate unique physiological changes
associated with yawning. These physiological
responses constitute clues as to the ultimate
function of yawning. Yawning, as well as deep
inhalation increased facial temperature, lung
volume, and heart rate. Yawning, but not deep
inhalation caused a transient increase in
sympathetic nervous system arousal, and a
temporary decrease in Eamp. Also a decrease in
breathing rate appeared to be associated with
deep inhalation behaviors rather than yawning
specifically. The current findings suggest an
acute sympathetic nervous system response
concurrent with increased heart rate and tidal
volume. These data also dispute previous
findings that claim yawning did not produce
autonomic nervous system arousal (Guggisberg et
al., 2007).
Our results also differ from previous
studies that observed an increased variability
in heart rate following a yawn (Greco and
Baenninger, 1991; Guggisberg et al., 2007). We
observed a significant increase in heart rate
which was surrounded by less variability than
was observed surrounding deep inhalation. This
discrepancy may be due to the large amount of
yawns that Greco and Baenninger (1991) analyzed,
and the awareness of their subjects to the
research topic. They observed an average of
18.58 yawns an hour per person, across 30
subjects (4.59 per person during a 15-min
trial). This is a much higher rate of yawning
than previous studies have reported, suggesting
that because they knew they were in a yawning
study their subjects were displaying aberrant
amounts of yawning. Furthermore, their data
should not be considered indicative of
spontaneous yawns, but rather contagious yawns.
In contrast, both studies herein examined
spontaneous yawning from individuals with no
knowledge of being observed or participating in
a yawning study.
In Study 2, the magnitude of increase in
heart rate immediately following yawning (from
82.71 at baseline to 90.59 at its highest point)
replicated the findings from Study 1, but
surprisingly the difference from baseline did
not occur until PostS as opposed to our previous
effect at Peak. Heusner (1946) also reported
similar cardiac acceleration: from 80 to 90
beats per minute, with variations depending on
the strength of yawning. The acceleration
reported by Heusner accompanied vasoconstriction
in the finger. Changes in both heart rate and
vasoconstriction began 4-5 s following the
initiation of inhalation and were maximal at
ri9lOs after initiation. These results
temporally mimic the present results, confirming
an increase in heart rate following yawning.
Heart rate findings coupled with previous
reports of vasoconstriction clearly reveal
circulatory changes associated with yawning.
Also, the observed increase in facial-eye
temperature suggests an increase in blood flow.
Local skin temperature has been shown to rise
with increases in blood flow (for review see
Charkoudian, 2003). With an increase in heart
rate and skin temperature, we feel confident
that there is an increase in blood flow
associated with yawning.
The rate of blood flow to the brain is one
of the key factors in determining the
temperature of the brain. Blood flow rate, blood
supply temperature, and metabolic thermogenesis
as a result of neural activity, are the three
primary determinates of temperature in the brain
(Kiyatkin et al., 2002). Kiyatkin et al. (2002)
also observed that the temperature of the
arterial blood supplying the brain is
consistently lower than the temperature of the
brain during neuronal activation. The increase
in heart rate observed in our study would enable
this cooler blood to pass through the warmer
brain tissue more rapidly, increasing convective
cooling.
Because of the observed changes in
physiology, we believe that yawning serves a
physiological purpose. The changes lend support
to multiple physiological hypotheses,
specifically giving evidence for changes in
arousal, cognitive state, and brain temperature.
An increase in heart rate, and sympathetic
nervous system activity could be causing
increases in arousal as well as facilitating
changes in cognitive state. Further, the
increased heart rate strongly suggests increased
blood flow, and thus increased convective
cooling This suggests that proposed changes in
arousal following a yawn (Baenninger, 1997;
Walusinski and Deputte, 2004; Matikainen and
Elo, 2008) may be caused by increased blood
flow. The same could be true for the proposed
state-change hypothesis (Provine, 1986,2005),
which suggests that yawning is a vigorous,
widespread behavior that stirs up our physiology
and thus facilitates transitions to different
cognitive states. Because of the increase in
blood flow, we believe that our physiological
data best match the brain cooling hypothesis
(Gallup and Gallup, 2007). The regulation of
brain temperature could explain observed changes
in arousal levels, and would also support
cognitive state-changes.
Consistent with the brain cooling
hypothesis, arousal, and statechange hypotheses,
it is known that human brain temperature and
yawning co-vary with circadian sleep-wake
cycles. Yawning occurs most frequently in the
morning after waking, and in the evening just
prior to sleep (Zilli et al., 2007). Brain
temperature is highest before sleep, while
lowest during sleep. Yawning stops during sleep,
but yawning upon waking may be due to an
increase in metabolic activity. The state-change
associated with waking, and the increased
arousal that accompanies waking may require an
immediate change in blood flow, and temperature
regulation as well.
Neither the brain cooling, arousal,
state-change hypothesis, nor our current
findings that heart rate increased during
yawning are mutually exclusive of the hypothesis
that yawning promotes alertness and wakefulness
by stimulating the carotid artery (Matikainen
and Elo, 2008). The carotid body is the main
oxygen sensing organ in the body, its primary
function is to mediate cardiorespiratory
reflexes in response to systemic hypoxia and
hypercapnia (Prabhakar et al., 2005; Kumar and
Bin-Jaliah, 2007; Matikainen and Elo, 2008). A
combination of increasing blood flow, inhaling
cool air, or a transient spike in oxygen may
cause the carotid body to release
physiology-regulating hormones. This hypothesis
needs to be empirically tested, and revised to
take into account the mounting physiological
evidence associated with yawning observed in
this paper as well as others.
Some hypotheses regarding yawning stress
that its primary significance is to promote
social or empathetic communication (Guggisberg
et al., 2010). The suggestion that the ultimate
function of yawning is a social one fails to
explain the changes in physiology associated
with yawning. While social communication may be
an additional/derived function among humans and
a limited number of other species (Gallup,
2011), it is important to note the prevalence of
yawning across species, including those that
live in solitude and the majority of species
which lack cognitive empathy and communicative
understanding, such as fish and rats. Among
humans yawning begins prenatally (Walusinski,
2010), yet contagious yawning does not begin
until age 4 or 5 (Anderson and Meno, 2003),
suggesting that social or communicative effects
of yawning are a derived feature in a very small
number of species.
These studies document the physiological
mechanisms that occur during and following a
yawn. While our findings show changes in
physiology that are consistent with the concept
that yawning acts as a thermoregulatory
regulator, future studies need to examine this
concept more closely. Further, we understand
that a behavior as complex and phylogenetically
salient as yawning may be amenable to numerous
hypotheses regarding its ultimate function. We
stress the importance of proximate mechanisms
that have been documented to occur in tandem
with yawning when when thinking about the
adaptive function of yawning. The physiological
changes we have identified are the measurable,
salient, and important features of yawning.
In conclusion, we believe that our
data are most consistent with the brain cooling
hypothesis, and demonstrate an increase in blood
flow; one of several physiological mechanisms by
which yawning could induce brain cooling. The
increase in heart rate and sympathetic nervous
system activity associated with yawning also
needs to be considered when dealing with cases
of excessive yawning, and yawning related
medical symptoms. There is evidence linking
painful headaches (Jacome, 2001) and a variety
of thermoregulatory disorders (Sato-Suzuki et
al., 1998; Gallup and Gallup, 2008) with
excessive yawning. The yawning experienced
during these times may be due to circulatory
dysfunction. This coupled with evidence that
yawning has medical implications for a variety
of disorders (Sato-Suzuki et al., 1998; Gallup
and Gallup, 2008), suggests that aberrant
yawning is symptomatic of thermoregulatory
dysfunction. Thus, excessive yawning could be
clinically associated with
thermoregulatory/circulatory
distress/dysfunction, and could be used as a
diagnostic indicator. Further research needs to
be done to examine cranial-facial blood
circulation, as well as take direct thermal
measurements during yawning to define pathways
by which yawning influences brain
temperature.
