Yawning is a stereotyped motor behavior
characterized by deep inhalation and associated
dilation of the respiratory tract, pronounced
jaw opening, and facial grimacing. The frequency
of spontaneous yawning varies over the diurnal
cycle, peaking after waking and before sleep.
Yawning can also be elicited by seeing or
hearing another yawn, or by thinking about
yawning, a phenomenon known as "contagious
yawning". Yawning is mediated by a distributed
network of brainstem and supratentorial brain
regions, the components of which are shared with
other airway behaviors including respiration,
swallowing, and mastication. Nevertheless, the
possibility of behavioral coordination between
yawning and other brainstem-mediated functions
has not been examined. Here we show, with a
double-blind methodology, a
greater-than-fivefold increase in rest (saliva)
swallowing rate during the 10-s period
immediately following contagious yawning
elicited in 14 adult humans through the viewing
of videotaped yawn stimuli. Sixty-five percent
of yawns were followed by a swallow within 10 s
and swallows accounted for 26 % of all behaviors
produced during this post-yawn period. This
novel finding of a tight temporal coupling
between yawning and swallowing provides
preliminary evidence that yawning and swallowing
are physiologically related, thus extending
current models of upper airway physiology and
neurophysiology. Moreover, our finding suggests
the possibility that yawning plays a role in
eliciting rest swallowing, a view not considered
in previous theories of yawning. As such, the
present demonstration of a temporal association
between yawning and swallowing motivates a
re-examination of the longstanding question,
"Why do we yawn?".
Introduction
Yawning is a stereotyped motor behavior
observed in a variety of vertebrate species
including non-human and human primates
[1&endash;3]. A yawn can be
conceptualized as a paroxysmal sequence of
muscle contractions that gives rise to three
phases of yawn-related movements over a period
of 4&endash;7 s [1, 3]. The initial
phase of yawning is characterized by gradual jaw
opening and retraction and lowering of the
tongue and hyoid bone [1]. This series
of movements is accompanied by contraction of
the diaphragm causing inspiration and associated
dilation of the pharynx, larynx, trachea, and
bronchi. During the second phase of yawning,
continued inspiration increases thoracic volume,
with associated continued dilation of the
pharynx, larynx, and thorax. There is maximal
jaw opening, facial grimacing, and extension of
the neck, trunk, and sometimes the limbs. The
third phase of yawning is passive and involves a
transition from inspiration to expiration,
possibly accompanied by vocalization, and the
return of the orofacial and thoracic musculature
to its rest position. Thus, yawning produces a
generalized and pronounced stretching of the
respiratory, axial and limb musculoskeletal
systems [1, 4, 5].
The frequency of spontaneous yawning varies
over the diurnal cycle, with the highest
frequencies observed at waking and before sleep
[6&endash;8]. In humans, the daily
frequency of spontaneous yawning has been
reported to average from 8.7 [9] to
13.46 [6], with a range of 0&endash;28
[9]. Additionally, in certain species,
''contagious yawning'' can be elicited by
experiencing another yawn or, in the case of
humans, by simply thinking about yawning [3,
10]. While the mechanisms underlying
contagious yawning remain unclear, brain-imaging
studies have implicated brain regions that
process motor imitation, empathy and social
behavior, including the mirror neuron system
[11&endash;15]. The phenomenology of
yawning has fuelled divergent hypotheses
regarding its functional significance. In
particular, the distinction between spontaneous
yawning and contagious yawning has led to the
view that yawning may have both physiological
and social roles.
Physiological hypotheses propose that
yawning regulates a peripheral organ system
and/or a central nervous system (CNS) function
such as respiratory homeostasis or CNS arousal
[14]. For example, Walusinski
[16] reported that the strong sequence
of muscle contractions in yawning disrupts the
functional neural network mediating
rapid-eye-movement (REM) sleep and associated
motor patterns, and facilitates the emergence of
another functional network that controls motor
patterns of awakening. In contrast, contagious
yawning has been linked to empathy and social
proximity to conspecifics. In support of this
proposal, humans who perform better on
self-recognition and theory-of-mind tasks, which
are believed to reflect the capacity for
empathy, demonstrate a greater propensity to
yawn in response to a contagion [12].
Contagious yawning in chimpanzees has been shown
to reflect social ''ingroup'' versus
''outgroup'' biases [17].
Nonetheless, the functional significance of
yawning remains unclear. Lesion studies in
patients and, more specifically,
neuropharmacological studies in which yawning
has been evoked through the application of
neurochemical agents to various sites within the
CNS in animal models, have suggested that
yawning is under the control of several
neurotransmitters and neuropeptides that act on
a distributed network of brainstem and
supratentorial regions including the medulla and
pons, the paraventricular nucleus (PVN) of the
hypothalamus, and cortical and subcortical
regions, with the PVN possibly playing a
fundamental role in initiating yawning [1,
18, 19]. Muscles that contract during
yawning are innervated by cranial nerves V, VII,
IX, X, XI, XII, cervical nerves C1&endash;C4,
and dorsal nerves innervating the intercostals
[20]. These brainstem circuits are also
involved in the sensorimotor control of other
upper airway behaviors including respiration,
swallowing, and mastication [21, 22].
This shared neural circuitry suggests the
possibility that yawning is coupled with other
brainstemmediated functions. Nevertheless, the
possibility of behavioral coordination between
yawning and other upper airway functions has not
been examined. Our laboratory and others have
reported a series of studies showing that
stimulation of the posterior oral cavity
and oropharynx with air-pulse trains is
associated with a statistically significant
increase in the frequency of resting (i.e.,
saliva) swallowing [23]. This
up-regulation of swallowing has been
demonstrated in young and older healthy adults,
and in patients with swallowing impairment
secondary to stroke [24, 25].
Interestingly, among individuals who had
suffered a stroke, the air-pulse trains were, in
a small number of instances, followed initially
by a yawn followed by swallowing (Theurer,
unpublished observations). This unanticipated
observation is consistent with the view that
yawning and rest swallowing may be
physiologically related. Therefore, the purpose
of the current study was to examine the temporal
relationship between contagious yawning and rest
swallowing. It was hypothesized that rest
swallowing rate would be increased during the
period of time immediately following yawning,
compared with other periods during which yawning
did not occur. A temporal coupling between
yawning and rest swallowing would be expected to
have clinical significance insofar as methods to
elicit contagious yawning might be employed in
rehabilitation to evoke swallowing, for example,
in individuals with dysphagia.
Discussion
Elicitation of Yawning
Based on previous evidence that yawning
frequency increases in association with the
viewing of yawning, the present study employed a
yawn video to elicit contagious yawning among
the study participants [6, 12, 26]. As
anticipated, the frequency of yawning increased
significantly during viewing of the yawn video,
supporting the efficacy of this visual stimulus
in promoting contagious yawning. Nevertheless,
the degree of contagious yawning varied
substantially across participants, consistent
with previous reports [12, 26].
Giganti and Zilli [6] studied
spontaneous and contagious yawning throughout
the course of the day in young adults and
reported a mean yawn frequency of 3.09 over a 3
min 12 s yawn-viewing condition conducted at
9:00 am. (i.e., a rate of approximately 0.96
yawns/min). The present study, which was
conducted at approximately the same time of day,
yielded a lower yawn rate of 0.37 yawns/min
during the yawn-viewing condition. This
discrepancy may be attributed to the fact that
participants in the present study were
naġ¨ve to the fact that the study was
examining yawning, whereas the subjects in
Giganti and Zilli [6] were made aware of
the study objectives. Thinking about yawning has
been shown to elicit contagious yawning [3,
10]. In the present study, yawn frequency
increased not only during the viewing of the
yawn video but also during the subsequent rest
and gape-viewing conditions. Previous research
has suggested that contagious yawning is not a
short-latency response but rather is evoked up
to several minutes following the presentation of
a yawning contagion [3]. Thus, it is
possible that the increased occurrence of
yawning during the rest and gape-viewing
conditions in the current study reflects a
carry-forward attribute of contagious yawning.
Temporal Coupling of Yawning and Swallowing The
present study provides the first evidence of a
temporal coupling between yawning and rest
swallowing. Sixty-five percent of yawns were
followed by a swallow within 10 s and swallows
accounted for 26 % of all behaviors produced
during this post-yawn period. Moreover, there
was a greater-than-fivefold increase in mean
swallowing rate during the 10 s following
yawning compared with the remainder of the study
period.
We are aware of only one previous study that
examined motor behavior immediately following
yawning. Baenninger et al. [9] showed
that wrist motion increased during the 15-min
period immediately following yawning in young
adults, suggesting that yawning is predictive of
an increase in motor activity level. Increased
skin conductance following yawning also has been
interpreted as supporting a period of heightened
arousal following yawning [10]. However,
decreased skin conductance during the immediate
post-yawn period also been reported, making
interpretation of these findings difficult
[27]. The present study examined a much
shorter post-yawn period than Baenninger et al.
[9] (i.e., 10 s vs. 15 min) and thus
provides novel evidence of a tight temporal
association between yawning and subsequent motor
behavior, in this case, motor activity involving
the upper aerodigestive tract. As to the
question of why the participants in the present
study tended to swallow immediately after
yawning, it is possible that yawning is
associated with increased salivary flow which,
in turn, evokes swallowing. Salivary flow has
been shown to have a direct influence on the
rate of resting swallowing in awake adults
[28, 29]. While increased salivary flow
in association with yawning has been noted
briefly in the literature [30], we are
not aware of any experimental evidence
supporting this claim. Nevertheless,
yawn-related modulation of salivary flow seems
plausible given that salivary secretion is
influenced by both oral sensory stimulation and
oral motor behavior [31, 32].
For example, increased parotid gland
salivary secretion during mastication has been
attributed to multiple oral mechanoreceptive
inputs from the periodontal ligament, gingival
tissues, and possibly the tongue [33].
Yawning produces a pronounced stretching of the
orofacial musculoskeletal system that would be
expected to stimulate multiple sensory receptors
along the length of the respiratory tract, as
well as potentially increasing perfusion to
muscles surrounding the salivary glands and
physically deforming the salivary glands
themselves. These yawn-related sensory and motor
events may modulate salivary flow.
Beyond its potential effects on salivary
flow, yawnrelated sensory stimulation of the
upper aerodigestive tract may have more direct
facilitatory influences on swallowing
elicitation. Sensory input is vital to the
initiation and regulation of the oral,
pharyngeal and esophageal phases of swallowing
[34, 35]. This view is supported by
evidence that the swallowing motor pattern is
(i) modulated by properties of the ingested
material and the bolus being swallowed
[36&endash;38], and (ii) impaired
following oropharyngeal anesthesia [39].
Moreover, it appears that swallowing is elicited
not only in relation to the presence of saliva
or ingested food and drink; non-nutritive
stimuli, including air-pulse trains directed
toward the oropharynx [23&endash;25,
40], and electrical stimulation of the
oropharynx [41], also have been shown to
be associated with increased rest swallowing. As
such, it is conceivable that the robust sensory
stimulation of the airway produced by yawning
exerts an excitatory influence on swallowing
regulatory mechanisms.
Swallowing is controlled by a medullary
central pattern generator that receives cranial
nerve afferent inputs and descending inputs from
cortical and subcortical centers, and produces a
stereotyped pattern of swallow-related
contraction of muscles innervated by cranial and
cervical nerves [42&endash;44]. This
neural network is extensively interconnected
with neural circuits that mediate other upper
airway behaviors such as mastication and
respiration [21, 22]. Moreover, there is
evidence that these behavior-specific networks
may share neural elements that are functionally
recruited to regulate, for example, respiration
or swallowing, depending on the prevailing
environmental demands [45]. These
mechanisms are believed to underlie the precise
coordination of respiration and swallowing, and
mastication and swallowing, which has been
documented through behavioral and
electrophysiological studies in a number of
species [46&endash;48]. Yawning, like
swallowing, is controlled by a distributed
network of supratentorial and brainstem regions,
including several cranial nerve nuclei [1,
18&endash;20]. The circuits that mediate
yawning and swallowing appear to share several
brainstem elements, suggesting a neural
substrate for the coordination of yawning and
swallowing. The present finding of a temporal
coupling between contagious yawning and resting
swallowing provides behavioral evidence for such
a coordinative functional organization.
It is possible that yawning influences
swallowing indirectly as a result of its effects
on respiration and ventilation. Nevertheless,
the hypothesis that yawning equilibrates blood
O2 and CO2 levels, which has been cited
frequently, lacks empirical evidence. The most
direct examination of the issue appears to be a
study by Provine et al. [49] who studied
the effect on yawning of breathing room air
(baseline), compressed air (control), 100 % O2,
and gas mixtures with higher than normal levels
of CO2 (3 or 5 % CO2) in healthy young adults.
They reported that breathing CO2 or O2 had no
significant effects on yawning rate or yawn
duration compared with breathing room air or
compressed air. In a companion study, the same
authors examined the effects of exercise on
yawning rate. While exercise significantly
increased breathing rate, it had no significant
effect on yawning rate. Another perspective is
that yawning may be a mechanism through which
the chest wall and diaphragm are adjusted for
optimal rest breathing, based on sensory
feedback. While our literature review failed to
identify any studies that have examined the
chest wall and diaphragm correlates of yawning,
the current finding of a temporal relationship
between yawn and swallow motivates future
studies of the relationships between respiratory
kinematics and gas exchange, yawning, and
swallowing. Adaptive Significance of Post-yawn
Swallowing The present finding that swallowing
occurs immediately following yawning begs the
question: what is the adaptive role of post-yawn
swallowing? Swallowing serves both supportive
and protective roles, transporting oral contents
and ingested material from the mouth to the
stomach and protecting the airway from tracheal
aspiration [21]. The frequency of both
spontaneous and contagious yawning peaks in the
early morning and late evening and is correlated
with the daily time-course of sleepiness [6,
50]. The early morning and late evening are
periods in the diurnal cycle when there would
appear to be a premium on ensuring that oral,
pharyngeal and laryngeal contents, including
whole saliva, nasal and pharyngeal mucus, food
stasis, and other particulate matter are cleared
from the upper aerodigestive tract. Accumulated
debris present in the oral cavity upon waking
must be cleared to optimize oral hygiene and
prepare the oral cavity for daily activities
including eating and speech production. Prior to
sleep, there may be an adaptive advantage to
clearing the oral cavity of contents to avoid
tracheal aspiration during sleep. Additionally,
swallow-related esophageal peristalsis would
contribute to clearing the bolus from the
esophagus prior to lying recumbent, thus
reducing the risk of gastroesophageal reflux
during sleep [21].
Clinical Significance
Our finding that yawning and rest swallowing
were temporally associated suggests that yawning
may hold potential in swallowing rehabilitation,
particularly for individuals whose dysphagia is
characterized by reduced swallowing rates
[51]. Yawn contagions, for example,
video images of yawning, could be provided to
patients to evoke contagious yawning and, by
association, swallowing. This general approach
would appear to have several clinical
advantages: the stimuli are non-invasive, can be
developed readily, at low cost, and accessed
through smartphone or tablet technology. In
addition, because the patient is not required to
follow instructions or perform voluntary
movements, the approach might be appropriate for
individuals whose rehabilitation options are
limited by reduced cognitive and language
capacities. That said, carryover of the yawn
stimuli to the swallowing of food/liquid has
never been examined and would need to be a focus
of future research before use of this technique
with patients.
Conclusion
The present study provides preliminary
evidence that adult humans tend to swallow
immediately following yawning. This finding of a
tight temporal coupling between yawning and
swallowing suggests that yawning and swallowing
are physiologically related, thus extending
current models of upper airway physiology and
neurophysiology. Our finding also implicates
yawning in the elicitation of rest swallowing, a
function not considered in previous theories of
yawning. Finally, the present demonstration of a
temporal association between yawning and
swallowing prompts a reexamination of the
longstanding question, ''Why do we yawn?''.
