Yawning and swallowing are fundamental
physiological processes that are present from
fetal stages throughout life and that involve
sequential motor activities in the
oropharyngo-larynx making it likely that they
may share neuroanatomical pathways. We postulate
that yawning and swallowing are controlled by a
distributed network of brainstem regions
including the central pattern generator of
swallowing, and therefore spontaneous swallowing
is frequently associated with spontaneous
yawning. In this study, we sought to test this
hypothesis by evaluating the elementary features
of yawning in the facial, masseter and submental
muscles, together with laryngeal movement sensor
and respiratory recordings for spontaneous
swallowing. We investigated 15 healthy, normal
control subjects, 10 patients with Parkinson's
disease (PD) and 10 patients with brainstem
stroke (BSS). Apart from four subjects with PD
and two with BSS, who had dysphagia, none of the
other study subjects were dysphagic by published
criteria. Twenty-five subjects (10 control, 10
BSS, 5 PD) were evaluated by 1-h polygraphic
recording, and 10 (5 control, 5 PD) underwent
whole-night sleep recordings. One hundred
thirty-two yawns were collected, 113 of which
were associated with spontaneous swallows, a
clear excess of what would be considered as
coincidence. The yawns related with swallows
could be classified into the following three
categories. The characteristics or the duration
of swallows and yawns were similar between
controls and disease subjects, with the
exception of increased duration of yawning in
subjects with BSS. Our findings support the
presence of common neuroanatomico-physiological
pathways for spontaneous swallows and
yawning.
Introduction
Yawning is an involuntary and stereotyped
behavior common to several vertebrate species
besides humans. It occurs from fetal stages to
adulthood (Baenninger 1997; Walusinski and
Deputte 2004; Provine 2005). One of the best
descriptions of yawning in humans was reported
by Barbizet (1958) as a complex, involuntary and
paroxysmal movement.
It is a motion unfolding itself in a certain
order wherein three phases may invariably be
distinguished. The first one is active and
inspiratory; the second phase corresponds to the
acme; and the third phase is passive and
expiratory (Barbizet 1958). Yawning occurs about
7&endash;8 times per day in adult human subjects
with a range of 0&endash;28. It is more likely
to take place during wake&endash;sleep and
sleep&endash; wake transitions. It may also
occur during boredom and the onset of hunger and
satiety (Barbizet 1958; Provine and Hamarnick
1986; Walusinski 2009).
When we look at yawning from the view of the
oropharynx and respirations, the three phases of
yawning described by Barbizet (1958) should be
very important for breathing and spontaneous
saliva swallowing. In the first phase, there is
a progressive slow opening of the mouth while
the dilatation of the pharynx, larynx and thorax
and lowering of the diaphragm muscle can be
shown by radiological methods. The second phase
of yawning corresponds to the acme of the
mouth's opening and to that of pharyngeal and
thoracic dilatation. Facial modification begins
at the end of the first phase. Contraction of
the lip dilatators exaggerates the mouth's
opening, and contraction of the eyelids causes a
partial or even total occlusion of the eyes. At
this phase, partial or general stretching could
also be observed particularly on the neck and
trunk extension including hyperextension of the
limb muscles. The third phase is passive, where
inspirium ceases abruptly and expiration is
slow. Pharynx goes back to its normal size,
mouth closes spontaneously, and the face resumes
its usual aspects.
During these 5&endash;7 s, we may expect a
highly significant amount of sensory input to
the brainstem from ponto-bulbar and upper spinal
cord (Ertekin et al. 2000; Ertekin and Aydogdu
2003; Ertekin 2014). Additionally, increased
salivary flow associated with yawning was
reported (Inomata et al. 2005). Duration of
yawning was reported as 4&endash;7 s (Barbizet
1958) and even as long as 5&endash;10 s
(Askenazy 1989; Walusinski 2009). Thus, it is
possible that spontaneous saliva swallowing
could overlap with yawning within this duration
or that the physiological nature of yawning
could elicit spontaneous swallowing. There are
likely to be similarities between the
neuroanatomical pathways utilized in yawning and
spontaneous saliva swallowing both of which
involve the oropharynx and larynx. It is
probable that the same ponto-bulbar and upper
cord afferents and their receiving nuclei are
involved in both activities. Swallowing occurs
mostly in non-REM-1 and non-REM-2 stages of
sleep (Sato and Nakashima 2006; Ertekin et al.
2013). Similarly, yawning was often observed in
the same stages of sleep. Thus, yawning and
swallowing may be controlled by a distributed
network of brain stem regions including the
central pattern generator (CPG) of swallowing
(Cattaneo et al. 2006; Zilli et al. 2008;
Walusinski 2009). Therefore, our hypothesis is
that spontaneous saliva swallowing is frequently
associated with spontaneous yawning.
Another piece of evidence in support of this
hypothesis comes from Parkinson's disease (PD)
and other parkinsonian disorders. There are
reports that certain extrapyramidal syndromes
are accompanied by the disappearance of yawning
such as patients under neuroleptic treatment
(Mogulnicka and Klimek 1977) and PD (Clossimo
and Pontieri 1999). The treatment by
apomorphine, a rapidly acting dopaminergic
stimulant, is observed to trigger yawning during
the "off" period in PD (Blin et al. 1990; Kolls
and Stacy 2006). Yawning difficulties were
described in progressive supranuclear palsy
(PSP) which were treated by dopamine agonists
(Sandyk 1987). Importantly, there are a
considerable number of PD and brainstem stroke
(BSS) patients with dysphagia (Ertekin et al.
2002; Ertekin 2014; Kalf et al. 2012; Michou et
al. 2013 and many others for PD and Horner et
al. 1991; Daniels et al. 1999; Aydogdu et al.
2001; Smithard 2002 for BSS).
Thus, studying the relationship between
yawning and swallowing in subjects with
parkinsonian disorders as well as healthy
controls can provide clues about the
relationship of these fundamental processes in
health and disease.
Thus, we postulate that yawning and
swallowing are controlled by a distributed
network of brainstem regions including the
central pattern generator of swallowing, and
therefore spontaneous swallowing is frequently
associated with spontaneous yawning. Therefore,
we studied by evaluating the elementary features
of yawning in the facial, masseter and submental
muscles, together with laryngeal movement sensor
and respiratory recordings for spontaneous
swallowing. To our knowledge, relationship
between spontaneous yawning and swallowing has
not hitherto been studied in health and disease
using such thorough neurophysiological
assessment.
Discussion
In this study, 132 spontaneous yawns from 35
normal controls and patients were individually
investigated. Only 19 yawns were not found to be
associated with spontaneous swallows. This may
be due to methodological artifact; because the
EMG of yawning in the OC, OR, MS and SM muscles
often had crescendo and later decrescendo
interference patterns with high amplitude, the
swallowing pattern of the related muscles could
not be distinguished. Furthermore, sometimes the
laryngeal sensor was disturbed by maximal
opening of the mouth, and swallowing pattern
could, therefore, not be distinguished easily
from the traces. Additionally, due to the low
incidence of yawning, some saliva swallows could
be missed by the examiners. All of these
technical issues could have resulted in the low
yawning&endash; swallowing association during
the yawning period This means that about 86 % of
spontaneous yawning is associated with
spontaneous swallows. Hence, these two
oropharyngo- respiratory spontaneous behaviors
are often but not always associated with each
other. The high incidence of spontaneous yawning
associated with swallowing is compatible with
these two oropharyngo-laryngeal behaviors.
The anatomophysiological conditions produced
by spontaneous yawning underscore the
physiological nature of this association.
Spontaneous yawning is a complex act consisting
of a long inspiration phase that comprises of
mouth opening, dilatation of pharynx, larynx and
thorax and diaphragm together with a brief
interruption of ventilation and final expiration
phase which involves the relaxation of all
participating muscles (Barbizet 1958; Baenninger
1997; Provine 2005). During the inspiratory
period of yawning, there is a strong possibility
that the saliva accumulated in the oral cavity
or escaping to the pharynx triggers a swallow.
It has been shown that inspiration is prolonged
in duration when swallowing takes place during
the inspiratory phase of respiration. Despite
this, the EMG activity of the diaphragm does not
cease with swallowing during inspiration (Uysal
et al. 2013). During prolonged inspiration, it
is easier to record spontaneous swallows
overlapping with the yawning period. Nearly 18 %
of spontaneous yawning was associated with a
swallow within its action period. In reality,
this number must be higher, but technically
during the maximal opening of the mouth, we
could neither observe nor record associated
swallows. This is because there is a crescendo
type of increase in the EMG amplitudes of
related muscles of yawning leading to a
tremendous peak, in parallel with the clinical
mouth opening. Therefore, in this part of
yawning, it is not possible to clearly visualize
swallowing-related muscle activity. The second
mode of association with swallowing that occurs
right at the end of yawning was the most
frequently encountered relationship between
these two spontaneous oropharyngeal behaviors.
The end of the yawn and the onset of the swallow
are rather close to each other. Clinically, at
the end of closing of the mouth, swallowing can
appear in this mode of association.
Why is spontaneous yawning frequently
associated with spontaneous saliva swallows?
Despite lack of clear evidence, we may postulate
that the tremendous inputs coming from many
muscles innervated by the lower motor cranial
nerves (V, VII, IX, X, XI and XII) and the
cervical (C1&endash;C4) and thoracic cord
(intercostal nerves) have already been excited
by about 6 s of yawning. It is well known that
the nuclei of the motor cranial nerves are
situated in the pontomedullary region. Given
that there is a sequential muscle activation
from cranial to caudal direction in the yawning
behavior, it is likely that this is organized at
the premotor level, like the central pattern
generator (CPG) of swallowing situated at the
nucleus tractus solitarii (NTS) and nucleus
ambiguous (NA) with a link to respiratory rhythm
center as pre-Bötzinger complex. (Jean
2001; Ertekin and Aydogdu 2003; German et al.
2009; Lang 2009; Ott et al. 2012; Ertekin et al.
2013). It is probable that spontaneous yawning
activity is organized at similar neural
structures as for swallowing, and the higher
excitability of premotor neurons during yawning
leads to the secondary behavior of swallowing.
Since brainstem circuits are involved in the
sensorimotor control of multiple functions
including respiration, mastication and
swallowing (Jean and Dallaporta 2006; German et
al. 2009), both yawning and swallowing may be
under the control of similar brainstem
circuitry. Furthermore, increased salivary flow
in association with yawning has been reported
(Inomata et al. 2005), which may also increase
the excitability of the swallowing CPG neural
network. This may produce firstly the spill of
saliva through pharynx during the yawn. It is
conceivable that just after yawning and within 2
s of its termination, a prolonged and rhythmic
excitability of the CPG might produce later
Materials and swallows (Nakamura et al. 2004;
Aydogdu et al. 2011). We also detected increased
saliva accumulation associated with yawning in
our patients with PD, as previously shown (Kalf
2011).
Yawning is classified into two types as
spontaneous and contagious yawning. Both types
are similar in their motor action and their
triggering mechanism, although their
evolutionary nature and social meaning are
different (Provine and Hamarnick 1986;
Baenninger 1997). Abe et al. (2014) reported
that contagious yawn and swallow are temporally
related, and frequency of yawn was increased
within 10 s of post-yawn period in normal adult
subjects. Our study is principally different
than that of Abe et al. as we describe and
demonstrate qualitative and quantitative
features of spontaneous yawning associated with
swallowing, from the onset to the end of yawning
and within a 2 s window after the end of a yawn.
The main conclusion from the Abe et al. study
was the identification of the increased rate of
swallowing after contagious yawning. Although it
was previously described that two patients had
inhalation of foreign bodies into their bronchi
which manifested as suffocation (Evans 1978),
spontaneous yawning associated with swallows
seemed to be safe for our patients. We did not
observe any clinical signs of aspiration such as
coughing just after yawning, even in our six
patients with neurogenic dysphagia.
In conclusion, spontaneous yawning
and swallowing are often but not always
associated with one another. Normal controls and
patient groups did not differ in their yawning
and swallowing features by clinical and
electrophysiological methods. Quantitatively,
the EMG duration of yawning was significantly
prolonged in the BSS group. This is probably due
to the fact that both spontaneous yawning and
spontaneous swallowing are operated within the
brainstem. Finally our electrophysiological
findings support the presence common
neuroanatomico-physiological pathways for
spontaneous swallows and yawning.
