Center of Sleep Medicine,
Department of Neurology, Inselspital,
University of Bern,
Switzerland.
BACKGROUND: Although yawning is a
ubiquitous and phylogenetically old phenomenon,
its origin and purpose remain unclear. The study
aimed at testing the widely held hypothesis that
yawning is triggered by drowsiness and brings
about a reversal or suspension of the process of
falling asleep.
METHODS: Subjects complaining of
excessive sleepiness were spontaneously yawning
while trying to stay awake in a quiet and
darkened room. Changes in their
electroencephalogram (EEG) and heart rate
variability (HRV) associated with yawning were
compared to changes associated with isolated
voluntary body movements. Special care was taken
to remove eye blink- and movement-artefacts from
the recorded signals.
RESULTS: Yawns were preceded and
followed by a significantly greater delta
activity in EEG than movements (p</=0.008).
After yawning, alpha rhythms were attenuated,
decelerated, and shifted towards central brain
regions (p</=0.01), whereas after movements,
they were attenuated and accelerated
(p<0.02). A significant transient increase of
HRV occurred after the onset of yawning and
movements, which was followed by a significant
slow decrease peaking 17s after onset
(p<0.0001). No difference in HRV changes was
found between yawns and movements.
CONCLUSIONS: Yawning occurred during
periods with increased drowsiness and sleep
pressure, but was not followed by a measurable
increase of the arousal level of the brain. It
was neither triggered nor followed by a specific
autonomic activation. Our results therefore
confirm that yawns occur due to sleepiness, but
do not provide evidence for an arousing effect
of yawning.
-Guggisberg AG, Mathis J, Hess CW. Interplay
between yawning and vigilance: a review of the
experimental evidence. Front Neurol Neurosci.
2010;28:47-54.
-Guggisberg
A, Hess Ch. Clinical significance of yawning
in disorders of consciousness and vigilance.
Epileptologie. 2014;31:82-86.
Mise en
doute de l'effet éveillant du
bâillement
Bien que le bâillement soit un
comportement ubiquitaire et
phylogénétiquement ancien, son
origine et sa fonction restent l'objet de
spéculations non
démontrées. Cette étude a
pour but de tester l'hypothèse largement
répandue que le bâillement est
induit par la fatigue et lutte contre
l'endormissement.
Des sujets se plaignant spontanément
d'une somnolence excessive ont été
observés. Leurs bâillement
spontanés ont été
comptabilisés, en particulier quand ils
essaient de rester éveillés dans
une pièce sombre et calme. Les
modifications de leur EEG et de leur
fréquence cardiaque ont été
enregistrées ainsi que leurs
bâillements, puis ces données ont
été comparées aux
modifications de mouvements corporels
isolés et /ou volontaires. Une attention
toute particulière a été
apportée aux clignements des
paupières et à ceux pouvant
être cause d'artéfacts
d'enregistrement EEG.
Les bâillements sont
précédés et suivis, de
façon significative, par un accroissement
de l'activité delta enregistrée
sur l'EEG. Après le bâillement,
l'activité alpha décroit
d'amplitude et se ralentit, en parcourant
l'ensemble du cortex alors qu'après
d'autres mouvements corporels, ces ondes sont
atténuées et
accélérées. Une
accélération sigificative mais
fugitive de la fréquence cardiaque
apparait aussi bien après un
bâillement que d'autres mouvements; elle
est suivie d'un ralentissement 17s après
le début de l'accélération,
sans différence entre les
bâillements et d'autres mouvements.
Les bâillements apparaissent dans les
périodes d'augmentation de la sensation
de fatigue, de somnolence et de pression de
sommeil, mais il n'a pas été
trouvé qu'ils généraient
une augmentation mesurable du degré
d'éveil cortical. Ils ne sont ni suivis
ni générateurs d'une activation
autonomique spécifique. Ces
résultats confirment que les
bâillements sont dûs à la
somnolence mais il n'y a aucune preuve qu'ils
aient un effet éveillant.
Introduction Yawning is a stereotyped
sequence of respiratory and motor phenomena,
which is observed in a wide variety of animal
species, from fetal stages to old age [3,
32]. Although there is little doubt that
such a conspicuous and phylogenetically old
behaviour of ubiquitous occurrence must have a
biological origin and purpose, its prerequisites
and its function have remained unclear [3,
27, 32]. From the various hypotheses on the
physiology of yawning, two concepts have
remained in literature from the past to present
days.
The communication hypothesis states that
yawning is a form of unconscious communication
to synchronize the behaviour of a group [8,
12, 33]. Specifically, yawning was proposed
to communicate drowsiness [8, 12, 33],
psychological stress [12], and boredom
[27].
The arousal hypothesis suggests that yawning
has an arousing effect thereby keeping off
impending sleep [1, 3, 8, 21, 32].
Initially it was thought that this arousing
effect depended on changes in brain perfusion
with blood and oxygen. Albrecht
von Haller assumed in 1749, that "Yawning is
preceded by a slow-down in pulmonary blood flow,
" which leads to insufficient oxygen (O2) in the
blood, and therefore in the brain (cited in
[27]). In 1881, Russell
hypothesized that yawning may cause a
"stimulation of the brain through increased
activity of the circulation" (cited in
[3]). These notions reappeared later in
the concept of "critical consciousness" by
Montagu
[21], who suggested that a reduced state
of consciousness due to a rise in carbon dioxide
(CO2) in the brain is normalized by yawning.
Askenasy
[1] postulated that yawning is a
"complex arousal defence reflex (…), whose
aim is to reverse brain hypoxia. " However,
theories ascribing an important role to blood
gases in the physiology of yawning had to be
rejected after the experiments of Provine
et al. [25], who showed that healthy
subjects did not yawn more frequently when
breathing gas mixtures with high levels of CO2
or low levels of oxygen (O2).
However, the concept of an arousing function
of yawning remained in variants: Baenninger
[3] suggested "that an important
function of yawning is to modify levels of
cortical arousal, especially in situations where
there is little external stimulation, " and
Walusinski and
Deputte [32] postulated that the
function of yawning in humans as in animals is a
"stimulation of vigilance". The present study
aimed at empirically evaluating the functional
relationship between yawning and vigilance by
measuring electrophysiological markers of
vigilance in temporal association with
yawning.
Both hypotheses have in common that they
assume an important causal relationship between
spontaneous yawning and vigilance, and both
hypotheses predicted that we would find signs of
sleepiness before yawns. We therefore
specifically assessed theta and delta power in
EEG segments before yawns as markers of
drowsiness. The hypothesis of an arousing effect
of yawning additionally suggested that
significant activating effects would be
observable in the EEG or HRV after yawning. We
therefore analyzed alpha power and the mean
alpha frequency [5, 6] in EEG segments
after yawning as markers of the arousal level,
as well as HRV changes as markers of an
autonomic activation. In order to rule out
confounding effects of concomitant movements
during yawning, we additionally compared the
data obtained before and after yawning to EEG
and HRV measurements before and after isolated
voluntary body movements without yawning.
Discussion This study evaluated the
functional relationship between yawning and
vigilance by measuring indicators of the
cortical arousal level and of autonomic activity
before and after yawning, as compared to
isolated movements. Our findings demonstrate,
that yawning indeed occurs during progressive
drowsiness, which is compatible with the notion
that yawning is triggered by states of low
vigilance. In contrast, we were unable to
observe a specific arousing effect of yawning on
the brain or the autonomic nervous system. The
arousal hypothesis of yawning is therefore not
supported by our data. The prerequisites of
yawning When analyzing long-term EEG power
spectra, we found that central midline delta
power density was significantly greater before
and after yawns than before and after movements
(Table 2, Figures 1 and 2). Delta power is known
to increase with the duration of wakefulness and
to decrease during sleep, and is therefore
interpreted as an indicator of a sleep promoting
process [7].
In addition, delta band activity increases
in anterior and central 12 brain areas during
the transition from wakefulness to sleep and
shows a maximum over the fronto-central midline
during drowsiness [9, 10, 31]. Thus,
sleep pressure and drowsiness proved
significantly greater when subjects yawned than
when they moved only. This finding provides
strong evidence for the notion that yawns are
triggered by drowsiness, which is also in
agreement with previous behavioural studies
showing that yawning occurs most frequently
before and after sleep [18, 24]. In
contrast, several studies have observed an
arousal rather than drowsiness before chemically
or electrically induced yawns of anesthetized
animals. For instance, microinjection of
histamine [29], L-glutamate, or nitric
oxide releasing compounds [26] into the
paraventricular nucleus of the hypothalamus, or
electrical stimulation of the same structure
[26], evoked an arousal response in the
EEG or electrocorticogram, which was followed by
yawning after about 11 s. Yawning also occurred
during induction of anaesthesia in humans, where
it was found to be associated with an arousal
shift as indicated by an increased bispectral
EEG index, although this shift may have been
confounded by EMG artefacts [19].
The time range of 15 s before yawning
analyzed in our study was adjusted so that an
arousal of this type would have been detected.
The fact that spontaneous yawns were independent
of a previous arousal in our study shows that
arousal is not a prerequisite of spontaneous
yawning during wakefulness or drowsiness.
However, preceding arousals may be necessary for
yawns to occur in the non-physiological state of
anaesthesia. It is noteworthy that no
significant short-term EEG changes were observed
before or after yawning, which speaks against
any fast "reflex"- like [1] cortical
processes generating yawns. Furthermore, there
was no evidence for a significant autonomic
activity before onset of yawning, which might
have triggered the yawning process. Besides
central midline delta power, occipital slow beta
activity was also significantly greater in the
yawning condition than in the isolated movement
condition. Slow beta (i. e., spindle) activity
increases in frontal, central, and parietal
brain regions during the transition from sleep
stage 1 to 13 stage 2 [9, 30].
The significance of the observed difference
over occipital regions is, however, unclear. The
function of yawning Once it is established that
yawning occurs due to drowsiness, the next
question one has to consider is the function of
yawning itself. We studied the effect of yawns
and movements on the brain arousal level by
comparing long-term EEG power spectra after
yawns and movements to power spectra before
yawns and movements, respectively (Table 1,
Figures 1 and 2). First, it is important to note
that the increased delta power over the vertex
(electrode Cz) observed before yawning persisted
to the same amount also after yawning. Thus,
yawning did not reverse the increased sleep
pressure and drowsiness that seemed to have
triggered it. From studies assessing EEG power
changes during the transition from wakefulness
to sleep, it is known that alpha activity
decreases and moves in an anterior direction
along the midline of the scalp with increasing
drowsiness [9, 10, 30].
In contrast, increased arousal levels are
manifested by an acceleration and attenuation of
alpha oscillations in EEG [5, 6]. Here,
we show that yawns and movements were associated
with different power changes in the alpha
frequency band: whereas alpha rhythms were
significantly accelerated and attenuated by
movements, they were decelerated, shifted
towards central brain regions, and attenuated by
yawning (see Fig. 2). Furthermore, slow alpha
rhythms decreased significantly less after yawns
than after movements. Thus, isolated movements
seemed to have an arousing effect on EEG that
was qualitatively similar as &endash; but
quantitatively smaller than &endash; the effect
that can be observed 30 min after oral ingestion
of 250 mg caffeine [6]. In contrast,
yawning was associated with signs of a
decreasing arousal level. Both movements as well
as yawns were also followed by rather complex
changes in beta power density, the significance
of which remains unclear.
An influence of EMG artefacts is unlikely,
since increases as well as decreases in power
could be observed, and power changes were most
14 prominent over the vertex and occipital brain
regions where less motor artefacts would be
expected. In addition, great precautions were
taken to avoid artefacts. The effects of yawning
on autonomic activity was investigated by
calculating the heart rate variability before,
during, and after yawning, and by comparing the
results with the movement condition (Fig. 3).
Both yawns and movements provoked a transient
increase in HRV starting after the corresponding
EMG onset, followed by a slow decrease. However,
no difference between yawning and isolated
movements could be found at any time-point.
Thus, although an autonomic activation occurs
after the onset of submental muscle activity
induced by yawning, it is entirely unspecific
and obviously due to the movement rather than
the yawning as such. This is in fact not the
first study that is unable to find evidence for
an arousing effect of yawning.
When analyzing vigilance states of premature
human newborns before and after spontaneous
yawns, significant vigilance changes (mostly
from wakefulness to drowsiness) were found in
the time period before but not in the period
after yawning [16], which fits well with
our finding of yawning occurring during
progressive drowsiness, but not having an
arousing effect. Autonomic changes during and
after yawning as observed in our study have been
previously described in a study assessing the
muscle sympathetic nerve activity during yawning
in a single subject, and these changes were
found to be temporally related to respiration
[2].
An increase in skin conductance (indicating
autonomic activation) was reported during yawns
that were voluntarily produced by the examined
subject, but this increase could be observed to
the same extent when subjects only opened their
mouth or took a deep breath [17]. In
addition, a significant increase in the mean
heart rate was found only when subjects opened
their mouth or took a deep breath, but not
during the self-produced yawns [17].
Thus, although an autonomic activation was
indeed observed in several studies, it was
consistently found to be unspecific. In
contrast, the communication hypothesis of
yawning has received recent empirical support
from functional imaging studies, which showed 15
that watching other persons yawn provokes
specific activations of brain areas responsible
for social behaviour [28] or
self-processing [23].
One of the main arguments [3, 8] for
the concept of an arousing effect of yawning had
been the observation that motor activity was
significantly increased after yawns [4,
16]. In the light of our results, this
finding may be explained differently: the
yawning subjects try to reduce their drowsiness
by making body movements that indeed proved to
have an arousing effect in this study. Thus, the
increased motor activity observed after yawning
is not an indicator of an arousing effect of
yawning, but an effective countermeasure against
the underlying drowsiness.
A further argument [3] for an
arousing effect of yawning was based on the
observation that yawning occurs frequently
before going to bed, but not anymore when the
subjects are actually lying in bed waiting to
fall asleep, thus at a moment when drowsiness is
expected to be greatest and no arousal is
required [4]. However, this observation
may just as well be explained by the
communication hypothesis, by stating that
yawning is a non-verbal signal to go to sleep
when drowsiness occurs, which is obviously no
longer needed when already lying in bed.
One might argue that the lacking empirical
support for the arousal hypothesis is due to
inherent methodological problems in the
assessment of vigilance and of yawning itself.
Thus, it might be suggested that yawning
provokes an arousal in certain brain areas that
are not accessible by measurements of EEG, HRV,
and skin conductance. However, vigilance changes
are typically manifested diffusely over the
whole brain rather than in a restricted area,
and we used the EEG electrode locations that are
most sensitive to them (Cz). Furthermore, we
were able to detect an arousing effect of
voluntary body movements, which shows that the
methodology was indeed capable of detecting
relevant brain activations.
A further criticism might refer to the
rather short time window of 10 s after yawning
that was analyzed in our study, and postulate
that the arousing effect of yawning occurs
later. However, our data not only demonstrates a
lacking increase of the arousal level, but even
a decrease of the arousal level after yawning.
Even if one assumed a reversal of this trend
after 10 s, one still 16 would have to explain
the advantage of yawning over simple body
movements, which proved to have a much faster
arousing effect. Finally, one might object that
some earlier studies assessed self-produced
[17] or chemically induced yawns
[19, 26, 29] rather than spontaneous
yawns, which might have a different physiology,
and this study analyzed mostly patients rather
than healthy subjects, for which reason the
results may not reflect the physiological
mechanisms of yawning.
However, none of the subjects included in
our study suffered from a condition which might
provoke pathological yawning (see Methods), and
the increased sleepiness present in the examined
patients is hardly sufficient to fundamentally
alter a phylogenetically old behaviour such as
yawning.
On the contrary, one can expect that, if
yawning indeed had an arousing effect, its
physiological function would have been maximally
challenged in our setting. In conclusion, having
found no empirical evidence for an arousing
effect of yawning, and in the absence of
convincing arguments against the validity of the
available data, we advocate a rejection of the
arousal hypothesis of yawning as stated
above.
In contrast, our findings are compatible
with the communication hypothesis.
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