Psychology Research Centre,
Bournemouth University, UK
Abstract
Yawning apparatus and exact location of the
yawn reflex remains controversial. Yet yawning
is a significant behavioural response and
potentially a new diagnostic marker of
neurological disease. Association between
cortisol, electromyography (EMG) and yawning was
found in humans supporting Thompson Cortisol
Hypothesis (TCH) which complements
thermoregulation hypotheses indicating brain
cooling occurs when yawning. 28 male, 54 female
volunteers, 18-69 years, randomly allocated to
experimentally controlled conditions of provoked
yawning. Saliva samples were collected at start
and after yawning, or after stimuli
presentation, in absence of yawning. EMG data
was collected from jaw muscles at rest and after
yawning. Specially designed yawning
susceptibility scale, Hospital Anxiety and
Depression Scale, General Health Questionnaire,
demographic, health details were collected.
Between- and within-subjects comparisons of
yawners and non-yawners was conducted. Exclusion
criteria: chronic fatigue, diabetes,
fibromyalgia, heart condition, high blood
pressure, hormone replacement therapy, multiples
sclerosis, stroke. Yawning group: significant
difference between saliva cortisol samples, rest
and yawning t (37)=2.842, p=0.007, compared with
non-yawners, rest and post-stimuli, which was
non-significant. Yawners, rest EMG: -100 to 200
millionth of a volt (mean=182.2) and -60 000 to
18 000 (mean=3 897.4) after yawning.
Non-yawners, rest EMG: -80 to 120 (mean=37.2)
and -400 to 800 (mean=57.5) after stimuli
presentation. Yawners showed larger peak
following yawn compared with post-stimuli for
non-yawners. Significant supporting evidence for
TCH suggests cortisol levels are elevated during
yawning. Changes in cortisol levels may become a
new diagnostic tool in early diagnosis of
neurological symptoms.
Résumé
Les mécanismes intimes du
bâillement et la localisation
cérébrale exacte de son origine
restent controversés. Pourtant, le
bâillement est une réponse
comportementale importante et potentiellement un
nouveau marqueur diagnostique de maladies
neurologiques.
Cette étude, associant celle des
niveaux du cortisol et
l'électromyographie (EMG), a
montré son intérêt chez
l'homme pour valider la théorie
cortisolique du bâillement (Thompson
Cortisol Hypothesis - TCH). Celle-ci
complète les hypothèses de
thermorégulation retrouvant un
refroidissement du cerveau lors du
bâillement.
28 hommes et 54 femmes volontaires, de 18
à 69 ans, répartis de façon
aléatoire, ont participé à
une étude contrôlée de
bâillements provoqués. Des
échantillons de salive ont
été prélevés au
début et après le
bâillement, ou après la
présentation de stimuli, en l'absence de
bâillement. Les données EMG ont
été recueillies au niveau des
muscles de la mâchoire au repos et
après le bâillement.
Une échelle de susceptibilité
aux bâillements a été
spécialement conçue,
l'anxiété a été
appréciée à l'aide de
l'échelle 'Hospital and Depression
Scale', un questionnaire général
sur la santé rempli, ainsi que des
renseignements d'identification.
L'étude a comporté des
comparaisons entre bâilleurs et non
bâilleurs. Les critères d'exclusion
étaient la fatigue chronique, le
diabète, la fibromyalgie, les maladies
cardiaques, l'hypertension artérielle, le
traitement substitutif hormonal, la
sclérose en plaques, les
antécédents d'accidents
vasculaires cérébraux.
Des différences significatives ont
été retrouvées entre
bâilleurs et non bâilleurs. Les
bâilleurs ont présenté un
pic du niveau de cortisol plus important que les
non bâilleurs ce qui confirme
l'hypothèse d'une élévation
du cortisol lors du bâillement. Les
changements dans les niveaux de cortisol
pourraient devenir un nouvel outil de diagnostic
précoce lors de certains symptômes
neurologiques.
Thompson
Cortisol Hypothesis : all the
publications
Introducion
The first yawn of the day is usually when we
awake to stretch our intercostal muscles
surrounding our lungs to bring in more oxygen.
Many of us recognise yawning as a sign of
tiredness or boredom yet we also yawn before
that important job interview. We contagiously
yawn when our pets yawn and because we are
empathe c towards another yawning human being
and therefore, most of us can relate to
yawning.
Yet the physiological apparatus and exact
loca on of our yawning response is uncertain. So
much so, that yawning has been the debate of
neuroscien sts and philosophers since 400 BC
when Hippocrates wrote about yawning in De
Flatibus Liber (A Trea se on Wind), "because the
large quan ty of air ascends all at once, li ing
with the ac on of a lever and opening the mouth,
the accumulated air in the body, like steam
escaping from hot cauldrons, is violently
expelled when the body temperature rises"
[1].
Hippocrates' theory was not so far from
reality but the focus of the study of yawning on
is on our body temperature which is lowered when
we yawn and thus protec ng us from cri cal brain
temperature rises especially when we become very
fa gued. A common symptom of mul ple sclerosis
(MS) is fa gue [2] which is also
associated with excessive yawning and a rise in
brain temperature, governed by a small structure
in the top of the brain, the hypothalamus
[3,4]
Temperature regulation and circadian rhythm
is the responsibility of the hypothalamus which
is in mately linked to two other body
structures, the pituitary gland, also situated
in the brain, and the adrenal glands which
secrete adrenaline. The hypothalamus-
pituitary-adrenal (HPA) axis helps us produce
enough hormones to protect against stress and
provides us with readiness for physical
activity.
Yawning is exhibited in many different
situations and it is because of this that it has
made yawning so difficult to research resulting
in its origin being so allusive. Anecdotally,
yawning has been seen in response to migraine
headaches; following excessive fatigue or
sleepiness [5]; after ingesting "magic
mushrooms" whose active ingredient is
psilocybin; following taking the antidepressant
Prozac; after an anxiety or panic attack; after
seeing images of animals and humans yawning;
after reading an article about yawning !
The link between excessive yawning and
neurological disease has been noted elsewhere.
For example, Lana-Peixoto, et al. [6]
found that excessive yawning was the presenting
symptom of five patients with neuromyelitis
optica spectrum disorders (NMOSD). Brain MRI was
abnormal and most frequently showed brainstem
and hypothalamic lesions. The authors conclude
that pathological yawning may be a neglected
although not a rare symptom in NMOSD.
Excessive yawning is also noted in adrenal
insufficiency [7]; this is thought to
occur because of an irregulation of adrenaline
and cortisol, both actively involved in the
HPA-axis. It is probable that other neurological
diseases such as Parkinson's disease and Motor
Neurone Disease may also be implicated in the
HPA feedback loop.
The Thompson Cortisol Hypothesis [8]
is the first evidence-based report that links
the naturally produced protective "stress"
hormone, cortisol, with yawning, and
demonstrates that cortisol rises when we
yawn.
Produced by the zona fasciculate of the
adrenal cortex within the adrenal gland
[7], it is suggested that the rise in
cortisol level triggers our yawning response.
Implications of this research are that yawning
is an important mechanism for controlling
hormone regulation and hypothalamus temperature
regulation.
Physicians working in the rehabilitation of
stroke patients have reported on significant
findings from yawning stroke patients
[9]. Sir Francis Walshe, a British
neurologist, first reported on patients with
lesions in the braintistem region who could
raise their paralyzed arm when spontaneously
yawning [10]. This has been evidenced
since and consistently, by others
[11-13] and particularly, in patients
with left hemiplegia, the yawning response has
been attributed to pseudobulbar syndrome
[14]. Swallow reflex and yawning have
been postulated to be temporally related in a
study that considered gape, smile and yawning
responses [15]. Participants were
observed to swallow directly after yawning;
again suggesting that the brain stem region
might be the commonality between both reflexes.
Findings supporting the presence of common
neuroanatomico-physiological pathways for
spontaneous swallows and yawning have also been
reported [16].
Mental Attribution Theory [17,18]
has been presented as the reason for us
contagiously yawning as we seem to be empathic
to others who yawn, especially when we perceive
our belonging to a particular social grouping
and yet it seems that yawning is so important to
our maintenance and regulation that it does not
wait un l we are born. In fact, it happens in
the womb [19].
Consistent reports have shown photographic
evidence of yawning in the foetus, reinforcing
the fact that it is one of the first crucial
developments we make. New-born babies yawn more
frequently than toddlers do, since sleep
deprivation increases the chances of us yawning
and makes us more susceptible to the effects of
stress and fatigue [20].
Yawning is not confined to humans either,
with most vertebrates experiencing yawning
perhaps because of the need to raise arousal and
the level of alertness. Universal yawning seems
to be found in vertebrates in association with
arousal but also with sleep, hunger and satiety
[21]. 'Emotional yawning' has been
reported in animals visiting the veterinary
surgeon, in elite athletes and actors before
performing, and in parachutists about to jump
[22].
From fMRI studies, communicative yawning,
such as in contagion, appears to involve the
frontal and parietal lobes, insula and amygdala
[23-25], and has been postulated to be
related to the mirror-neuron system
[26]. Interestingly, temperature
contagion has been evidenced in participants
observing and ra ng others whose hands were
immersed in ice cold water [27]. Hence,
it is possible that yawning and temperature,
seen to be linked in conditions such as MS, may
also be subject to contagion and empathy.
Regardless of the function of the yawn, it
is probable that the critical threshold level of
cortisol is reached because of fatigue, empathy,
or sleep deprivation, to elicit the yawning
response. Electromyography (EMG) activity in the
jaw muscles is increased which in turn regulates
the further production of cortisol and also of
adrenaline from the adrenal glands [28].
Feedback via the HPA-axis continues to regulate
cortisol and adrenaline production within the
closed loop.
Discussion
There are several interesting findings of
this study, which are consistent with the
Thompson Cortisol Hypothesis. Significant
difference in saliva cortisol levels for those
who yawned, between sample one and sample two,
were found, which lends support for the
hypothesis. No significant difference was found
for the non-yawners between saliva cortisol
sample 1 and sample 2. EMG activity also
increased with elevated cortisol levels and when
yawning.
Small (non-significant) rises in saliva
cortisol levels in the nonyawners (between rest
and post-stimuli) may be explained in terms of
the experimental procedure. Since two time
points of saliva cortisol sampling were taken
for both groups, it is possible that cortisol
levels rose for both groups in the presence of
yawnstimuli but for the yawners, cortisol levels
reached the threshold necessary for the
elicitation of a yawning response.
Previous studies have not consistently
focused on repeat sampling which provides the
advantage of indicating change in cortisol
levels.
Neurological diseases are complicated
because they present with different ranges of
symptoms and severity. However, it is intriguing
that diseases are often exacerbated by stress
and thus by fluctuation in cortisol and
adrenaline levels. Since both naturally
occurring hormones are involved intimately in
the body's HPA-axis, it is probable that they
also play a part in regulating the effects of
neurological disease. Other researchers have
alluded to the fact that a common symptom in
several neurological conditions and diseases is
excessive yawning.
For example, in multiple sclerosis, fatigue
often gives rise to excessive yawning together
with brain temperature rise3. In brain-stem
ischaemic stroke, patients who excessive yawn
are seen to execute an involuntary rise of their
affected "paralyszed" arm [11,13]. In
Parkinson's disease, it is has been long
considered to be effective to regulate serotonin
as well as dopamine levels, and it is possible
that cortisol levels may also have an
interaction with the overall homeostasis of
hormones [4,7,8]. The Thompson Cortisol
Hypothesis provides an explanation for excessive
yawning, and links cortisol with this reflex
behaviour. The extent to which they are involved
in each neurological disease and condition is
yet to be investigated.
It is understood that cortisol acts to
protect our body against stress and plays a role
in the regulation and balance of hormones
released within the HPA-axis. The yawn response
may give rise to an increase in cortisol levels
to provide symptom relief such as in lowering
brain temperature as proposed by Gallup
[3]. This may be the mechanism involved
in the excessive yawning of people with multiple
sclerosis via the hypothalamus as temperature
regulator.
To understand the extent to which brain
temperature may be regulated by the hypothalamus
would require temperature monitoring around the
surface of the skull together with induced fa
gue paradigms to discern threshold levels of
cortisol release. The author is leading a team
in the UK and in France (Université Paris
X Ouest Nanterre La Défense;
Hôpital Universitaire Amiens; and Jules
Verne Université de Picardie) to conduct
a series of fMRI studies involving people with
multiple sclerosis to analyse fatigue,
temperature moderation and yawning-cortisol
response. It is hoped that this with further our
limited knowledge of the complex yet intriguing
mechanism that we see as simply yawning.
Conclusions
Yawning and cortisol is of interest to
clinical scientists, practitioners, neurologists
and neuroscientists. Whilst still presenting a
scientific conundrum, it has presented as a
fascination for centuries but is now emerging
with potential clinical and neuro-scientific
importance, especially in the domain of
diagnostic biomarkers. Clearly, further research
is indicated; particularly, mapping the
frequency and variance in cortisol levels in
different neurological diseases. However, it is
fitting that this ancient mechanism, common to
most of us that has been reported for many
centuries, is perhaps a breakthrough for modern
neuroscience and rehabilitation.
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