-
- ABSTRACT
-
- Yawning is a stereotyped physiological
behavior that can represent a sign or symptom of
several conditions, such as stroke, parakinesia
brachialis oscitans, parkinsonism, Parkinson's
disease and epilepsy. More rarely, it can occur
in patients with intracranial hypertension,
brain tumor, multiple sclerosis, migraine,
Chiari malformation type I, and amyotrophic
lateral sclerosis. Drug-induced yawning is an
uncommon clinical condition and yawning in
patients with autism or schizophrenia is very
rare. The aim of this review is to describe in
detail the occurre Figure 1nce of the phenomenon
in such conditions, and its' phenomenology and
pathophysiology.
-
-
- RESUMO
-
- Bocejo é um comportamento
estereotipado fisiológico, o qual,
contudo, pode representar um sinal ou sintoma de
várias condições
neurológicas, tais como, acidente
vascular encefálico, incluindo a
parakinesia brachial oscitans, parkinsonismo,
doença de Parkinson, e epilepsia. Mais
raramente, o bocejo pode ocorrer em pacientes
com hipertensão intra-craniana, tumor
cerebral, esclerose múltipla,
migrânea, malformação de
Chiari tipo I, e esclerose lateral
amiotrófica. Bocejo-induzido por drogas
representa outra condição
clínica pouco comum. De outro modo,
bocejo é muito raro em pacientes com
autismo e esquizofrenia. O objetivo desta
revisão foi descrever em detalhes a
ocorrência deste fenômeno em tais
condições, sua fenomenologia e
fisiopatologia.
-
- Teive
HAG, Munhoz RP, Camargo CHF, Walusinski O.
Yawning in neurology: a review. Arq
Neuropsiquiatr. 2018;l76(7):473-480
- Walusinski
O. Le bâillement, un symptôme
oublié Neurologies
2010;13(132):428-433
- Walusinski
O. Yawning in diseases European Neurology
2009;62(3):180-187
- Walusinski
O. Associated Diseases. Front Neurol
Neurosci 2010;28:140-155
-
-
- Yawning is considered an intriguing and
fascinating phenomenon with an obscure
etiopathogenesis. It involves opening the mouth
wide and closing the eyelids while inhaling
deeply and then exhaling more briefly. A yawn
typically lasts 5-10 seconds and is usually
accompanied by retroflexion of the head and
sometimes by elevation of the arms (known as
pandiculation when occurring together). Human
beings yawn with a frequency of up to 28 times a
day, often after waking up and before falling
asleep. Yawning is frequently contagious and is
considered a sign of boredom or even
disrespectful behavior in the presence of
others. In the 19th century, Charcot considered
yawning an important clinical neurological sign,
but for many years neurologists attached little
importance to it. Nowadays, however, although
yawning continues to be a largely
under-appreciated behavior, chasmology, the
study of yawning, has become the focus of
considerable interest. The aim of this article
is to review yawning in neurology.
-
-
- METHODS
-
- A literature search was performed in Pubmed,
for English-language articles over the time
period from 1992 to 2018, using the terms
"yawning" and "CNS", "neurology", "neurologic
disorders". The initial references were selected
using the following main exclusion criteria: 1)
duplicate articles; 2) articles unrelated to the
purpose of the study; 3) articles unrelated to
yawning; 4) articles not including sufficient
relevant data.
-
- HISTORICAL
ASPECTS OF YAWNING
-
- Phylogenetically, yawning is a very old
behavior that can be detected in most
vertebrates from the fetal stages to old age.
Its meaning has been the subject of speculation
since antiquity. In some cultures, it has been
associated with Satan (Arab countries) and
spirits (India), while Hippocrates associated it
with apoplexy. In the Hindu world, yawning in
public is a religious offense. Since the 17th
century, various explanations for its meaning
have been put forward. Boerhaave, the founder of
clinical medicine, stated in 1680, that yawns
promote "the equitable distribution of spiritus
in all muscles and unblock the vessels". In the
18th century, yawning was believed to be
associated with the "improvement of brain
oxygenation" and, in the 19th century, it was
associated with different etiologies, including
hysteria, and considered a reflex. Curiously, in
1888, in his famous Leçons du Mardi
à la Salpêtrière, Charcot
discussed the case of a 17-year-old patient who
yawned eight times a minute, or 480 times an
hour, and only stopped when she went to sleep.
Her condition was believed at the time to be
associated with hysteria and oxygenation of the
nervous centers. She had generalized epileptic
seizures, complete anosmia and binasal
hemianopsia. She had been amenorrheic for a
year. Charcot's young patient was most likely
suffering from a prolactinoma compression of her
optic chiasma and her hypothalamus.
-
- During the 20th century, substantial
progress was made in understanding yawning, and
several studies on this behavior and
neurophysiology, hormones, dopamine receptors
and social behavior were carried out. Despite
this progress, yawning remains a mysterious and
fascinating physiological, or even pathological,
phenomenon.
-
-
- THE
NEUROPHYSIOLOGY OF YAWNING &endash; A
SUMMARY
-
- There are several hypotheses to explain
yawning: physiological hypotheses (such as the
respiratory and circulatory system, arousal,
sleepiness, thermoregulatory, ear-pressure and
state-change hypotheses) and the
social/communication hypothesis. In a study
published in 2011, Guggisberg et al. concluded
that the hypothesis best supported by
experimental evidence is the
social/communication hypothesis. In contrast,
Gallup argued, in 2011, that the
social/communication hypothesis is unattractive
and suggested that yawning is probably
multifunctional across species. In their view,
the most acceptable hypothesis in humans is the
thermoregulatory one, according to which yawning
is a brain-cooling mechanism.
-
- In 2014, Walusinski proposed a new
hypothesis, according to which yawning switches
the default-mode network to the attentional
network by activating cerebrospinal fluid flow.
The default-mode network is a set of
interconnected brain areas identified in
functional neuroimaging (fMRI) that exhibit
spontaneous physiological activity during the
normal resting state. There is a high level of
activity in the default-mode network when the
mind is not involved in specific behavioral
tasks, and a low level of activity during
focused attention. According to Walusinski's
hypothesis, yawning is a homeostatic process
that appears when the default-mode network is
active and sleepiness increases; yawning then
disengages the default-mode network to promote
the attentional network, which accelerates the
circulation of cerebrospinal fluid, increasing
clearance of somnogens such as adenosine,
prostaglandin D2, VIP, prolactin and anandamide,
and reducing sleepiness.
-
- The anatomic structures involved in yawning
have yet to be elucidated and, more recently,
fMRI has demonstrated that different levels of
the neuroaxis, including the brainstem,
prefrontal cortex and subcortical regions, may
be involved. In 2010, Collins and Eguibar
hypothesized that there are three main neural
pathways involved in the regulation of yawning.
Two of these are formed by groups of
oxytocinergic neurons projecting from the
paraventricular nucleus (one of the hypothalamic
nuclei) to the hippocampus, pons, medulla and
spinal cord; the other is formed by ACTH
(adrenocorticotrophic hormone) and
melanocyte-stimulating hormone-activated neurons
projecting from the paraventricular nucleus to
the hippocampus via activation of cholinergic
neurons. There is also direct activation of
hippocampal cholinergic neurons and a
serotonergic-cholinergic pathway. In summary,
several neurotransmitters and neuropeptides,
such as dopamine, acetylcholine, serotonin,
glutamate, GABA, adrenergics, excitatory amino
acids, nitric acid, ACTH-related peptides,
_-melanocyte-stimulating hormones and oxytocin,
seem to be involved biochemically in the
mechanism of yawning. Dopamine activates
oxytocin production in the paraventricular
nucleus of the hypothalamus, and oxytocin in
turn activates cholinergic transmission in the
hippocampus and the reticular formation of the
brainstem, resulting in acetylcholine induction
of yawning via muscle muscarinic receptors. In
general, dopamine and its agonists trigger
yawning, while opioid peptides and GABA reduce
its frequency. Yawning is used as an indicator
of dopaminergic and oxytocinergic transmission
and, in Parkinson's disease it is an expression
of therapeutic dopaminergic activity,
particularly as a marker of D3 dopamine receptor
activity.
-
- YAWNING &endash; A CONTAGIOUS
BEHAVIOR
-
- It is a popular belief that yawning is
contagious, and it is well known that watching
another person yawn may induce the person
watching to yawn too. According to Guggisberg et
al., who support the social/communication
hypothesis, contagious yawning is due to
activation of a complex network of brain areas
associated with imitation, empathy and social
behavior. In 2005, Schürman et al. studied
this intriguing phenomenon using fMRI. They
observed activation of the left periamygdalar
region, suggesting a connection between yawn
contagiousness and amygdala activation. In
contrast, Platek et al., using fMRI in 2005 to
study contagious yawning, showed activation of
the posterior cingulate and precuneus and, in
2009, Nahab et al., also using fMRI,
demonstrated activation in the ventromedial
prefrontal cortex, suggesting that mirror neuron
networks play a role in yawning. Since the
latter study, various papers on the relationship
between contagious behavior, such as yawning and
itching/scratching, and the activation of mirror
neurons and the neurological mechanism of social
behavior have been published. In 2014, Provine
stated that contagious behaviors such as yawning
have mirror-like properties.
-
- PHYSIOLOGICAL YAWNING
-
- Physiological yawning can occur during the
transition between wakefulness and sleep or vice
versa, or in response to fatigue, tiredness,
stress, overwork, lack of stimulation, hunger or
satiety. In general, it is associated with sleep
deprivation during the night and drowsiness
during the day and often occurs when people are
bored.
-
- YAWNING IN NEUROLOGICAL CLINICAL
PRACTICE
-
- Yawning may occur not only because of
boredom, drowsiness, or by contagion but also in
association with various diseases. Yawning is
termed pathological, abnormal, or excessive if
it is spontaneous, more frequent than generally
perceived as normal, compulsive, and not
triggered by appropriate stimuli including
fatigue or boredom. No consensus definition
exists concerning the frequency of yawns. A
recent recommendation adopted the abnormal
yawning frequency as three yawns per 15 minutes
to decrease the likelihood that two subsequent,
accidental yawns were counted as one episode
with abnormal yawning.
-
- Yawning can be present in the clinical
picture of several neurological diseases,
including stroke, multiple sclerosis,
neuromyelitis optica spectrum disorders,
parkinsonism, Parkinson's disease, migraine,
vasovagal syncope, brain tumor, intracranial
hypertension, Chiari malformation type I and
epilepsy, and can be induced by drugs.
-
- Yawning in sleep disorders
-
- In general, excessive yawning occurs more
frequently in patients with sleep disorders
(e.g., insomnia and sleep obstructive apnea) and
is most common in children and young
adults.
-
- Excessive yawning in clinical
conditions
-
- Other clinical conditions associated with
yawning are functional digestive disorders
(e.g., dyspepsia and irritable bowel syndrome),
motion sickness and hypoglycemia in diabetic
patients under insulin therapy. In addition,
vasovagal syncopal or presyncopal episodes
frequently present with yawning as well as
malaise, dizziness, visual obscuration, nausea,
pallor and loss of consciousness. Excessive
yawning has also been reported in patients with
depression and can be caused by the many
medications used in neurology, psychiatry and
internal medicine. This issue is discussed in
the following section.
-
- Drug-induced yawning
-
- Drug-induced yawning represents a rare and
frequently not very serious adverse side-effect.
Antidepressants, dopaminergic agents, opioids
and benzodiazepines are the main pharmacologic
classes associated with yawning. The most
widely-used antidepressants are serotonergic
agents (selective serotonin reuptake
inhibitors), including fluoxetine, paroxetine,
escitalopram, venlafaxine and duloxetine.
Dopaminergic drugs include levodopa,
dopaminergic agonists (pramipexole, ropinirole,
rotigotine and apomorphine) and monoamine
oxidase inhibitors. Blin et al. evaluated eight
healthy volunteers, in 1990, after they used
apomorphine and after a placebo, allowing 48
hours for the medication to be washed out. They
found that this dopamine agonist induced
blinking and yawning in all their participants.
Another interesting finding is the occurrence of
yawning in the withdrawal syndrome after
prolonged use of opioids or coffee. In 2007,
Sommet et al. studied drug-induced yawning
reported in the French Pharmacovigilance
Database between 1985 and 2004. They found 28
reports involving 38 drugs, especially
serotonergic agents, dopaminergic agents,
opioids, and benzodiazepines26.
-
- Yawning and stroke
-
- Yawning has been observed secondary to acute
hemorrhagic or ischemic anterior or posterior
circulation stroke. In general, it indicates
damage to the brainstem reticular formation and
cortical and subcortical structures. In 2006,
Cattaneo et al. published a case report of two
patients with pathological yawning as a
presenting symptom of brainstem ischemia
involving the upper pons and the
pontomesencephalic junction. Yawning has been
described in patients with locked-in syndrome
due to vertebrobasilar stroke caused by a
thrombosed megadolichobasilar artery. Another
potential cause of yawning in patients with
stroke is intracranial hypertension or even
herniation.
-
- More recently, Krestel et al. studied 10
patients with acute anterior circulation stroke
and yawning using neuroimaging (brain MRI with
diffusion-weighted images). They found a
correlation between ischemic lesions in the
insula and caudate nucleus and a period of
abnormal yawning and suggested that the insula
may be the main region of the brain responsible
for serotonin-mediated yawning. A rare and very
interesting clinical condition involving yawning
known as parakinesia brachialis oscitans is
related to stroke and will be described
below.
-
- Parakinesia
brachialis oscitans
-
- Occasionally, in patients with acute
hemiplegia, the onset of yawning is associated
with an involuntary raising of the paralyzed
arm. This phenomenon was named parakinesia
brachialis oscitans in 2005 by Walusinski et
al., who studied four cases and compared them
with other cases published in the literature
over the previous 150 years. Parakinesia
brachialis oscitans was probably first described
by Erasmus Darwin, the grandfather of Charles
Darwin, in 1794, in his book "Zoonomia of the
laws of organic life". In their seminal paper,
Walusinski et al. proposed a possible mechanism
for this abnormal involuntary movement. They
suggested that resection of the
cortico-neocerebellar tract of the
extrapyramidal system disinhibits the
spino-archeocerebellar tract, enabling motor
stimulation of the arm by the lateral reticular
nucleus, which has a link with respiratory and
locomotor rhythms. Several case reports have
since been published describing this phenomenon,
including others by Walusinski et al. and a few
other reports. In 2013, Zorzetto et al. also
published a case report of parakinesia
brachialis oscitans in the setting of
thrombolytic therapy (Figure 2). In 2015, Kang
and Dhand published a case report of a
63-year-old man who presented with an acute
ischemic infarct in the left middle cerebral
artery distribution, aphasia and paralysis of
the right arm, which consistently rose to his
chest when he yawned. After yawning, paralysis
always resumed. In a recent publication, Alves
et al. describe a patient who has voluntary
control over that movement.
-
-
- Figure 1.
Parakinesia brachialis oscitans in a patient
with right hemiplegia due to ischemic
stroke.
-
- Yawning, parkinsonism and Parkinson's
disease
-
- In general, yawning is used as an indicator
of activity of the dopamine-oxytocin pathway. In
patients with Parkinson's disease (PD), it is
associated with the presence of dopaminergic
activity and has been considered an aura for an
L-dopa-induced "on" state. It is very well known
that PD patients who receive apomorphine
injections (a direct D1/D2 dopamine receptor
agonist) frequently present with yawning before
positive motor effects, sometimes in association
with penile erections40. Yawning was described
by von Economo in patients with acute
encephalitis lethargica or postencephalitic
parkinsonism. Curiously, Sandyk et al.41
reported a series of five patients with
progressive supranuclear palsy (Richardson's
syndrome) who presented with balance deficits,
falls, oculomotor abnormalities and bursts of
repeated yawning without any correlation with
their dopaminergic treatment. In 2013, Giganti
et al. studied 18 untreated early-PD patients
and compared them with 18 age-matched healthy
controls. They showed that the circadian
distribution of yawning was not altered in
untreated patients with early-stage PD and
concluded that yawning is a behavioral marker of
sleepiness in de novo PD patients.
-
- Yawning and epilepsy
-
- Yawning can occur in different epileptic
syndromes. It has been described in the
peri-ictal period in children with infantile
spasms and in patients with temporal lobe
epilepsy (peri-ictal yawning preceding complex
partial seizures or yawning in the post-ictal
period). In 2011, Specchio et al. reported ictal
yawning in an adult patient with drug-resistant
focal epilepsy. Kuba et al. investigated the
incidence and lateralizing value of peri-ictal
yawning in patients with temporal lobe epilepsy
who had undergone surgery for epilepsy. They
observed peri-ictal yawning in 4.1% of 97
patients and, in 1.8% of these patients' 380
seizures, yawning occurred in the post-ictal
period. They also observed that peri-ictal
yawning occurred only in patients with
right-sided, nondominant temporal lobe epilepsy,
suggesting that it may have a lateralizing
value. Wasade et al. published an interesting
case report, in 2016, of a young male who
presented with controllable yawning expressed as
focal seizures of frontal lobe epilepsy. In
2012, Nicotra et al. discussed the case of an
elderly patient who presented with pathological
yawning as an ictal seizure manifestation.
-
- Yawning and intracranial
hypertension
-
- Some patients with intracranial
hypertension, brain swelling or herniation due
to stroke, head trauma or brain tumors may
present with yawning together with headache and
seizures. In 2014, Saura et al. described
intractable yawning associated with mature
teratoma of the supramedial cerebellum. Yawning
may also occur as a presenting symptom of Chiari
malformation type 1.
-
- Migraine and yawning
-
- Migraine represents a very common
neurological problem, and the pathophysiology of
migraine attacks has been shown to be related to
dopaminergic transmission. In the premonitory
phase, yawning can be present in association
with malaise, somnolence and mood changes among
other manifestations. Some migraineurs may
experience excessive yawning during the visual
aura before the attack. However, excessive
yawning in migraine can be improved with
dopamine receptor antagonists, which are
effective therapeutic agents for this
condition.
-
- Yawning, multiple sclerosis and
neuromyelitis optica spectrum disorders
-
- Some patients with multiple sclerosis (MS)
present with thermoregulatory dysfunction.
Therefore, sleep problems and yawning could be
symptoms of MS. Gallup et al. also showed that
yawning can provide symptom relief in MS
patients. In 1996, Postert et al. published a
case report on pathological yawning as a symptom
of MS and, in 2014, Lana-Peixoto et al.
described nine patients with neuromyelitis
optica spectrum disorders and excessive yawning
unrelated to sleep deprivation or fatigue. They
concluded that yawning may be a neglected
symptom in neuromyelitis optica spectrum
disorder.
-
- Yawning and amyotrophic lateral
sclerosis
-
- Yawning can be observed in patients with
amyotrophic lateral sclerosis (ALS). Williams
published a case report, in 2000, of a
64-year-old woman who presented with
progressive, very frequent yawning characterized
by bouts of 20 to 30 successive yawns in
association with painful cramping and a
sensation of choking. During the follow-up, the
patient developed bulbar palsy, and an
electromyogram confirmed the diagnosis of
amyotrophic lateral sclerosis. In 2007, Wicks
published a paper in which he noted that
excessive yawning is a common sign in the
bulbar-onset form of amyotrophic lateral
sclerosis.
-
- Yawning, autism and
schizophrenia
-
- Contagious yawning can be explained by the
relationship between yawning and social empathy.
Interestingly, in some psychiatric disorders,
such as autism and schizophrenia, yawning is
very rare. In 2007, Senju et al. evaluated 24
children with autism spectrum disorder and 25
age-matched, normally-developing children, in
terms of their frequency of yawning, using video
clips of either yawning or control mouth
movements. They concluded that contagious
yawning is impaired in autism spectrum disorder,
supporting the idea that contagious yawning is
based on the capacity for empathy. Haker and
Rössler, in 2009, compared changes in
yawning patterns in a group of 43 schizophrenic
patients and an age- and sex-matched group of
healthy controls using a video with sequences of
yawning, laughter and neutral faces. They
observed that schizophrenic patients showed a
significantly lower rate of yawning, suggesting
that susceptibility to contagious yawning is
reduced in patients with impaired social
empathy.
-
- Yawning &endash; problems and
solutions
-
- Yawning can sometimes cause complications,
such as mandibular subluxation, painful cramps
in the geniohyoid muscle and fracture of the
styloid apophysis. More rarely, it can trigger
an attack of glossopharyngeal neuralgia,
idiopathic carotidynia or even Marin Amat
syndrome, a form of acquired facial synkinesis
manifesting as involuntary eyelid closure on jaw
opening that often occurs following the aberrant
regeneration of the facial nerve after a
peripheral facial palsy. In contrast, yawning
can improve Eustachian tube dysfunction and
dysbaric facial paralysis and even acts as a
therapy for vocal fatigue. Gallup and Gallup
studied the frequency of yawning as an initial
signal of fever relief.
-
- CONCLUSION
-
- Yawning is a stereotyped physiological
behavior that can be a sign or symptom of
several neurological conditions, such as stroke
(including stroke with parakinesia brachialis
oscitans), parkinsonism and epilepsy. More
rarely, yawning can occur in patients with
intracranial hypertension, multiple sclerosis,
migraine and amyotrophic lateral sclerosis and
can be induced by drugs. It is rare in patients
with autism spectrum disorders or
schizophrenia.
-
-
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