Olivier Walusinski (Ed.): The Mystery of
Yawning in Physiology and Disease
Karger, Basel, 2010, 160 pp
Review in
the Journal "Primates" by Akiehika Mikami
pdf
Yawning is a stereotyped phylogenetically
ancient phenomenon. The editor says in the
Forward, "Yawning is a stereotyped and often
repetitive motor act characterized by gaping of
the mouth accompanied by a long inspiration,
followed by a brief acme and a short expiration.
It is not merely a simple opening of the mouth,
but a complex coordinated movement bringing
together a flexion followed by an extension of
the neck, a wide dilatation of the
laryngopharynx with strong stretching of the
diaphragm and anti-gravity muscles." Although
yawning is not a simple motor action but complex
coordinated movements, it is highly
stereotypical and can be observed in almost all
vertebrates, including cold-blooded and
warm-blooded, from reptiles with rudimentary
"archaic" brains to human primates, in water,
air, and land environments. Yawning is a
mysterious but fascinating physiological
phenomenon, nevertheless, it has so far been
poorly addressed in the field of bioscience.
This is probably the first scientific book on
yawning.
Chapters 1 and 2, about historical
perspectives and popular beliefs about yawning,
are written by O. Walusinski,
the editor himself. The written history of
yawning started when the Greek medical
scientist, Hippocrates in 400 BC wrote "Yawning
precedes a fever, ...the accumulated air in the
body is violently expelled through the mouth
when the body temperature rises". It is
interesting to see the similarity of his view to
the hypothesis presented by Gallup in the later
chapter of this book, "The Thermoregulatory
Behavior". In 1755, Dutch author, Gorter
attributed yawning "to a need for faster
blood circulation and to cerebral anemia" and
this was a start of the idea repeated by many
authors: yawning improves brain oxygenation. The
history of scientific hypotheses and general
beliefs are both fun to read, to learn how
people treated yawning.
Chapter 3, written by F. Giganti
and P. Salzarulo, and Chapter 4, written
by O. Walusinski,
are about yawning during development. Studies of
yawning during the gestational age became
possible with significant advances in the image
quality and resolution of ultrasound 3D and 4D
technology. Yawning starts in fetuses of 12-14
weeks' gestational age. In preterm infants, the
number of yawns decreases between 31 and 40
weeks' postconceptional age, mainly during the
day. Analysis of the yawning behavior of the
fetus cannot support the popular belief that
yawning is a response to elevated CO2 or
depressed 02 levels in the blood. Recognition of
fetal yawning rather helps to verify the
harmonious progress of brainstem maturation and
to appreciate the neural underpinnings of the
sleep and arousal systems. It is important to
know that, in babies, yawning is often an
isolated event not yet organized into consistent
bursts and rarely accompanied by the stretching
seen in adults. During the first stage of
development only spontaneous yawning is present,
and contagious yawning is only observed from 4
to 5 years of age. The incidence of yawning
seems to increase when children attend
elementary school.
Chapter 5, written by F. Giganti
et al., and Chapter 6, written by A. G.
Guggisberg et al.,
are about the correlation of yawning with sleep
or vigilance. The frequency of yawning is higher
before sleep onset. It increases progressively
during the 3 h period preceding sleep. The time
of sleeping also affects yawn production:
evening types yawn more frequently than morning
types. Thus the relationship between yawning,
sleep, and sleepiness seems evident. ERG studies
have provided evidence that yawning occurs
during states of low vigilance. However, yawning
did not result in specific autonomic activation
or increased arousal levels. Thus the EEG data
did not support an arousing effect of yawning or
a role in regulation of vigilance or autonomic
tone.
Chapter 7, written by W. Seuntjens,
discusses the hidden sexuality of the yawn.
According to this author, an erotic and sexual
aspect of yawning can be seen in linguistics,
social ethnology, psychology, ethology,
pathology, pharmacology, even in the arts.
Yawning can be linked with arousal, ejaculation,
and orgasm. In dogs, yawning can be associated
with penile erection. In heroin-withdrawal
syndrome, yawning and spontaneous sexual
response are associated.
Chapter 8, written by J. R. Anderson,
and Chapter 9, written by A. Moyaho
and J. Valencia, are about animal yawning. In
Chapter 8, Anderson discusses three aspects of
yawning in non-human primates. The first is
yawning as communication. Yawning has been
described as an expression of passion and anger
in Old World monkeys. Several lines of evidence
link the frequency of yawning in adult male Old
World monkeys to dominance rank. Yawning could
be actively inhibited during the male-male body
contact phase of an encounter, and physical
separation between the males switched off the
inhibitory effect and thereby permitted a
"tension component" to be expressed in the form
of yawning. The second topic is voluntary
control of yawning. Anderson provides evidence
of the ability of adult male macaques to
voluntarily control yawning. The third topic is
contagious yawning. According to Anderson
evidence of contagious yawning in non-human
primates is not compelling and he concludes that
the chimpanzees have little need to catch up on
yawning, they show little susceptibility to the
contagious yawning effect. It can be seen only
when some form of extra yawning stimulation is
given to chimpanzees, for example in the form of
repeated video or animated images. In Chapter 9,
Moyaho and Valencia discuss the modulation of
yawning by punishment-induced fear in rats. The
author suggested a tendency for yawning to
increase in response to mild stress. He also
suggested a delaying effect of punishment.
Chapter 10, written by A. C.
Gallup, is about
thermoregulatory behavior. Yawning frequently
occurs in the evening, when brain temperature is
at its peak, and upon waking, when brain
temperature begins increasing from its lowest
point. Yawning in the early morning may be a
compensatory thermal stabilizing mechanism.
Chapter 11, written by G. T.
Collins
and J. R. Eguibar, is about the
neuropharmacology of yawning. Two hormones,
adrenocorticotropic hormone (ACTH) and
alpha-melanocyte-stimulating hormone (alpha-MSH)
are known to be related to yawning. Yawning is
abolished by hypophysectomy, and microinjection
of ACTH into several hypothalamic nuclei will
induce yawning. In addition to these hormones,
yawning can be regulated by various
transmitters, including acetylcholine, dopamine,
glutamate, serotonin, oxytocin, GABA, opioids,
adrenergics, or nitric oxide. Despite the great
advances that have made towards our
understanding of the neuropharmacologic
regulation of yawning, further studies are
needed to fully elucidate how these
neurotransmitter systems interact with each
other, and the specific receptor subtypes and
brain regions involved in the induction and
inhibition of yawning.
The next three chapters are about contagious
yawning. In Chapter 12, S. M Platek,
on the basis of animal studies and human Mill
studies, suggests that contagious yawning may be
an evolutionarily old process that begat a
higher level of social cognition in some
species. He writes "contagious yawning is a
vestigial fixed action pattern that may be a
glimpse into the neurobiological substrates that
gave rise to more sophisticated social cognitive
processes such as theory of mind". In Chapter
13, A. Senju discusses the atypical
development of contagious yawning and the
results of animal experiments. He concludes that
contagious yawning shares its mechanism with the
capacity for theory of mind. He also suggests,
on the basis of his observation of autistic
children, that spontaneous orientation to
socially relevant stimuli, for example eyes, may
mediate contagious yawning in humans. In
Chapter 14, M. W. Campbell and F. B. M de
Waal discuss methodology to study contagious
yawning. They point out that different
researchers analyze their results differently
and suggest more rigorous, thorough, and
informative analyses. They raise awareness of
these issues to generate new experiments and
improve discussion of existing research. The
contagious yawning of nun-human primates was
also discussed in the previous chapter.
Chapter 15, written by F. B. Nahab,
is about neuroimaging of yawning. The
ventromedial prefrontal cortex (vmPFC) is a
unique brain area activated when human subjects
view videos of yawns, compared with the
condition when subjects viewed other facial
expressions. The author's group did not find any
significant activation in the so-called "minor
neuron system". The vmPFC has been associated
with emotional processing of internal and
external stimuli and representation of emotional
responses. Thus vmPFC seems a reasonable
candidate as the brain region associated with
viewing contagious yawning. On the other hand,
yawning is the motor act. The weak point of this
type of study is that the subject is lying down
in the MR machine without any motion and just
looking at the video of yawning.
Chapter 16, written by R.
Meenakshisundaram et al., and Chapter 17,
written by O. Walusinski, are about clinical
aspects of yawning. Meenakshisundaram et al.
introduce movements of hemiplegic limbs
associated with yawning. They suggest that the
appearance of associated movements in hemiplegic
limbs indicates the return of ancestral function
observed in quadrupeds. Walusinski discusses
disorders of yawning, for example disappearance
of yawning, excessive yawning, or
yawning-triggered disorder. Some extrapyramidal
syndromes including Parkinsons' disease are
accompanied by disappearance of yawning.
Dyspepsia, migraine, stroke, hypertension,
epileptic seizure, hypothalamic-pituitary
disorder and some drug use can cause excessive
yawing.
As seen in the chapters of this book,
yawning has many aspects and it is very complex.
We need to try various approaches to study
yawing. I will suggest several points for future
research on yawning. Yawning can be seen in all
vertebrates and can be seen at the gestational
age. Neural structures involved in yawning may
be subcortical systems including the
hypothalamus. Thus, yawning is phylogenetically
and ontogenetically old behavior. However, in
this book, direct comparison of yawning behavior
among vertebrates is missing. I believe that it
is important to study primitive vertebrates, for
example reptiles. The primitive vertebrates
could be a good target to study the core neural
structures and the original function of yawning.
It is necessary to clarify the common parts and
difference of yawning behavior in lower and
higher vertebrates. The correlation with sleep
or sleepiness may be evident in human subjects
but this kind of correlation must be tested in
lower animals also. In higher animals, higher
brain functions or cortical functions can be
combined with the core function of yawning. It
is also necessary to compare yawning behavior
across species in higher animals. Contagious
yawning is one possible phenomenon that appeared
as a result of such integration. For this
purpose, as Campbell and de Waal suggested, we
need to pay attention to standardizing methods
to enable comparison of different studies. To
study brain functions in human subjects, it is
necessary to conduct imaging studies during
yawning behavior. Imaging studies using MRI,
PET, or MEG are not suitable for this purpose.
We should try other methods, for example EEG,
MRS, or SPECT for this purpose. Anyway, this
book is standing at the entrance of these
studies and is a good book for gaining insight
for future studies of yawning.
