-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.
Yawning is a phylogenetically old behaviour
that can be observed in most vertebrate species
from foetal stages to old age. The origin and
function of this conspicuous phenomenon have
been subject to speculations for centuries.
Here, we review the experimental evidence for
each of these hypotheses. It is found that
theories ascribing a physiological role to
yawning (such as the respiratory, arousal, or
thermoregulation hypotheses) lack evidence.
Conversely, the notion that yawning has a
communicative function involved in the
transmission of drowsiness, boredom, or mild
psychological stress receives increasing support
from research in different fields. In humans and
some other mammals, yawning is part of the
action repertoire of advanced empathic and
social skills.
1 Introduction Yawning can be
observed in most vertebrate species from foetal
stages to old age. In mammals, it consists of an
involuntary sequence of mouth opening, deep
inspiration, brief apnea, and slow expiration
(Walusinski and Deputte, 2004). It can be
accompanied by other facultative motor acts such
as stretching (Provine et al., 1987a). In
humans, yawns last on average about 6 seconds,
and the individual yawn duration and frequency
remains remarkably stable over weeks (Provine,
1986). In birds and fish species, a mouth gaping
similar to yawning can be observed, and yawning
as opposed to other forms of mouth openings has
been defined as a slow opening of the mouth,
maintenance of the open position for more than 3
s, followed by a more rapid closure of the mouth
(Baenninger, 1987). The homology of yawning
between different species is controversial, but
at least similar movement sequences and similar
conditions of occurrence can be observed
(Baenninger, 1987; Deputte, 1994). Since yawning
seems to be a phylogenically old and frequent
phenomenon, one would expect that it provides
some evolutionary advantage, i.e., that is has a
certain useful function.
Indeed, numerous hypotheses on the function
of yawing have been posited throughout the
centuries. They were usually derived from
behavioural observations of yawns. In mammals,
it has been observed that more than 90% of yawns
occur at rest whereas the remaining yawns seem
to be triggered by social or emotional stimuli.
These contextual differences have motivated a
classification of yawning into "physiological"
and "social" yawns, although the phenomenology
of yawns does not depend on the context
(Deputte, 1994; Walusinski and Deputte, 2004).
In accordance with the distinction of
physiological and social yawn contexts, the
hypotheses on the function of yawning have
emphasised either a physiological or a social
role of yawning.
In contrast to the abundance of theoretical
considerations, experimental data is relatively
scarce. Yet, in the last few decades, an
increasing number of studies have shed some
light on its conditions and effects. Although
the available data is still far from providing a
complete or generally accepted account of the
mechanisms and consequences of yawning, it does
allow confronting some of the theoretical models
with empirical observations. In this review, we
will try to classify existing hypotheses
according to their current experimental
evidence. All hypotheses postulating a
physiological role of yawning share the common
assumption that yawning regulates a particular
body function, e.g., the blood oxygen level or
the brain arousal level. Thus, the mechanisms of
yawning are characterised as a homeostatic
system with negative feedback regulation.
Accordingly, physiological models necessarily
make at least two different predictions that can
be empirically tested: i) yawning is triggered
by up- or downturns of a given body state and,
ii) yawning acts on the corresponding body
function. We will therefore review the evidence
of each physiological hypothesis based on its
predictions with regards to triggers and effects
of yawning. In the case of social models of
yawning, the postulated regulating function of
yawning would not concern body functions of
individuals but rather the communication within
social groups. The predictions of this model as
well as the corresponding evidence will also be
reviewed. This article will focus on normal
yawning; a recent review on pathological yawns
can be found elsewhere (Walusinski, 2009).
2 Anatomy and Pharmacology ....
3 Physiological Hypotheses
3.1 Respiratory and Circulatory
Hypotheses For several centuries, at least
since Hippocrates in the 4th century BC,
scholars have thought that yawning might remove
"bad air" from the lungs and increase oxygen
circulation in the brain (Trautmann, 1901;
Schiller, 2002; Matikainen and Elo, 2008).
3.1.1 Oxygen Need and Hypercapnia Do Not
Induce Yawning This hypothesis predicts that
yawning is triggered when blood or brain
oxygenation is insufficient, i.e., when oxygen
(O2) levels drop and the CO2 concentration
rises. However, from self-observation most
people will confirm that they do not yawn more
frequently when they do exercise and need more
oxygen than when they are at rest (Provine et
al., 1987b). In accordance with this notion,
experiments by Provine et al. (Provine et al.,
1987b) demonstrated that healthy subjects who
are exposed to gas mixtures with high levels of
CO2 or physical exercise, do not yawn more
frequently. .........
Taken together, the occurrence of yawning
during periods with too much blood oxygenation
but not during periods with oxygen need is
exactly the opposite of what would have been
predicted by the respiration hypothesis and thus
casts severe doubts on its correctness.
3.1.2 Yawning Does Probably Not Increase
Brain Oxygenation There are, to our
knowledge, no studies that measured the change
in blood oxygenation induced by yawning.
However, yawning would be a much less effective
way of increasing oxygen intake than rapid
breathing, especially since the deep inspiration
during yawning is followed by a period of
relative apnoea (Baenninger, 1997).
........
3.1.3 Conclusions The predictions of the
respiratory hypothesis are not supported by
current experimental data. Additional research
is needed to test the effects of hypoxia on the
yawning rate under more controlled conditions.
Studies investigating the effects of yawning on
blood and brain ygenation are also missing.
Given current evidence, it seems unlikely that
yawning has respiratory or circulatory
functions.
3.2 The Arousal Hypothesis The idea
that yawning might play an important role in
regulating physiological brain processes has
remained in the literature also after the
appearance of evidence against the respiratory
hypotheses. A widely expressed proposition now
speculated that yawning might be responsible for
the homeostatic regulation of vigilance and
brain arousal level (Baenninger, 1997; Giganti
et al., 2002; Walusinski and Deputte, 2004;
Matikainen and Elo, 2008; Vick and Paukner,
2010).
3.2.1 Drowsiness Induces Yawning
Yawning occurs preferentially during periods of
drowsiness, as it is predicted by the arousal
hypothesis. Behavioural studies consistently
reported that yawns occur most frequently before
and after sleep, i.e., during periods with lower
levels of alertness (Greco et al., 1993; Provine
et al., 1987a). The circadian distribution of
yawns precisely reflects the individual
sleep-wake rhythm (Giganti et al., 2007; Zilli
et al., 2007; Zilli et al., 2008).
....
Thus, sleep pressure and drowsiness proved
significantly greater when subjects yawned than
when they moved only.
3.2.2 Yawning Does Not Produce an
Arousal Arousals are defined as a global
activation of brain activity that progresses
from brain stem structures to centres of the
autonomic nervous system and to distributed
cortical areas (Moruzzi and Magoun, 1949; Sforza
et al., 2000). They are accompanied by a typical
acceleration of EEG activity. Several studies
have therefore analyzed spectral EEG changes
after yawns in humans to test the hypothesis
that yawning has an arousing effect. However,
the results were negative. Two studies looking
at 30 s samples of EEG before and after yawns
were unable to find significant and lasting
changes in EEG activity related to yawns (Laing
and Ogilvie, 1988; Regehr et al., 1992). One of
these studies reported transient increases in
theta, spindle, and beta activity, but they only
reached significance when the analysis was a
priori limited to data segments between 10 and
20 s before and after yawning (Regehr et al.,
1992). Furthermore, EEG power after yawning was
not significantly different from EEG power after
postural adjustments without yawning (Laing and
Ogilvie, 1988). In our analyses of EEG power
spectra from patients undergoing MWTs, we
observed that the increase in delta power over
the vertex that was found before yawning (as
compared to delta activity before postural
adjustments without yawning, see 3.2.1 above)
persisted to the same amount also after yawning
(Fig. 1, right panel). Thus, yawning did not
reverse the increased sleep pressure and
drowsiness that seemed to have triggered it.
Besides delta power, alpha oscillations (~ 7.5 -
12.5 Hz) also reflect the individual vigilance
level. They become faster and smaller in
amplitude when the arousal level increases.
Figure 2A gives an example of the EEG power
spectrum 30 min after oral ingestion of 250 mg
caffeine (Barry et al., 2005). In contrast,
drowsiness is associated with a slowing of alpha
oscillations, and with a shift of alpha
oscillations from mainly occipital towards
central brain regions (Tanaka et al., 1997; De
Gennaro et al., 2001b; De Gennaro et al.,
2001a). Figure 2B shows that alpha power after
yawning showed a pattern that is typical for
sleepiness: alpha rhythms decelerated, and
shifted towards central brain regions after
yawning, as compared to the data segments before
yawning. Conversely, we did observe EEG markers
of increased arousal levels after simple
postural adjustments, as shown in Figure 2C:
alpha rhythms became faster and smaller after
body movements. Hence, if yawning had an
arousing effect &endash; even if it were as
small as the effect of simple postural
adjustments &endash; we would have detected it
with our EEG analyses. Instead, we observed
signs of progressive drowsiness after
yawning.
........
3.2.3 Conclusions The experimental data
suggests that yawning indeed occurs during
progressive drowsiness, which is compatible with
the notion that it is triggered by states of low
vigilance. However, no specific arousing effect
of yawning on the brain or the autonomic nervous
system could be observed. Experimental evidence
therefore suggests a rejection of the arousal
hypothesis. The absence of an arousing effect of
yawning does obviously not exclude that it might
have some other form of activating function on
brain metabolism or neuropharmacology, but these
effects should not be named arousal.
3.3 The Sleepiness Hypothesis Rather
than attributing an arousing effect to yawning,
some authors have suggested that it might lower
the arousal level (Deputte, 1994). Studies
assessing the arousal level after yawing have
indeed found signs of decreasing wakefulness
(see section 3.2.2 above), which would be
compatible with this notion. However, the
observations could simply represent the
drowsiness underlying yawning that continues to
progress also after yawning. Thus, there is no
established causal link between yawning and
subsequent drowsiness. Moreover, if yawning had
a soporific effect apart from being induced by
drowsiness, it would be a self-reinforcing
mechanism and would need to be controlled by
other processes in order to ensure stability of
the sleep-wake balance.
3.4 The Thermoregulation Hypothesis
Recently, another physiological function of
yawning has been proposed: the regulation of
brain temperature. It is postulated that yawning
might cool down the brain when its temperature
increases. The advocates of this model give a
detailed description of their arguments in
(Gallup and Gallup, Jr., 2008). Here, we provide
a brief critique of the corresponding
experimental evidence.
3.4.1 Does Brain Hyperthermia Trigger
Yawning? .......
The same concern also applies to a second
study of the same group performed in birds which
were exposed to different ambient temperature
conditions. A rapidly increasing room
temperature was associated with more frequent
yawns than relatively stable cold or warm
temperatures (Gallup et al., 2009), which may
again be due to uncontrolled factors such as
differences in drowsiness or related to rapidly
changing vs. stable temperatures. The proponents
of the thermoregulation hypothesis also advance
anecdotal data of yawning frequency in patients
with different brain diseases, but in the
absence of direct comparisons and controls, the
evidence remains inconclusive.
3.4.2 Yawning Does Probably Not Cool Down
the Brain The greatest challenge for the
proponents of the thermoregulation hypothesis
lies in demonstrating how yawning would be able
to cool down the brain. It is suggested that the
inflow of cool air during yawning ventilates
heat off the brain. However, the proposition
faces similar problems as the respiratory
hypotheses discussed above. Yawning actually
interrupts normal nasal breathing which seems to
be a more efficient way of ventilation.
3.4.3 Conclusions There is currently
insufficient evidence for a thermoregulatory
effect of yawning. The thermoregulation
hypothesis seems to be counterintuitive and has
important explanatory gaps which seem to be
difficult to close.
3.5 The Ear Pressure Hypothesis
Yawning has the much appreciated capacity to
equalize air pressure in the middle ear with
outside air pressure. It can thus relieve
discomfort in the ear and hearing problems due
to rapid altitude changes in air planes or
elevators. This is achieved through contraction
and relaxation of tensor tympani and stapedius
muscles during yawning, which results in an
opening of the Eustachian tubes and the aeration
of the tympanal cavities (Laskiewicz, 1953;
Winther et al., 2005). This observation has led
to the postulation that yawning might be a
"defence reflex" of the ear, which is triggered
by rapid altitude changes or other conditions
leading to air trapping in the middle ear
(Laskiewicz, 1953). However, there is to our
knowledge no systematic investigation that would
confirm increased yawning rates under rapidly
changing ear pressure conditions. Also, yawning
is not the only mechanism to open the Eustachian
tube; swallowing, chewing, and the Valsalva
manoeuvre have the same effect (Laskiewicz,
1953; Winther et al., 2005). The middle ear
pressure release of yawning does therefore not
represent by itself an indispensable
evolutionary advantage. Equalization of ear
pressure seems to be a useful effect that yawns
have in common with other contractions of
oropharyngeal muscles rather than the primary
purpose of yawning.
3.6 The State Change Hypothesis
Rather than suggesting a single physiological
function of yawning, Provine attempted to
combine the multiple behavioural state changes
associated with yawning (wakefulness to sleep,
sleep to wakefulness, alertness to boredom, etc)
within a single framework. He proposed that
"yawning is a vigorous, widespread act that may
stir up our physiology and facilitate these
transitions" (Provine, 1986; Provine, 2005).
This approach has the advantage that it might
integrate findings from different research
fields. However, the proposition does not go
beyond a mere description of the behavioural
changes associated with yawning and does not
give insights into how or why the proposed state
changes might be achieved. Given the current
scarcity of experimental evidence for any
physiological function of yawning, the
combination of several physiological states
within a single concept also lacks empirical
support.
3.7 Other Physiological Hypotheses
Several other variants of a regulatory function
of yawning on body physiology have been proposed
(Smith, 1999). To name only a few: yawning
prevents lung atelectasis (Cahill, 1978);
yawning renews surfactant films in lungs
(Forrester, 1988); yawning ensures intermittent
evacuation of the palatine tonsillar fossae
(McKenzie, 1994). None of these propositions has
been experimentally tested. 4 The
Social/Communication Hypothesis In many
cultures, yawning is interpreted as a sign of
boredom and sleepiness and is therefore
considered to be rude (Schiller, 2002). Thus,
yawning seems to communicate a message that is
almost universally understood. Moreover, yawning
frequently occurs in social contexts. A
communicative function of yawning has therefore
long been suspected. The hypothesis states that
yawning is a non-verbal form of communication
that synchronizes the behaviour of a group
(Barbizet, 1958; Provine, 1986; Weller, 1988;
Deputte, 1994).
4.1 Yawning Has Physiological and Social
Triggers Yawning can be triggered by several
different physiological body states as well as
social contexts. Drowsiness (see above) and
boredom (Provine and Hamernik, 1986) are well
documented precursors of yawning. Observations
in animals further suggest that yawns may be
facilitated by hunger or mild psychological
stress (Deputte, 1994). The communication
hypothesis accounts for all these inductors by
stating that they generate yawning to transmit
the corresponding information to other members
of a social group. The number of possible
yawning triggers must of course not be
unlimited; otherwise the transmitted message
would be too ambiguous. Indeed, all triggers of
yawning mentioned above have in common that they
are mildly to moderately unpleasant while not
presenting an immediate threat.
4.2 Social Effects of Yawning The
social hypothesis predicts that yawning has some
impact on the behavioural organization of a
social group. Communication should result in
better synchronization of group behaviour. Such
effects have indeed been observed in Ostriches
(Sauer and Sauer, 1967), but studies that test
the prediction in a controlled fashion are
lacking.
4.3 Contagious Yawning Yawning has a
well-known contagious effect in humans
(Baenninger, 1987; Provine et al., 1987b;
Provine, 1989a; Provine, 1989b; Platek et al.,
2003) and this effect is now frequently used to
induce yawning for research purposes. Recent
studies have accumulated evidence that this
contagiousness depends on an intact social
competence of the yawning individual. The
susceptibility to contagious yawning correlates
with empathic skills in healthy humans (Platek
et al., 2003) and is reduced in patients with
disorders affecting the ability of social
interaction, such as autism (Senju et al., 2007)
and schizophrenia (Lehmann, 1979; Haker and
Rossler, 2009). In patients with schizophrenia,
the occurrence of yawns has been interpreted as
a positive sign indicating that the patient is
in an accessible mood (Lehmann, 1979).
Watching or hearing other persons yawn
activates a complex network of brain regions
related to motor imitation, empathy, and social
behaviour. Figure 3 illustrates the brain
regions that have been reported to activate in
different functional magnetic resonance imaging
(fMRI) studies when human subjects observe yawns
of others. The so-called mirror neuron system is
important for action understanding and imitation
(Rizzolatti and Craighero, 2004) and mirror
neurons in the right posterior inferior frontal
gyrus also seem to be recruited for contagious
yawning (Arnott et al., 2009). The mirror neuron
activity is however not specific to yawning but
occurs to the same amount also during
observation of other movements (Nahab et al.,
2009; Arnott et al., 2009). Activations that are
more specific to contagious yawns have been
observed in the posterior cingulate (Platek et
al., 2005), the bilateral superior temporal
sulcus (Schurmann et al., 2005), or the
ventromedial prefrontal cortex (Nahab et al.,
2009). The fMRI activations in these areas were
significantly greater when the study subjects
watched other persons yawn than when they
watched control face movements of others.
Although different studies have reported
divergent areas to be implicated in contagious
yawning, all of them seem to be part of a
distributed neural network related to empathy
and social behaviour (Saxe et al., 2004;
Carrington and Bailey, 2009). In children, no
contagious yawning can be induced before the age
of five (Anderson and Meno, 2003), suggesting
that the contagiousness of yawning depends on
mechanisms that have to develop during childhood
in parallel with the empathic capacity to
understand mental states of others (Saxe et al.,
2004).
In animals, contagious yawning has been
consistently observed in chimpanzees (Anderson
et al., 2004; Campbell et al., 2009; Vick and
Paukner, 2010), whereas it seems to be absent in
lions (Baenninger, 1987). In old-world monkeys
(Baenninger, 1987; Paukner and Anderson, 2006;
Palagi et al., 2009) and dogs (Joly-Mascheroni
et al., 2008; Harr et al., 2009), different
studies showed divergent results, but contagious
yawning occurs at least in some individuals. The
findings from animal studies therefore also
support the notion that contagious yawning
mostly occurs in individuals and species with
advanced empathic and social skills. In monkeys,
the contagiousness of yawning correlates with
the level of grooming contact between
individuals (Palagi et al., 2009), i.e., it is
higher in animals that are socially and
emotionally close to each other. In summary,
research on contagious yawning has revealed that
yawns are part of the action repertoire of
empathic and communicative processes in adult
humans and some mammals, which provides strong
evidence for a social role of yawns in these
species.
4.4 Other Social Modulators of
Yawning Social contexts were found to have
an important impact on the yawning rate. In
animals, the hierarchical position within a
social group influences the frequency of
yawning: group leaders initiate more yawns than
subordinates (Hadidian, 1980). This difference
in the yawning rate may correspond to the
greater importance of communications from
leaders than from other individuals for the
synchronized behaviour of the group (Sauer and
Sauer, 1967), and may thus also be explained
within the framework of the communication
hypothesis. There are however also yawns that
are independent of social modulation. Yawning
also occurs when individuals are alone and in
non-social animals. This might be used as an
argument against the communication hypothesis
and for the need to postulate an additional
physiological effect of yawning. However, the
existence of yawns during aloneness does not
contradict the communication hypothesis in
general; it merely shows that the generators of
yawning lack a negative feedback mechanism
checking for the presence of other individuals.
Hence, the message of yawning seems to be
triggered by certain body states and "sent out",
no matter whether there are other individuals
that might actually receive it. In humans, the
presence of other humans may even have a
suppressive effect on the yawning rate. If human
subjects feel socially observed, they completely
stop yawning even if the usual conditions of
yawning are met (Baenninger and Greco, 1991;
Provine, 2005). This suppression may result from
arousing effects inherent to social observation.
Alternatively, the negative connotation of
yawning in human society may push the
individuals to hide or inhibit yawns when they
are felt to be inappropriate.
4.5 Conclusions The communication hypothesis
has the best experimental evidence among all
propositions on the function of yawning. It is
the only model that can account for social
effects of yawning such as contagiousness and
for the different physiological states and
social contexts that can trigger it.
Missing elements of this model include
controlled studies observing a regulating effect
of yawning on synchronized group behaviour and
data on the neuropharmacological mechanisms
underlying the social inductors and effects of
yawning. It is also far from clear whether the
findings of contagious yawns derived mostly from
studies in humans and primates can be
generalized to other forms of yawns and to yawns
in other species. The social aspects of
spontaneous (non-contagious) yawns, particularly
in species and individuals who are not
susceptible to contagious yawning, have received
little research interest so far.
5
Discussion
In 1986, Robert R. Provine, the pioneer in
yawning research, wrote that "yawning may have
the dubious distinction of being the least
understood, common human behaviour." (Provine,
1986). Today, more than two decades later, this
may well still be the case. In particular, the
centuries-old question of why we yawn still
awaits a corroborated answer. None of the
numerous propositions on the function of yawning
has currently sufficient experimental support or
links to neuropharmacological mechanisms.
Nevertheless, the preceding sections (which are
summarized in Table 1) may have demonstrated
that the emphasis of models on yawning has
changed. Whereas traditional hypotheses were
mostly characterized by the quest for a
physiological function of yawning in
individuals, these propositions now face severe
explanatory problems or lack empirical evidence.
In contrast, the idea that yawning might rather
serve a social function in groups of individuals
receives increasing support from studies in
different fields. It emerges that yawning might
communicate unpleasant but not immediately
threatening states to other members of a group
in order to enhance behavioural
synchronization.
This social hypothesis of yawning is also
the only model that can account by itself for
all elements associated with yawns. For
instance, contagious effects or social contexts
of yawning cannot be explained when assuming a
purely physiological function. Physiological
hypotheses therefore have to postulate social
effects in addition to a physiological effect of
yawning, whereas the physiological triggers of
yawning form an integral part of social models.
Hence, the social hypothesis has not only the
best experimental support but is also the most
parsimonious model.
From an evolutionary perspective, the
communicative value of yawning may yield
sufficient advantage to explain its persistence
and frequent usage in many vertebrate species.
The capacity to exchange information about the
physical and mental state of each individual
seems indeed to be crucial for the survival of a
group. There is therefore no need to postulate
additional physiological functions of yawning to
explain its selection during evolution. One may
argue that the difficulties with physiological
models results from an oversimplification of a
complex phenomenon.
There might be different types of yawning
that assume different functions which are
unrecognized if all yawns are inappropriately
pooled. However, the data from observational
studies does not support this notion. Although
numerous yawn morphologies and contexts have
been described (Provine, 1986; Deputte, 1994;
Baenninger, 1987; Palagi et al., 2009; Vick and
Paukner, 2010), the different studies did not
converge on a consistent classification into
well-delimited types. Furthermore, most studies
found no functional or contextual differences
among the different yawning morphologies
(Provine, 1986; Deputte, 1994; Baenninger, 1987;
Palagi et al., 2009). Vick and Paukner (2010)
interpreted differences in the scratching rate
after "full yawns" vs. "modified yawns" with
additional voluntary face movements of
chimpanzees as evidence for a selective arousal
effect of modified yawns only, but we have seen
above that indirect behavioural markers of
arousals are problematic. The current limited
data therefore seems to suggest that yawning is
a single mechanism associated with a continuum
of behavioural manifestations rather than a
discrete set of functional entities.
On the species level, the generators and
functions of yawning may have evolved
differently in different species, and yawns may
even be a residual of earlier life forms with no
remaining function at all in some species.
However, in the absence of evidence for
systematic differences in the mechanisms and
functions of yawning between species or yawn
morphologies, this call for more complexity does
not withstand the simplicity and elegance of the
social model of yawning. In conclusion, current
data suggests that we might have to get used to
the idea that yawns have a primarily social
rather than physiological function.
6 Future Research Directions Several
lessons can be learned from research of the last
3 decades. Experience with the respiratory and
arousal hypotheses demonstrates that one must be
careful when interpreting indirect or anecdotal
evidence. Although both hypotheses had some
arguments and indirect evidence on their side,
direct measurements showed negative results. In
order to differentiate between specific features
of yawning and nonspecific coexisting elements,
it is important to include control groups or
conditions during experiments. The lack of
controlled experimental studies on yawning
illustrates the need for research programs in
all related fields. Some of the specific
questions that could be addressed are listed in
Table 2.
All current models on the function of
yawning are derived from observations of the
phenomenology and contexts of yawning, which may
result in a negligence of aspects that are not
behaviourally evident. An exploration of the
neural and metabolic mechanisms may give new
hints on the functions of yawning that were
hitherto unsuspected or on the mechanisms of
existing concepts. Future research should
therefore systematically assess behavioural,
physiological, and social features of yawning
and combine observational with interventional
techniques. This requires interdisciplinary
strategies that would overcome limitations of
traditional techniques. For example, a
combination of interventional approaches
[e.g., administration of yawn-inducing or
-inhibiting drugs (Argiolas and Melis, 1998),
experimental lesions of brain structures
involved in yawn-generation such as the PVN
(Argiolas et al., 1987), manipulation of
environmental conditions] with systematic
behavioural observations during wakefulness may
increase the value of both animal models and
observational approaches.
A multimodal approach of this kind also
seems to be necessary to resolve long-standing
controversies on whether different types of
yawning exist and on whether yawns in different
species are homologous. Future studies
addressing these issues should systematically
compare not only behavioural but also social,
functional, and physiological parameters when
trying to classify yawns within and across
species. Besides this explorative approach,
there is also a need for hypothesis-driven
research based on the current models of yawning.
Numerous open questions related to the
hypotheses discussed above remain unanswered;
Table 2 lists only a few. Page 26 of 37
7 Acknowledgments The authors would like to
thank Olivier Walusinski for his invaluable
online archive of articles on yawning
(http://www.baillement.com) which greatly
facilitated the literature research for this
article.
mise à jour
du
26 décembre
2010
Neurosci Biobehav
Res
2011;35(5):1302-1304
Why
do we yawn?
The
importance of evidence
or
specific yawn-induced
effects
Adrian G. Guggisberg, Johannes
Mathis, Armin Schnider,
Christian W. Hess
Gallup (Gallup, 2010) believes that our
recent review on the function of yawning
(Guggisberg et al., 2010) is unbalanced and that
it ignores evidence for his thermoregulation
hypothesis. Here we address these criticisms and
show them to be untenable. While we never
claimed that the social hypothesis of yawning
has "definite experimental support", we
emphasize the importance of experimental
evidence for specific effects of yawns when
considering why we yawn. The only specific
effect of yawning that could be demonstrated so
far is its contagiousness in humans, some
nonhuman primates, and possibly dogs, whereas
all studies investigating physiological
consequences of yawns were unable to observe
specific yawn-induced effects in the individual
of any species. The argument that from an
evolutionary perspective, yawns must have a
"primitive" physiological function arises from
imprecise reasoning.
Yawning is a multifaceted, ubiquitous, and
frequent behavior that has been largely
neglected by research. The existing scientific
literature on yawning is characterized by a
relative abundance of theoretical considerations
and hypotheses which contrasts with a scarcity
of experimental data. In an attempt to encourage
future research and to provide an overview of
the current state of empirical investigations,
we recently published a review that purposely
focused on experimental studies (Guggisberg et
al., 2010).
When going through the literature, it was
important to carefully distinguish between
triggers and effects of yawns in order to
correctly interpret the causal chain of this
complex behavior. With this approach, it became
evident that yawning has several rather well
documented triggers, which can be physiological,
psychological, or social. However, when it comes
to the effects of yawning, there is a striking
absence of evidence for any specific
physiological effect of yawning with several
studies reporting negative results (Baenninger
and Greco, 1991; Greco and Baenninger, 1991;
Guggisberg et al., 2007; Laing and Ogilvie,
1988; Provine et al., 1987; Regehr et al.,
1992). This is in contrast to the relatively
abundant evidence from research in different
fields showing that yawns have a specific
contagious effect in humans, some non-human
primates, and possibly dogs (Anderson et al.,
2004; Baenninger, 1987; Campbell et al., 2009;
Haker and Rossler, 2009; Harr et al., 2009;
Joly-Mascheroni et al., 2008; Palagi et al.,
2009; Paukner and Anderson, 2006; Provine, 1989;
Provine, 1989), which is associated with
activations in neural networks responsible for
empathy and social skills (Arnott et al., 2009;
Nahab et al., 2009; Platek et al., 2003; Platek
et al., 2005; Schurmann et al., 2005).
Our review concluded that no model of the
function of yawning has currently sufficient
experimental support, and that there is more
evidence for social effects than for
physiological effects of yawns. This
constellation forces us to consider the
possibility that yawning might actually have a
mainly social function.
Our article provoked criticisms by Andrew
Gallup who prefers to advocate a
thermoregulatory function of yawning (Gallup,
2010). Here we show that these criticisms are
ill-founded and based on precisely those
mistakes that we had tried to overcome with our
article.
The commentary of Gallup fails to
distinguish between triggers and effects of
yawning. By merely looking at the pooled
evidence for the different models of yawning, he
supposes that physiological and social models of
yawning both have similar evidence and dismisses
our conclusions as unbalanced. However, any
hypothesis on the function of yawning must be
supported not only by evidence for a
corresponding specific trigger, but also for a
specific effect. In the example of the arousal
hypothesis, there are at least 6 studies
suggesting that yawns can be triggered by
sleepiness (Giganti et al., 2007; Greco et al.,
1993; Guggisberg et al., 2007; Provine et al.,
1987; Zilli et al., 2007; Zilli et al., 2008),
but at least 5 studies that were unable to
observe a specific arousing effect of yawning
with at least 3 different techniques that are
considered the gold standard for measuring
vigilance (Baenninger and Greco, 1991; Greco and
Baenninger, 1991; Guggisberg et al., 2007; Laing
and Ogilvie, 1988; Regehr et al., 1992). In this
situation, we must conclude that the main
prediction of the arousal hypothesis is not
supported by experimental evidence. Gallup does
not agree with our argument that the
non-specific variation in heart rate
accompanying yawns is insufficient to conclude
on an activating function of yawns. However, we
keep insisting that an ubiquitous behavior such
as yawning should yield more evolutionary
advantage than to induce variation in heart rate
which already occurs hundreds of times each hour
with each movement and respiration. Unlike
claimed by Gallup, this lack of specificity does
not apply to the contagious effect of yawns,
because only yawn-related behavior can provoke
other yawns.
Gallup also accuses us of having ignored
evidence for his thermoregulation hypothesis.
However, the experimental studies published by
his group at the time we published our review
reported only changes in brain temperature as
triggers of yawns and provided no evidence for a
brain cooling effect. After the appearance of
our review, Gallup's group published a new study
measuring cortical temperature with implanted
thermocoupled probes in rats which showed an
increase of -O.2 t in brain temperature starting
about 1 minute before yawns and stretches, which
then starts to decrease again about 20-40
seconds after the onset of yawns and stretches
(Shoup-Knox et al., 2010). This is the first
study that provides direct evidence for an
association between brain temperature and
yawning. However, the question remains whether
this association is causal, i.e., whether the
decrease in brain temperature is produced by the
yawns as such. The observation that the
temperature decrease after yawning was similar
as after stretching suggests that the
respiratory component of yawns (inflow of cool
air) does not play a significant role. What
remains is an increase in blood flow associated
with yawns and stretches. However, the increase
in cerebral blood flow which is supposed to cool
down the brain according to the thermoregulation
hypothesis occurs within a few seconds after the
yawns.
Conversely, the brain continued to warm up
with the same speed as before until -20-40
seconds after the yawns and stretches of the
observed rats. Even if we allow for a certain
delay in venous blood drain and thermal
convection, this time difference appears to be
too large. The thermometer seems to have been
placed close to the dura and therefore should
have rapidly captured a blood flow induced
temperature change. Hence, as (Shoup-Knox et
al., 2010) discuss in their article, the
observed variation in brain temperature
associated with yawns is probably mediated by
concomitant thermoregulatory brain processes and
not caused by the yawns themselves as would have
been predicted by the thermoregulation
hypothesis (Gallup and Gallup, 2008). Moreover,
(Elo, 2010) has recently shown for humans that
even small yawn-induced decreases of temperature
(Gallup and Gallup, 2010) are physically
impossible as long as there is no massive
sweating associated with the yawning. Despite
the criticisms of Gallup, we also keep insisting
that the design of his earlier studies exploring
temperature as a trigger of yawns did not
include recordings of physiological parameters
such as brain temperature and vigilance. It is
therefore impossible to exclude confounding
effects in these studies.
We agree with Gallup that yawning needs to
be studied from a phylogenic perspective in
different species. However, we prefer to avoid
premature and problematic conclusions such as
"any social or communicative value of yawning
among humans and non- human primates is likely a
derived feature, while the underlying primitive
feature or function is physiological". Let's
start from the experimental finding of
contagious yawns in species and individuals with
empathic skills. We agree that empathic
contagion has developed late in evolution, and
that it must have been derived from a basic
communicative value of yawns. Indeed, we cannot
be empathic to states of others if this state is
not somehow communicated to us. Hence, the
existence of contagious yawning strongly
supports a communicative value of yawns at least
in these species. Gallup goes a step further and
proposes that basic communication must in turn
be derived from "primitive" physiological
features. Now, there is no doubt that the
components of yawns such as opening and closing
of the mouth and respiration have physiological
functions. In this sense, yawns are indeed
derived from more primitive physiological
features. However, this does not mean that the
combination of these components, i.e., the yawns
as such, also must have a physiological
function. Basic communication is a
phylogentically old phenomenon; even primitive
cells and organisms maintain communications with
the exterior. Yawning as a non-verbal form of
communication could therefore have evolved in
vertebrates independent of a physiological
function. Gallup's proposition that contagious
yawns may help to spread an arousing effect of
yawns to all individuals of a social group would
therefore need to be supported by empirical
evidence, which is, as we have discussed above,
negative. Hence, all we know so far is that
yawning has a communicative function in humans,
some non-human primates, and possibly dogs. Even
though this communicative function has so far
only been convincingly demonstrated in species
with empathic skills, it does not necessarily
depend on empathy and could therefore exist also
in non-empathic animals and contexts. Some
observational studies suggest that this may be
the case (Deputte, 1994; Sauer and Sauer, 1967),
but we repeat that controlled studies of social
effects in non-empathic species are lacking.
Yawning could additionally have physiological
functions in the individual, but the claim that
this is likely the case arises from imprecise
reasoning and the corresponding experimental
studies are essentially negative. Until
systematic comparative data across species
becomes available, we should also avoid
premature statements such as "it is likely that
instead of serving one purpose, yawning is
multifunctional across a number of
species".
We are further criticized for having given
only a "vague and imprecise" description of a
possible social function of yawning and for not
having integrated "theories on signal evolution"
in this framework. We believe that we need more
controlled empirical studies on social effects
of yawns in different species before we start to
construct precise theories. Precise hypotheses
that turn out to be wrong are of no use for the
advancement of yawning research.
Gallup distorts our article's content.
Unlike claimed we do discuss the lack of
experimental data for a social effect of yawns
beyond its contagiousness, and we conclude that
"none of the numerous propositions on the
function of yawning has currently sufficient
experimental support or links to
neuropharmacological mechanisms." Nevertheless,
given that there is no evidence for any specific
physiological effect of yawns in any species,
the evidence for social effects is still better.
Unlike claimed, we do include all empirical
studies in our discussion of the arousal
hypothesis, including the ones mentioned in the
article of Baenninger (1997). Unlike claimed we
do consider experimental data from all species
and discuss the possibility that yawning might
be multifunctional across species.
In conclusion, we cannot agree with the
criticisms expressed by Gallup (Gallup, 2010).
Discussions on the function of yawning should be
based on experimental evidence and not on
problematic assumptions.
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