Yawning behavior is characterized by mouth opening
accompanied by deep inspiration, as well as arousal
response, and is often observed not only in states of
boredom or drowsiness, but also in stressful emotional
situations in humans and animals. These phenomena suggest
that yawning response may be an emotional behavior,
possibly through activation of the central nucleus of
amygdala (CeA), which is a critical region for emotional
responses.
However, the involvement of the CeA in triggering
yawning remains unknown. Here, the authors investigated
whether neuronal activation of the CeA by microinjection
of L-glutamate into the CeA is able to induce stereotyped
yawning responses in anesthetized, spontaneously
breathing rats. In addition, they assessed the effects of
the CeA stimulation on the activation of oxytocin (OT)
and CRF (corticotropin-releasing factor) neurons in the
paraventricular nucleus of the hypothalamus (PVN), which
is responsible for induction of yawning, using c-Fos
immunohistochemistry. Microinjection of L-glutamate into
the CeA causes an initial depressor response in the blood
pressure and an arousal shift on the electrocorticogram
followed by a single inspiration, which is the same as
the typical pattern of the stereotyped yawning response
induced by the PVN stimulation. In addition, the CeA
stimulation activated the neuronal activities of both OT
and CRF neurons in the PVN, as well as yawning
responses.
These results indicate that activation of the CeA is
involved in the induction of yawning response, suggesting
that yawning is an emotional behavior.
Le
bâillement est-il un comportement émotionnel
?
Le bâillement se caractérise par une
large ouverture de la bouche accompagnée d'une
inspiration profonde et par une stimulation de la
vigilance. On l'observe souvent non seulement dans des
états d'ennui ou de somnolence, mais
également dans des situations émotionnelles
stressantes chez l'homme et les animaux. Ces
phénomènes suggèrent que le
bâillement peut être un comportement
émotionnel, possiblement par l'activation du noyau
central de l'amygdale (CeA), une région critique
pour les réponses émotionnelles. Cependant,
l'implication de la CeA dans le déclenchement du
bâillement reste inconnue.
Ici, les auteurs ont examiné si l'activation
neuronale du CeA par microinjection de L-glutamate dans
le CeA est capable d'induire des bâillements
stéréotypés chez des rats
anesthésiés et respirant
spontanément. De plus, ils ont
évalué les effets de la stimulation du CeA
sur l'activation des neurones ocytocinocynergiques (OT)
et CRF (facteur de libération de la
corticotropine) dans le noyau paraventriculaire de
l'hypothalamus (PVN), responsable de l'induction du
bâillement, à l'aide de Immunohistochimie
Fos. La microinjection de L-glutamate dans la CeA
provoque une réponse dépressive initiale de
la pression artérielle et un décalage de
l'excitation sur l'électrocorticogramme, suivis
d'une seule inspiration, ce qui correspond au
schéma typique d'un bâillement
stéréotypée induite par la
stimulation PVN. En outre, la stimulation du CeA a
activé les activités neuronales des
neurones OT et CRF dans le PVN, ainsi que des
bâillements. Ces résultats indiquent que
l'activation du CeA est impliquée dans l'induction
du bâillement, suggérant que bâiller
est un comportement émotionnel.
-Kita I,
Kubota N, Yanagita S, Motoki C
Intracerebroventricular administration of
corticotropin-releasing factor antagonist attenuates
arousal response accompanied by yawning behavior in rats.
Neurosci.Letter 2008;433(3):205-208
-Kita I,
Yoshida Y, Nishino S. An activation of parvocellular
oxytocinergic neurons in the paraventricular nucleus in
oxytocin-induced yawning and penile erection. Neurosci
Res. 2006;54(4):269-275
-Kita I, Sato-Suzuki
et al.Yawning responses induced by local hypoxia in
the paraventricular nucleus of the rat.Behavioural Brain
Research 2000;117(1-2):119-126
-Kubota
N, Amemiya S, Motoki C, Otsuka T, Nishijima T, Kita
I. Corticotropin-releasing factor antagonist reduces
activation of noradrenalin and serotonin neurons in the
locus coeruleus and dorsal raphe in the arousal response
accompanied by yawning behavior in rats. Neurosci Res.
2012;72(4):316-323
-Sato-Suzuki I, Kita I,
Oguri M, Arita H Stereotyped yawning responses
induced by electrical and chemical stimulation of
paraventricular nucleus of the rat Journal of
Neurophysiology, 1998;80(5)2765-2775
-Seki Y, Y Nakatani, et
al Light induces cortical activation and yawning in
rat Behav Brain Res 2003;140(1-2):65-73-
-Seki Y,
Sato-Suzuki I, et al Yawning/cortical activation
induced by microinjection of histamine into the
paraventricular nucleus of the rat. Behav Brain Res.
2002;134(1-2):75-82.
Yawns function as a
compensatory brain cooling mechanism
The existence of yawning across a diverse array of
species has led many researchers to postulate its
neurological significance. One hypothesis, which has
garnered recent support, posits that yawns function to
cool the brain by flushing hyperthermic blood away from
the skull while simultaneously introducing a cooler
arterial supply. The current study tested this hypothesis
by examining how manipulations aimed at modifying carotid
artery temperature, which in turn directly alters cranial
temperature, influences contagious yawning in
humans.
Participants held either a warm (46 °C), cold (4
°C) or room temperature (22 °C) pack firmly to
their neck, just over their carotid arteries, for a
period of five minutes prior to watching a contagious
yawning stimulus. Thermographic imaging verified that
these manipulations produced predicted changes in
temperature at the superomedial orbital area, a region
previously used as a noninvasive measure of brain
temperature (i.e., the brain temperature tunnel).
As predicted by past research, both the urge to yawn
and overall yawn frequency significantly diminished in
the cooling condition (p < .05). Less than half
(48.5%) of the participants in the cooling condition
reported the urge to yawn, while this urge was expressed
by the vast majority of participants in the warming
condition (84.8%). Moreover, there was a threefold
difference in the mean number of yawns per participant
between the cooling and warming conditions (0.364
compared to 1.121). These findings are consistent with
previous research indicating that yawns function as a
compensatory brain cooling mechanism.
Refroidir le cerveau
en bâillant
L'existence de bâillements
repérés dans un large éventail
d'espèces a conduit de nombreux chercheurs
à postuler une signification neurologique. Une
hypothèse, qui a recueilli un soutien
récent (et contesté), postule que les
bâillements servent pour refroidir le cerveau en
chassant le sang hyperthermique du crâne tout en
introduisant simultanément un apport
artériel plus froid. La présente
étude a testé cette hypothèse en
examinant la manière dont les manipulations visant
à modifier la température de
l'artère carotide, qui à son tour modifie
directement la température crânienne, ont
une incidence sur le bâillement contagieux chez
l'homme. Les participants ont tenu un sac chaud (46
° C), froid (4 ° C) ou à la
température ambiante (22 ° C) fermement sur
leur cou, juste au-dessus de leurs artères
carotides, pendant une période de cinq minutes
avant de regarder des enregistrements vidéos de
bâillements, afin d'en déclencher par
contagion.
L'imagerie thermographique a permis de
vérifier que ces manipulations produisaient les
changements de température prévus au niveau
de la région orbitale super-médiale, une
région précédemment utilisée
comme mesure non invasive de la température
cérébrale. Comme prévu par des
recherches antérieures, le besoin de bâiller
et la fréquence globale de bâillements ont
considérablement diminué dans les
conditions de refroidissement (p <0, 05). Moins de la
moitié (48, 5%) des participants en période
de refroidissement ont signalé l'envie de
bâiller, à l'inverse de ce qui a
été exprimé par la grande
majorité des participants en période de
réchauffement (84, 8%).
De plus, le nombre moyen de bâillements par
participant était trois fois plus important entre
les conditions de refroidissement que de
réchauffement (0,364 contre 1,121). Ces
résultats sont cohérents avec les
recherches précédentes indiquant que les
bâillements fonctionnent comme un mécanisme
accesoire de refroidissement du cerveau.
Body temperature is
controlled by the preoptic area of anterior
hypothalamus
The ability to thermoregulate is essential and in
mammals, body temperature is controlled by the preoptic
area of anterior hypothalamus (POA). Approximately 30% of
the neurons in the POA are sensitive to changes in brain
temperature. However, the mechanisms by which these
neurons are involved in thermoregulation are unclear.
Now, Wang et al. show that Ptgds-expressing POA neurons
detect increases in brain temperature and reduce core
body temperature via increased production of
prostaglandin D2 (PGD2).
La
température corporelle est contrôler par
l'aire préoptique de
l'hypothalamus
La capacité de réguler sa
température corporelle est essentielle chez les
mammifères. La température corporelle est
contrôlée par la zone pré-optique de
l'hypothalamus antérieur (POA). Environ 30% des
neurones de la POA sont sensibles aux changements de la
température cérébrale. Cependant,
les mécanismes par lesquels ces neurones sont
impliqués dans la thermorégulation ne sont
pas clairs. Maintenant, Wang et al. montrent que les
neurones POA exprimant Ptgds détectent les
augmentations de la température
cérébrale et réduisent la
température centrale du corps via une production
accrue de prostaglandine D2 (PGD2).
Whole-cell patch-clamp recording followed by single-cell
RNA sequencing was used to determine a class of POA
neurons that showed an increase in firing on exposure to
increased temperature and expressed Ptgds, which encodes
lipocalin-type prostaglandin-D synthase (L-PGDS), which
generates PGD2, a neuromodulator of a variety of
physiological processes.
To mimic the effect of brain temperature elevation or
reduction on mouse Ptgds POA neurons, the authors used
engineered G protein-coupled receptors exclusively
activated by designer drugs (DREADD). Body temperature
fluctuates during the circadian cycle, and chemogenetic
manipulation of the activity of Ptgds POA neurons
disrupted the normal fluctuation pattern, suggesting a
role for these neurons in circadian temperature
changes.
Next, the role of L-PGDS and PGD2 was explored in
more detail. First, brain slices from the POA were
incubated at different temperatures. A greater amount of
PGD2 was detected in brain slices incubated at 39_°C
for 30_min than in those incubated at 36_°C or
33_°C. In addition, in a mouse model of fever
(induced by intracerebroventricular injection of PGE2),
blocking L-PGDS, and therefore blocking synthesis of
PDG2, led to a greater increase in core body temperature
than in mice injected with vehicle control. By contrast,
injection of PDG2 led to hypothermia in wild-type mice.
Together, these results suggest that production of PGD2
is increased in response to a rise in temperature of the
POA, leading to a reduction in core body
temperature.
An optogenetic approach was then used by the
researchers to test and confirm their hypothesis that
PGD2 exerts its effect on body temperature by activating
its receptor DP1 on downstream neurons in the ventral
medial preoptic area.
Finally, mice with Ptgds knockdown in POA were unable
to regulate body temperature: compared with controls kept
under the same conditions, mice housed at an elevated
ambient temperature displayed an increase in body
temperature, and mice housed at normal room temperature
showed a large drop in body temperature that eventually
lead to death, indicating that Ptgds expression is
important for thermoregulation.
"PGD2-synthase-expressing POA neurons have a
crucial role in homeostatic body temperature regulation"
The authors conclude that PGD2-synthase-expressing
POA neurons have a crucial role in homeostatic body
temperature regulation. Identification of Ptgds as a
genetic marker for temperature-sensitive neurons could
facilitate future research in thermoregulation.
F. Desmoulins, dessinateur et graveur, adepte de
spiritisme, produit une oeuvre abondante,
léguée par sa veuce au Musée de
Brantôme dans les années 1950.
