Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
http://www.baillement.com

mystery of yawning 

 

 

mise à jour du
25 septembre 2022
Behav Brain Res
2022 Sep 1:114091
 Neural pathways from the central nucleus
of the amygdala to the paraventricular nucleus
of the hypothalamus are involved in induction
of yawning behavior due to emotional stress in rats
Kubota N, Amemiya S, Yanagita S, Kita I.

Chat-logomini

 
Abstract
As yawning is often observed in stressful or emotional situations such as tension and anxiety, this suggests that yawning can be considered to be an emotional behavior. However, the neural mechanisms underlying emotion-induced yawning remain unclear. It is well known that the hypothalamic paraventricular nucleus (PVN) is the most important brain structure for induction of yawning behavior. The authors previously showed that induction of yawning involves the central nucleus of the amygdala (CeA), as well as the PVN. Therefore, emotion-induced yawning could potentially be induced through activation of the direct/indirect neural pathways from the CeA to the PVN. The present study used a combination of retrograde tracing (injection of Fluoro-Gold (FG) into the PVN) and c-Fos immunohistochemistry to examine the neural pathways that evoke emotion-induced yawning. They additionally performed lesion experiments on the CeA using ibotenic acid, a neurotoxin, to determine whether the CeA is involved in the induction of emotion-induced yawning. Emotional stress by fear conditioning induced yawning behavior, and induced expression of double-labeled cells for c-Fos and FG in the bed nucleus of the stria terminalis (BNST), but not in the CeA. Furthermore, the CeA lesions caused by ibotenic acid abolished the induction of emotion-induced yawning. These results suggest that a neural pathway from the CeA to the PVN via the BNST may be primarily involved in the induction of emotion-induced yawning behavior.
 
Résumé
Le bâillement est souvent observé dans des situations stressantes ou émotionnelles. Cela suggère que le bâillement peut être considéré comme un comportement émotionnel. Cependant, les mécanismes neuronaux qui sous-tendent les bâillements induits par les émotions ne sont toujours pas clairs. Il est connu que le noyau paraventriculaire de l'hypothalamus (PVN) est la structure cérébrale la plus importante pour l'induction de ce comportement de bâillement. Les auteurs ont précédemment montré que l'induction du bâillement implique le noyau central de l'amygdale (CeA), ainsi que le PVN. Par conséquent, le bâillement induit par l'émotion pourrait potentiellement être induit par l'activation des voies neuronales directes/indirectes de la CeA au PVN. Cette étude a utilisé une combinaison de traçage rétrograde (injection de Fluoro-Gold (FG) dans le PVN) et d'immunohistochimie c-Fos pour examiner les voies neuronales qui déclenchent le bâillement induit par l'émotion. Ils ont également réalisé des expériences de lésion de la CeA en utilisant de l'acide iboténique, une neurotoxine, afin de déterminer si la CeA est impliquée dans l'induction des bâillements induits par les émotions. Le stress émotionnel par conditionnement à la peur a induit un comportement de bâillement, et a induit l'expression de cellules doublement marquées pour c-Fos et FG dans le noyau de la stria terminalis (BNST), mais pas dans la CeA. En outre, les lésions de la CeA causées par l'acide iboténique ont aboli l'induction de bâillements induits par l'émotion. Ces résultats suggèrent qu'une voie neuronale allant de la CeA au PVN via le BNST pourrait être principalement impliquée dans l'induction du comportement de bâillement induit par l'émotion.
-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
-Kubota N, Amemiya S, Yanagita S, Nishijima T, Kita I. Emotional stress evoked by classical fear conditioning induces yawning behavior in rats. Neurosci Lett. 2014;566:182-187
-Kubota N, Amemiya S, Tanagita S, Nishijima T, Kita I. Central nucleus of the amygdala is involved in induction of yawning response in rats. Behavioural Brain Research 2019;371:111974
-Kubota N, Amemiya S, Yanagita S, Kita I. Neural pathways from the central nucleus of the amygdala to the paraventricular nucleus of the hypothalamus are involved in induction of yawning behavior due to emotional stress in rats. Behav Brain Res. 2022 Sep 1:114091.

 
Yawning is a common behavior in animals and humans, but the biological significance of yawning remains poorly understood. In fact, yawning is often observed in not only in the state of boredom or drowsiness, but also stressful emotional situations such as tension and anxiety. These phenomena suggest that yawning can be considered to be an emotional behavior, which could work as a non-verbal communica- tion tool indicating emotional responses to stressors from inside/outside the body. It has been reported that the emotional arousal evoked by neuropharmacological stimulations, including anxiogenic or anxiolytic drugs, can potentially affect the frequency of yawning in animals [1&endash;4]. In addition, several clinical studies have reported finding that patients with anxiety disorder frequently yawn [5,6]. If yawning is an emotional behavior, the neural circuit generating emotional stress may be involved in yawning occurrence. However, at the present time, the neural mechanisms underlying the emotion-induced yawning are poorly undrstood.
 
 
The paraventricular nucleus (PVN) of the hypothalamus, which plays a critical role in integrated stress responses [7,8], is the most important of the brain structures for the induction of yawning behavior [9,10]. Furthermore, it has been reported that both parvocellular oxytocin (OT) neurons and corticotropin-releasing factor (CRF) neurons in the PVN are responsible for induction of the yawning accompanied by arousal re- sponses [11&endash;14]. Recently, we additionally reported that emotional stress evoked by classical fear conditioning induces yawning behavior accompanied by neuronal activation of the central nucleus of the amygdala (CeA), as well as activation of both OT and CRF neurons in the PVN in freely moving rats [15]. The CeA, which is part of the amygda- loid complex, is known to be essential for the expression of emotional responses, including behavioral, autonomic and hormonal responses during stressful situations [16&endash;19]. We also recently showed that microinjection of L-glutamate into the CeA induced arousal/yawning response accompanied by the activation of OT and C PVN [20]. Neuroanatomical studies have shown that the CeA not only directly innervates the PVN [21&endash;23] but also indirectly innervates the PVN through the bed nucleus of the stria terminals (BNST), which is one of the brain regions involved in emotional responses [23,24]. Therefore, it is possible that emotion-induced yawning could be induced by the activation of the direct/indirect neural pathways from the CeA to PVN.RF neurons in the In the present study, we used a combination of retrograde tracing and c-Fos immunohistochemistry to examine the neural pathways evoking emotion-induced yawning. We also performed lesion experi- ments on the CeA using ibotenic acid, a neurotoxin, to determine whether the CeA is involved in the pathway that can induce the emotion- induced yawning. Our results suggest that emotion-induced yawning is induced by activation of the CeA-PVN pathway.
 
 
Discussion
 
The present study showed that emotional stress by fear conditioning could induce yawning behavior and induce expression of double-labeled cells for c-Fos and FG in the BNST, but not in the CeA. In addition, the CeA lesions caused by ibotenic acid abolished the induction of emotion- induced yawning. This is the first demonstration that an indirect neural pathway from the CeA to the PVN could potentially be involved in the induction of yawning behavior.
 
We have previously reported that classical fear conditioning induced yawning behavior in rats, i.e., emotion-induced yawning, which is consistent with the results of our present study, in addition to showing that the emotion-induced yawning is accompanied by increased anxiety- related behavior and neuronal activation in the CeA, as well as both the OT and CRF neurons in the PVN [15]. Furthermore, we have also recently shown that the microinjection of L-glutamate into the CeA was able to induce the stereotyped yawning responses, which are charac- terized by an initial depressor in the blood pressure and an arousal shift on the electrocorticogram followed by a single deep inspiration [10,20]. These findings suggest that yawning can be an emotional behavior, and that emotion-related neural structures and/or pathways, including the CeA or the direct/indirect pathways from the CeA to the PVN, may be involved in the induction of emotion-induced yawning. However, one limitation of this study is that it cannot be ruled out the possibility that the total number of yawning in emotional stress group may include not only emotion-induced yawning following fear conditioning but also non-emotion-induced yawning. The data on neuronal activity could partly support our hypothesis.
 
In the present study, we found that the CeA lesions caused by ibo- tenic acid were able to abolish the induction of emotion-induced yawning, accompanied by impairment of the expression of grooming. These results suggest a crucial role of the CeA in the induction of emotion-induced yawning. Fear conditioning is a commonly used model to evoke a stressful emotional state such as anxiety, which is mainly since it cannot be ruled out that the exitotoxicity and electrical lesion techniques can damage not only neurons but also the fibers passed by.
 
We also found that double-labeled neurons for c-Fos and FG in the BNST, but not in the CeA, were increased during emotion-induced yawning. Several neuroanatomical studies have indicated that the PVN directly receives neural projections from the CeA and BNST [21&endash;24, 39&endash;42]. It has been shown that the BNST can directly receive projections from the CeA [24,43], which suggests that there is an indirect pathway from the CeA to the PVN. The BNST is also involved in the emotional responses such as fear and anxiety [18,44&endash;48]. In addition, recent studies have shown that neuronal activation of the BNST induced yawning behavior [49,50]. Although increases in c-Fos expression in the CeA and BNST are considered to reflect the emotional stress situation including yawning and grooming, our data provided by a combination of retrograde tracing and c-Fos immunohistochemistry suggests that the indirect neural pathway from the CeA to the PVN via the BNST may be primarily involved in the induction of emotion-induced yawning.
 
In summary, the present study investigated the role of the CeA - PVN pathway in emotion-induced yawning using a combination of retrograde tracing, c-fos immunohistochemistry, and ibotenic acid lesions. The findings of the present study indicated that the CeA is crucial for in- duction of emotion-induced yawning, and that the neural CeA-PVN circuits generating emotional stress may be primarily involved in yawning occurrence, via the BNST, suggesting that yawning might be an emotional behavior. Further studies will need to be conducted to assess the contribution of the direct/indirect neural pathways in the induction of emotion-induced yawning.