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mise à jour du
23 mars 2014
Neurosci Lett.
2014;566:182-187
Emotional stress evoked by classical fear conditioning
induces yawning behavior in rats
 
Kubota N, Amemiya S, Yanagita S, Nishijima T, Kita I.
Department of Human Health Science, Tokyo Metropolitan University Japan  

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Abstract
 
Yawning is often observed not only in a state of boredom or drowsiness but also in stressful emotional situations, suggesting that yawning is an emotional behavior. However, the neural mechanisms for yawning during stressful emotional situations have not been fully determined, though previous studies have suggested that both parvocellular oxytocin (OT) and corticotropin-releasing factor (CRF) neurons in the hypothalamic paraventricular nucleus (PVN) are responsible for induction of yawning.
 
Thus, using ethological observations and c-Fos immunohistochemistry, we examined whether emotional stress evoked by classical fear conditioning is involved in induction of yawning behavior in freely moving rats. Emotional stress induced yawning behavior that was accompanied by anxiety-related behavior, and caused neuronal activation of the central nucleus of the amygdala (CeA), as well as increases in activity of both OT and CRF neurons in the PVN. These results suggest that emotional stress may induce yawning behavior, in which the neuronal activation of the CeA may have a key role.
-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, Seki Y, Nakatani Y, Fumoto M, Oguri M, Sato-Suzuki I, Arita H. Corticotropin-releasing factor neurons in the hypothalamic paraventricular nucleus are involved in arousal/yawning response of rats. Behav Brain Res. 2006;169(1)48-56.
-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
-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 Mar 11.
-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.
-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
-Sato-Suzuki I, I Kita, Seki Y, M Oguri, H Arita Cortical arousal induced by microinjection of orexins into the paraventricular nucleus of the rat Behavioural Brain Research 2002;128:169-177

pvn
 
1. Introduction
 
Yawning is often observed not only in a state of boredom ordrowsiness, but also in stressful emotional situations in humans and other animals. Ethological and psychological studies in primates have reported yawning following neighboring individualsthat are vocalizing and showing sexual jealousy [4,5]. Clinical reports have shown that yawning is frequently observed in anxiety disorders, including patients with hysteria, depression, and motion sickness [7,28]. In addition, Major et al. [19] reported that anxiogenic compounds induce anxiety-like behavior in monkeys that is accompanied by yawning. Thus, yawning is considered an emotional behavior.
 
Previous pharmacological and lesion studies have suggested that the paraventricular nucleus of the hypothalamus (PVN) is essential for the occurrence of yawning [3,26]. Additionally, we have reported that both parvocellular oxytocin (OT) neurons and corticotropin-releasing factor (CRF) neurons in the PVN, each of which sends descending axons to the lower brainstem involved in either arousal, respiratory, cardiovascular, or other autonomic functions, are responsible for yawning that is accompanied by an arousal response [14&endash;16].
 
Although these results suggest that the stereotyped yawning response is mediated by both parvocellular OT and CRF neurons in the PVN, the mechanisms of yawning during stressful emotional situations have not been fully determined.
 
The amygdala is generally known to play a pivotal role in emotion [1,2]. The central nucleus of the amygdala (CeA), which is a part of the amygdaloid complex, is particularly known to be essential for integration of behavioral, autonomic, and hormonal responses to emotional stress, and is one of the most important output regions an intrinsic reward, known as the "warm glow" effect. Humans report feeling good when they do good and show activation of reward-related brain for the expression of these emotional responses [18,20]. In addition,neuroanatomical and functional studies have suggested the importance of connections from the CeA to the PVN for stress responses[10,12,13]. Thus, yawning during emotional stress may be induced through activation of CeA neurons, as well as both parvocellular OT and CRF neurons in the PVN. In the present study, using ethological observation and c-Fos immunohistochemistry in rats, we investigated whether emotional stress is involved in induction of yawning behavior.
 
4. Discussion
 
To the best of our knowledge, this is the first study to determine the involvement of emotional stress in induction of yawning behavior using ethological observations and c-Fos immunohistochemistry in rats. Classical fear conditioning induced yawning behavior accompanied by anxiety-related behavior, and caused neuronal activation of the CeA, as well as increases in activity of both OT and CRF neurons in the PVN. These results suggest that emotional stress may induce yawning behavior.
 
The present study showed that yawning behavior was observed after fear conditioning, which is a common model to produce anxiety [11,20]. Our results showed significant decreases in the number of entries into the center of the field, lines crossed, and rearing after fear conditioning, suggesting that the fear conditioning used in the present study produced anxiety. Previous studies in monkeys have shown that anxiogenic compounds induce anxiety-like behavior that is accompanied by yawning [17,19], and that yawning is observed in stressful emotional situations, such as in punishment-induced fear and neighboring individuals who are vocalizing and showing sexual jealousy [4,5,22]. Thus, yawning behavior may be a type of emotional behavior caused by emotional stress.
 
The neural mechanisms underlying yawning as a type of emotional behavior are poorly understood. The PVN plays a critical role in behavioral and arousal responses that are associated with various stressors [9,21] and is the most important brain structures for the induction of yawning behavior [3,26]. We have reported that both parvocellular OT and CRF neurons in the PVN are responsible for the yawning that is accompanied by arousal responses [14&endash;16].The present study showed increases in activity of both parvocellular OT and CRF neurons in the PVN during emotional stress, suggesting that emotional stress may induce yawning behavior directly or indirectly through neuronal activation of the PVN which is responsiblefor induction of yawning.
 
What type of signaling pathway is involved in the emotionalstress-induced yawning behavior that is mediated by the PVN? Neuroanatomical and functional studies have suggested that connections from the CeA to the PVN may be important for stressand emotional responses [10,12,13]. Gray et al. [12] reported thatinjections of an anterograde tracer into the CeA resulted in a few labeled axons and terminals within the caudal lateral and medial parvocellular regions of the PVN, indicating that the CeA directly innervates the PVN [6,13]. On the other hand, the CeA is wellknown to send dense projections to the bed nucleus of the stria terminalis [8,13], which is one of the brain regions that is involved in emotional responses and that densely innervates the PVN. Furthermore, several studies have shown that emotional and physical stress increases neuronal activation of the portions of the amygdala that project to the PVN and induces behavioral and physiological responses, whereas lesions of the CeA block or greatly attenuate stress responses [10,12,13]. Recently, pharmacological study suggested the involvement of mesolimbic regions including amygdala in induction of yawning [25]. Taken together, it is possible that neuronal activation of the CeA caused by emotional stress may beinvolved in the induction of yawning as an emotional behavior.
 
Unfortunately, our data provide a correlation between neuronal activation in the CeA and yawning, but there is no real evidence in this study that they are related. This possibility should be investigated further using physiological, anatomical, and lesion studies.
 
In summary, we observed yawning behavior that was accompanied by anxiety-related behavior during emotional stress in which a state of anxiety was evoked by classical fear conditioning. The emotional stress increased neuronal activation of the CeA, as well as increases in activity of both OT and CRF neurons in the PVN which are responsible for induction of yawning. These results suggest that emotional stress may induce yawning behavior, in which the neuronal activation of the CeA may have a key role.