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17 avril 2003
Behav Brain Res
2003; 140(1-2):65-73
lexique
Light induces cortical activation
and yawning in rats
Seki, Y., Y. Nakatani, I Kita, I Sato-Suzuki, M Oguri, H Arita
Department of Physiology, Toho University School of Medicine, Ohta-ku, Tokyo. Japan

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-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

Abstract : We examined the effects of light stimulation on cortical activation and yawning response in anesthetized, spontaneously breathing rats. Cortical activation was assessed by means of an electrocorticogram (ECoG) and yawning response was evaluated by monitoring an intercostal electromyogram as an index of inspiratory activity and a digastric electromyogram as an indicator of mouth opening. Light stimulation elicited an arousal shift in the ECoG to faster rhythms. This arousal response was followed by a single large inspiration with mouth opening, i.e. a yawning response. Higher light intensity significantly reduced the onset latency of the arousal/yawning response. Pretreatment with pyrilamine, an H1-histamine receptor antagonist, injected into the lateral ventricle blocked both the cortical activation and the yawning response induced by light stimulation, suggesting a role of brain histaminergic neurotransmission in modulating the light-induced arousal yawning responses.
 
1. Introduction : Yawning is a very common behavior in humans and other animals, yet it has received little attention in science as well as in daily life. The lack of interest in yawning behavior may be due to the lack of knowledge of its physiological significance. One approach to clarify the functions of yawning is to reliably evoke a yawning response and monitor the response together with the concomitantly occurring associated phenomena. In this connection, we have recently reported that a stereotyped yawning response can be evoked by chemical stimulation of the paraventricular nucleus (PVN) of the hypothalamus in anesthetized, spontaneously breathing rats. In those studies, we recorded the electrocorticogram (ECoG) to evaluate arousal responses during yawning, and found that ECoG arousal, represented by lower voltage and faster rhythm, occurred before the yawning behavior, which indicates that yawning has physiological significance in increasing alerting mechanism.
 
Although the PVN is known to be essential for the occurrence of yawning, our previous studies raised another fascinating possibility: that the PVN may also play an important role in triggering cortical activation. We have shown that the PVN mediates the arousal yawning response induced by higher brain ischemia. It was also suggested that the PVN plays an important role in the arousal yawning responses evoked by orexinergic as well as histaminergic neurotransmission. Since the PVN is generally known to play a critical role in stress responses, the PVN may also be involved in cortical activation related to stress.
 
In this study we sought to determine whether bright light stimulation, one kind of acute stress, can induce cortical activation together with the yawning response. This idea was first suggested by two lines of evidence. The first is that bright light has immediate alerting effects in humans as well as rats. The second is that yawning, a behavior generally believed to be induced by drowsiness or boredom, is also influenced by the circadian rhythm in humans as well as rats. Everybody might have yawned due to light stimulation when waking up in the morning. Indeed, it is reported that yawning is most likely in the morning shortly after waking, a condition corresponding to a transition from dark to light, but the neural mechanisms underlying the light-induced arousal effect or yawning are poorly understood. The present study was designed to explore whether the PVN is involved in this mechanism.
 
By using our model of the arousal yawning response, we examined whether brief light stimulation of the eyes of anesthetized, spontaneously breathing rats induces the cortical activation as well as the yawning response. Attempts were also made to identify whether histamine, a neurotransmitter considered to be important in regulation of the arousal system, yawning and the circadian rhythm, is involved in these responses. [...]
 
4. Discussion : This is the first study showing the effects of light stimulation on arousal yawning response in anesthetized rats. Light stimulation induced yawning, together with an arousal shift in the ECoG; Since yawning is a behavior mediating the PVN of the hypothalamus, we speculate that the PVN might be also involved in the light-induced arousal signaling pathway.
 
The concept that the PVN is essential for the occurrence of yawning was first proposed by the Argiolas and Melis group, who found that microinjection of several substances, including apomorphine, into the PVN increases the frequency of spontaneous yawns in freely moving rats. Consequently, they demonstrated that lesions of the PVN prevent yawning induced by apomorphine. On the other hand, we provided evidence that a stereotyped yawning response can be evoked by several chemical stimulations of the PVN in anesthetized, spontaneously breathing rats. The yawning response has important physiological significance in anesthetized animals, since various physiological aspects accompanied to the yawning behavior, such as the autonomic or arousal responses can be concomitantly monitored. We further found that it is the medial parvocellular subdivision(mp) of the PVNwhich is involved in the yawning response. Within the mp, the neurons: responsible for yawning might be the oxytocinergic: parvocellular neurons projecting to the lower brain stem. This suggestion was principally based on the report of Sawchenko and Swanson who demonstrated that oxytocinergic parvocellular neurons in the PVN send descending axons to the lower brain stem, a region involved in arousal, respiratory, cardiovascular and other autonomic functions. In view of this, we suggest the possibility that light stimulation induces the yawning response by indirectly activating the oxytocinergic parvocellular neurons in the PVN projecting to the lower brain stem. However, we cannot exclude the possibility that other pathways, besides the oxytocinergic ones, can be involved in the yawning response. For instance, ACTH injected into the PVN and surrounding periventricular region induces yawning, that is not involving oxytocinergic pathways.
 
What kind of signaling pathway is then involved in the light-induced yawning response mediated by the PVN? Light is the predominant stimulus in maintaining the circadian rhythm in humans as well as other animals. The principal pacemaker that generates circadian rhythms is located in the suprachiasmatic nucleus (SCN) of the hypothalamus, and the light signal reaches the SCN through the retina-hypothalamic tract from the retina. Among the various target areas of the SCN, the parvocellular part of the PVN is a region especially important because it plays a role in autonomic functions that are influenced by circadian rhythins. For example, light stimulation modifies the autonomic nervous system in rats via the SCN and via further projection to the parvocellular part of the PVN. As mentioned above, the parvocellular part of the PVN is also the site responsible for the yawning response, a behavior known to be influenced by the circadian rhythm. Therefore, the light signal may first be transmitted from the retina to the SCN, which in turn projects to the PVN, then mediating the yawning response.
 
Our hypothesis that the light-induced yawning response is mediated by signals conveyed from the retina to the SCN and further to the PVN is also supported by several pieces of histological evidence. Daikoku et al. reported that in rats light exposure induces a remarkable enhancement of c-fos immunoreactivity in neurons within the SCN and the parvocellular part of the PVN. More evidence comes from the observation that light induces c-fos expression in the SCN output neurons targeting the PVN [. Although not directly to the stress-related area of the PVN, Buijs et al. showed projections from the SCN to the periventricular and rostral PVN together with the dorsomedial hypothalamus, the regions known to project into the PVN, and proposed a mechanism that input from the SCN to the PVN could be influenced by either stress or environmental factors, such as light.
 
Although we suggest that the signals from the retina to the SCN and further projection to the PVN is responsible for the light-induced yawning response, we cannot exclude the possibility that other inputs to the PVN may mediate this response. For instance, signals conveyed from the retina to the superior colliculuspretectum, another region known to be involved in light perception, could be related to this response, but until now there has been no report showing direct projection from the superior colliculus-pretectum to the PVN.
 
As to neurotransmission from the SCN to the PVN, several transmitters have been reported. The most essential one is the vasoactive intestinal polypeptide (VIP) of the SCN which plays a role in the control of the autonomie nervous system. Subsequently, VIP as well as gastrin-releasing peptide was shown to be involved in the light-activated output neurons of the SCN. On the other hand, glutamate and GABA were shown to mediate rapid neurotransmission from the SCN to the parvocellular region of the PVN in rats. Considering our previous data showing that microinjection Of L-glutamate induces an arousal yawning response, L-glutamate might be one neurotransmitter mediating the light-induced response in the present study. Nevertheless, the possibility of other transmitters, especially VIP, being involved in this response still needs clarification.
 
We demonstrated that light stimulation induces the yawning response together with an arousal shift in the ECoG, which suggests that the PVN is involved not only in the light-induced yawning response but also in the light-induced cortical activation. The role of the PVN in arousal regulation has been consistently reported in our previous studies. For example, the PVN mediates the arousal pathway induced by higher brain ischemia. It is also suggested that the PVN plays an important role in the arousal responses evoked by orexinergic as well as histaminergic neurotransmissien. We have suggested that the projection from the PVN to the basal forebrain or the locus coeruleus could account for the cortical activation. In all of these studies, a yawning behavior accompanied the arousal response, which indicates that the PVN mediates the cortical activation related to the yawning behavior. In view of these notions, the light-induced arousal response observed in the present study may be mediated by inputs from the retina to the SCN, then projecting to the parvocellular region of the PVN, which in turn sends efferents to the basal forebrain as well as the locus coeruleus to cause cortical activation.
 
Since the PVN is a region implicated in stress responses, it may also be involved in cortical activation induced by various stressors. In this regard, the bright light used in the present study can be regarded as a kind of novel stress. Although not directly related, it should be noted that anatomical projections of the SCN to stress-related areas of the PVN have been reported and connections between the SCN and PVN are affected by stress.
 
A unique aspect of the yawning response is that a depressor response always precedes the final yawning event (a single large inspiratory effort) induced by light stimulation. The reduction in autonomie responses by light stimulation is supported by recent data of Scheer et al. who demonstrated a reduction in HR after light exposure in rats. One may raise a question whether the depressor response observed in the present study by light stimulation might be an arousal response or rather the reverse as could be inferred from the fact that light in nocturnal rodents suppresses activity. In this concern, we observed an arousal shift in the ECoG concurrent with the depressor response in the present study. In addition, we reported in our previous studies that the depressor/arousal response occurs not only by light stimulation but also by local hypoxia of the PVN as well as the yawning responses induced by L-glutamate, nitric oxide donor or orexin. As we mentioned above, the yawning response together with the depressor response may be mediated by the oxytocinergic PVN neurons descending to the lower brain stem. On the other hand, the arousal response induced by light stimulation may be mediated by ascending pathway from the PVN to areas responsible for cortical activation. Corticotropin-releasing factor (CRF) neurons within the PVN could be nominated for such ascending pathway, however this is not yet clear and we are currently examining this possibility.
 
Histamine is a neurotransmitter involved in yawning as well as in the arousal system. It has also been suggested that histamine participates in the regulation of the circadian rhythm. Although histamine-containing neuronal cell bodies are restricted to the hypothalamic tuberomammillary nucleus (TM), there is a high concentration of histamine in the SCN. Indeed anatomically, fibers are known to arise in the TM and project to the SCN. These facts give rise to the suggestion that histamine participates in the regulation of the circadian rhythm. In this study we examined whether histamine could modify the light-induced arousal yawning response. Pretreatment with HI-histamine receptor antagonist in the lateral ventricle blocked the light-induced yawning as well as the cortical activation, indicating that these responses are modified by histamine neurotransmission. It has been shown that histamine has excitatory and inhibitory effects on neurons in the SCN. Whereas the excitatory effect of histamine is mediated by the HI receptor in the SCN, the inhibitory effect is mediated by the H2 receptor. Therefore, the neurons responsible for the light-induced arousal yawning response within the SCN could have been blocked by HI antagonist in the present study.
 
Administration of HI antagonist into the lateral ventricle caused a shift to slower waves in the ECoG which is consistent with the studies using mepyramine, another HI-histamine receptor antagonist, causing an increase in cortical slow waves. These data are also consistent with the sedation and drowsiness caused in man by antihistaminics, together confirming the role of histaminergic neurotransmission in arousal regulation.
 
In conclusion, light stimulation elicited a yawning response together with cortical activation. Since yawning is a behavior mediated through the PVN, the results suggest that the light-induced yawning response as well as the arousal response is mediated by signals from the retina to the SCN and further projection to the PVN. These findings further strengthen our hypothesis that the PVN plays a significant role in the arousal mechanism related to, yawning.
light
-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. Lettre 2008; 
-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.Beh Brain Res 2000; 117; 1-2; 119 - 126
-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, YSeki, M Oguri, H Arita Cortical arousal induced by microinjection of orexins into the paraventricular nucleus of the rat Behav Brain Res 2002; 128; 169-177
-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.
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Tous les travaux de MR Melis & A Argiolas 
Tous les travaux de M Eguibar & G Holmgren
Modulation by sudden darkness of apomorphine-induced behavioral responses Nasello AG et al
Apomorphine induced yawning in the rat : influence of fasting and time of day Naselo AG et al