Bidirectional brain‐gut interactions: Involvement of noradrenergic transmission within the ventral part of the bed nucleus of the stria terminalis

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Aims The bed nucleus of the stria terminalis (BNST) is a limbic structure mediating autonomic and neuroendocrine responses and negative affective states such as anxiety and fear. We previously demonstrated that noradrenergic transmission via β‐adrenoceptors within the ventral part of BNST (vBNST) is involved in bidirectional interactions between the brain and the upper gastrointestinal (GI) tract. The present study aimed to examine the roles of intra‐vBNST noradrenergic transmission via β‐adrenoceptors in bidirectional interactions between the brain and lower GI tract. Methods In vivo microdialysis experiments were performed to examine colorectal distention (CRD)‐induced noradrenaline release within the vBNST of freely moving male Sprague‐Dawley rats. Colonic transit and abdominal pain perception were examined following intra‐vBNST injections of isoproterenol, a β‐adrenoceptor agonist, with and without co‐administration of timolol, a β‐adrenoceptor antagonist. Results CRD increased extracellular noradrenaline levels within the vBNST and evoked abdominal contractions in a pressure‐dependent manner (30‐60 mm Hg). Bilateral intra‐vBNST injections of isoproterenol (30 nmol/side) significantly increased CRD (30 mm Hg)‐induced abdominal contractions. Intra‐vBNST injections of isoproterenol (30 nmol/side) significantly increased colonic transit, which was reversed by co‐administration of timolol (30 nmol/side). Conclusion The results of this study suggest (a) the existence of a positive feedback loop between intra‐vBNST noradrenaline release and abdominal pain perception, and (b) the modulation of colonic motility by intra‐vBNST noradrenergic transmission via β‐adrenoceptors. Dysfunction of the lower GI tract may increase noradrenaline release within the vBNST, which, in turn, may exacerbate impairment of its motility and pain perception.

Section: Discussionsupporting

confidence: 90%

Section: Discussionsupporting

confidence: 76%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 98%

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Roles of noradrenergic transmission within the ventral part of the bed nucleus of the stria terminalis in bidirectional brain‐intestine interactions

Ide

Yamamoto

Suzuki

et al. 2018

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Bidirectional brain‐gut interactions: Involvement of noradrenergic transmission within the ventral part of the bed nucleus of the stria terminalis

Ide

Yamamoto

Takeda

et al. 2018

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Exposure to hot and cold environments increases noradrenaline release in the bed nucleus of the stria terminalis in rats

Minami

Nomura

Minami

2018

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Aims Thermoregulatory responses in homeothermic animals, including humans, are classified into involuntary autonomous and voluntary behavioral thermoregulatory responses. Although behavioral thermoregulatory responses are probably driven by positive (pleasant) and/or negative (unpleasant) emotions, the neuronal mechanisms underlying the induction of negative emotions by hot and cold environments remain poorly understood. The bed nucleus of the stria terminalis is a brain region implicated in stress responses and negative emotions, such as fear, anxiety, and aversion. Various stimuli that cause negative emotions, such as immobilization stress, fox odor, gastric distension, and inflammatory pain, increase noradrenaline release in the rat bed nucleus of the stria terminalis, especially in the ventral bed nucleus of the stria terminalis. It has been reported that the negative emotional component of pain is mediated by noradrenergic neurotransmission in the ventral bed nucleus of the stria terminalis. However, the role of intra‐ventral bed nucleus of the stria terminalis noradrenergic neurotransmission in the induction of negative emotion by exposure to hot and cold environments remains to be elucidated. For the first step to address this issue, the effects of hot and cold environments on noradrenaline release in the ventral bed nucleus of the stria terminalis were examined. Methods In vivo microdialysis analyses in unanesthetized, freely moving male Sprague‐Dawley rats were performed to examine hot and cold environments‐induced noradrenaline release in the ventral bed nucleus of the stria terminalis. Results Exposure to hot (38°C) and cold (8°C) environments significantly increased noradrenaline release in the ventral bed nucleus of the stria terminalis. Conclusions The results suggest that exposure to hot and cold environments enhances noradrenergic neurotransmission in the ventral bed nucleus of the stria terminalis, which may induce negative emotion, and thereby drive avoidance behaviors, that is, escape from hot and cold environments.