Gastric distension-induced release of 5-HT stimulates c-fos expression in specific brain nuclei via 5-HT3 receptors in conscious rats

Dec 20, 2003American journal of physiology. Gastrointestinal and liver physiology

Stomach stretching causes serotonin release that activates certain brain areas through 5-HT3 receptors in awake rats

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Abstract

Gastric distension stimulated the release of 5-HT more from the vascular system than from the stomach's lumen.

Gastric distension induced c-fos expression in several brain regions, including the nucleus of the solitary tract, area postrema, paraventricular nucleus, and supraoptic nucleus.
The c-fos expression was blocked by truncal vagotomy and perivagal capsaicin treatment, indicating the involvement of vagal afferent pathways.
Intravenous injection of the 5-HT3 receptor antagonist granisetron inhibited c-fos expression in all examined brain nuclei.
Intracerebroventricular injection of granisetron did not affect c-fos expression, suggesting a peripheral role for the 5-HT3 receptors.
5-HT released from the stomach may activate peripheral 5-HT3 receptors on vagal afferent nerve terminals, leading to neuronal activation in the brain.

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We examined c-fos expression in specific brain nuclei in response to gastric distension and investigated whether 5-HT released from enterochromaffin (EC) cells was involved in this response. The role of 5-HT3 receptors in this mechanism was also addressed. Release of 5-HT was examined in an ex vivo-perfused stomach model, whereas c-fos expression in brain nuclei induced by gastric distension was examined in a freely moving conscious rat model. Physiological levels of gastric distension stimulated the vascular release of 5-HT more than luminal release of 5-HT, and induced c-fos expression in the nucleus of the solitary tract (NTS), area postrema (AP), paraventricular nucleus (PVN), and supraoptic nucleus (SON). The c-fos expression in all these brain nuclei was blocked by truncal vagotomy as well as by perivagal capsaicin treatment, suggesting that vagal afferent pathways may mediate this response. Intravenous injection of 5-HT3 receptor antagonist granisetron blocked c-fos expression in all brain nuclei examined, although intracerebroventricular injection of granisetron had no effect, suggesting that 5-HT released from the stomach may activate 5-HT3 receptors located in the peripheral vagal afferent nerve terminals and then induce brain c-fos expression. c-fos Positive cells in the NTS were labeled with retrograde tracer fluorogold injected in the PVN, suggesting that neurons in the NTS activated by gastric distension project axons to the PVN. The present results suggest that gastric distension stimulates 5-HT release from the EC cells and the released 5-HT may activate 5-HT3 receptors located on the vagal afferent nerve terminals in the gastric wall leading to neuron activation in the NTS and AP and subsequent activation of neurons in the PVN and SON.

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Gastric distension-induced release of 5-HT stimulates c-fos expression in specific brain nuclei via 5-HT3 receptors in conscious rats

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