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Neural components of distension-evoked secretory responses in the guinea-pig distal colon

Eckhard Weber, Michel Neunlist *, Michael Schemann * and Thomas Frieling

1. Using a Ussing chamber and neuronal retrograde tracing with 1,1'-didodecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (DiI) we characterized the afferent and efferent neuronal pathways which mediated distension-evoked secretion in the guinea-pig distal colon.
2. Acute capsaicin application (10 µM) to the serosal site of the Ussing chamber evoked a secretory response which was blocked by tetrodotoxin (1 µM), the combined application of the NK1 and NK3 receptor antagonists CP-99,994-1 and SR 142801 (1 µM), and by combined application of atropine (10 µM) and the VIP receptor antagonist VIP(6-28) (10 µM). Functional desensitization of extrinsic primary afferents by long-term application of capsaicin significantly diminished distension-evoked secretion by 46 %.
3. After functional desensitization by capsaicin, serosal application of gadolinium (100 µM) inhibited the distension-evoked chloride secretion by 54 %; the L-type Ca²⁺ channel blocker nifedipine (1 µM) and the 5-HT_1P receptor antagonist renzapride (1 µM) had no effect. The combination of atropine and VIP(6-28) or the combination of NK1 and NK3 receptor antagonists almost abolished distension-evoked secretion.
4. The secretory response evoked by electrical field stimulation, carbachol (1 µM) or VIP (1 µM) was not attenuated by gadolinium. Field stimulation-evoked chloride secretion was not affected by blockade of NK1 and NK3 receptors.
5. Twelve per cent of DiI-labelled submucosal neurones with projections to the mucosa were immunoreactive for choline acetyltransferase, substance P and calbindin and very probably represented intrinsic primary afferent neurones.
6. Distension-evoked chloride secretion was mediated by capsaicin-sensitive extrinsic primary afferents and by stretch-sensitive intrinsic primary afferent neurones. Both the extrinsic and intrinsic afferents converge on common efferent pathways. These pathways consist of VIPergic and cholinergic secretomotor neurones that are activated via NK1 and NK3 receptors.

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