Polarized enteric submucosal circuits involved in secretory responses of the guinea-pig proximal colon

Michel Neunlist, Thomas Frieling, Claudia Rupprecht, Michael Schemann

Research output: Contribution to journalArticlepeer-review

40 Scopus citations

Abstract

1. Neuronal retrograde tracing with the dye DiI(1,1'-didodecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate), in combination with immunohistochemical detection of choline acetyltransferase (ChAT) and vasoactive intestinal peptide (VIP), were used to identify the innervation of the mucosa of the guinea-pig proximal colon by submucosal neurones. Ussing evoked by electrical stimulation of the oral or anal end of the preparation. 2. The tracing studies revealed that the mucosa was primarily innervated by descending neurones (78%); the vast majority of these were VIP positive (85%). The numerically smaller ascending pathway (13%) was predominantly ChAT positive (69%). A small population (9%) of DiI-labelled neurones projected circumferentially. 3. Ussing chamber experiments revealed that oral electrical stimulation induced a significantly larger ΔI(sc) than anal stimulation. The VIP antagonist VIP(6-28) significantly reduced only orally induced ΔI(sc). Anally induced ΔI(sc) were significantly more atropine sensitive that orally induced ΔI(sc). Tissue incubation with carbachol or VIP significantly potentiated ΔI(sc) induced by VIP and carbachol, respectively, indicating cross-potentiation. 4. This study provides the first functional demonstration of polarized innervation patterns from submucosal neurones to enteric mucosa. The ascending ChAT and descending VIP pathways suggest the existence of reflexes resulting in preferential release of VIP or acetylcholine. The distinct pathways might favour the observed cross-potentiation of cholinergic and VIPergic mediated secretion.

Original languageEnglish
Pages (from-to)539-550
Number of pages12
JournalJournal of Physiology
Volume506
Issue number2
DOIs
StatePublished - 15 Jan 1998
Externally publishedYes

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