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Enteric co-innervation of motor endplates in the esophagus: state of the art ten years after

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Abstract

The existence of a distinct ganglionated myenteric plexus between the two layers of the striated tunica muscularis of the mammalian esophagus represented an enigma for quite a while. Although an enteric co-innervation of vagally innervated motor endplates in the esophagus has been repeatedly suggested, it was not possible until recently to demonstrate this dual innervation. Ten years ago, we were able to demonstrate that motor endplates in the rat esophagus receive a dual innervation from both vagal nerve fibers originating in the brain stem and from varicose enteric nerve fibers originating in the myenteric plexus. Since then, a considerable amount of data could be raised on enteric co-innervation and its occurrence in a variety of species, including humans, its neurochemistry, spatial relationships on motor endplates, ontogeny, and possible roles during esophageal peristalsis. These data underline the significance of this newly discovered innervation component, although its function is still largely unknown. The aim of this review is to summarize current knowledge about enteric co-innervation of esophageal striated muscle and to provide some hints as to its functional significance.

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Abbreviations

ACh:

acetylcholine

AChE:

acetylcholinesterase

AChR:

acetylcholine receptor

AMB:

nucleus ambiguus

α-BT:

α-Bungarotoxin

CGRP:

calcitonin gene-related peptide

cNTS:

central subnucleus of the nucleus tractus solitarius

CS:

cryosections

co rate:

co-innervation rate

DEA-NO:

diethylamine-NO

DiI:

1,1′-dioleyl-3,3,3′,3′-tetramethylindocarbocyanine methane sulfonate

DRG:

dorsal root ganglion

EH:

enzyme histochemistry

ENF:

enteric nerve fibers

GAL:

galanin

Glu:

glutamate

IGLEs:

intraganglionic laminar endings

IH:

immunocytochemistry

L-ENK:

Leu-enkephalin

LES:

lower esophageal sphincter

L-NNA:

Nω-Nitro-L-arginine

mAChRs:

muscarinic acetylcholine receptors

M1, M2:

muscarinic acetylcholine receptor subtype M1 and M2

M-ENK:

Met-enkephalin

MEP:

motor endplate

MF:

muscle fiber

MG:

myenteric ganglion

NADPH-d:

NADPH-diaphorase

NKA:

neurokinin A

NO:

nitric oxide

NOD:

nodose ganglion

nNOS:

neuronal nitric oxide synthase

NPY:

neuropeptide Y

PACAP:

pituitary adenylyl cyclase-activating (poly)peptide

SC:

swallowing center

sGC:

soluble guanylyl cyclase

SP:

substance P

Tm-i, Tm-o:

tunica muscularis, inner and outer muscle layer

Tmuc:

tunica mucosa

Tsubm:

tela submucosa

UES:

upper esophageal sphincter

VAChT:

vesicular acetylcholine transporter

VIP:

vasoactive intestinal (poly)peptide

WM:

whole mounts

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Acknowledgements

Research in the authors’ laboratory has been supported by “Johannes und Frieda Marohn-Stiftung”, Erlangen.

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Wörl, J., Neuhuber, W.L. Enteric co-innervation of motor endplates in the esophagus: state of the art ten years after. Histochem Cell Biol 123, 117–130 (2005). https://doi.org/10.1007/s00418-005-0764-7

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