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Enteric co-innervation of striated muscle in the esophagus: still enigmatic?

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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 has represented an enigma for quite a while. Although an enteric co-innervation of vagally innervated motor endplates in the esophagus has been suggested repeatedly, it was not possible until recently to demonstrate this dual innervation. Twenty-two years ago, we were able to demonstrate that motor endplates in the rat esophagus receive dual innervation from both vagal nerve fibers originating in the brain stem and from varicose enteric nerve fibers originating in the myenteric plexus. Meanwhile, a considerable amount of data has been gathered on enteric co-innervation and its occurrence in the esophagus of a variety of species including humans, its neurochemistry, spatial relationships on motor endplates, ontogeny and possible functional roles. These data underline the significance of this newly discovered innervation component, although its function in vivo is still largely unknown. The aim of this review, which is an update of our previous paper (Wörl and Neuhuber in Histochem Cell Biol 123(2):117–130. doi:10.1007/s00418-005-0764-7, 2005a), is to summarize the current knowledge about enteric co-innervation of esophageal striated muscle and to provide some hints as to its functional significance.

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Modified from Breuer et al. (2004), with permission of the publisher

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Abbreviations

ACh:

Acetylcholine

AChE:

Acetylcholinesterase

AChR:

Acetylcholine receptor

AMB:

Nucleus ambiguus

α-BT:

α-Bungarotoxin

CGRP:

Calcitonin gene-related peptide

CLR:

Calcitonin-receptor-like receptor

cNTS:

Central subnucleus of the nucleus tractus solitarii

CS:

Cryosections

Co rate:

Co-innervation rate

DiI:

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

DBH:

Dopamine-β-hydroxylase

DMX:

Dorsal motor nucleus of the vagus nerve

DRG:

Dorsal root ganglion

E17:

Embryonic day 17

EH:

Enzyme histochemistry

ENF:

Enteric nerve fibers

GAL:

Galanin

Glu:

Glutamate

IGLEs:

Intraganglionic laminar endings

IH:

Immunocytochemistry

L-ENK:

Leu-enkephalin

3mo:

3 Months

M-ENK:

Met-enkephalin

MEP:

Motor endplate

MF:

Muscle fiber

MG:

Myenteric ganglion

NADPH-d:

NADPH-diaphorase

NKA:

Neurokinin A

NOD:

Nodose ganglion

nNOS:

Neuronal nitric oxide synthase

NPY:

Neuropeptide Y

P4, -7, -14:

Postnatal day 4, 7, 14

PACAP:

Pituitary adenylyl cyclase-activating (poly)peptide

RAMP1:

Receptor-activity-modifying protein 1

SC:

Swallowing center

SP:

Substance P

Tm-i, Tm-o:

Tunica muscularis, inner and outer muscle layer

Tmuc:

Tunica mucosa

Tsubm:

Tela submucosa

TpH-1 and -2:

Tryptophan hydroxylase 1 and 2

TRPV1:

Transient receptor potential ion channel of the vanilloid type 1

TH:

Tyrosine hydroxylase

VAChT:

Vesicular acetylcholine transporter

VIP:

Vasoactive intestinal (poly)peptide

WM:

Whole mounts

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Acknowledgements

The research conducted in the authors’ laboratory has been supported by the “Johannes und Frieda Marohn-Stiftung” (Wö/04) and ELAN Fonds (04.08.07.1) to Dr. Christian Breuer and J. W., Erlangen, a travel grant to J. W. from the Chihiro and Kiyoko Yokochi Fund, Kanehara Ichiro Foundation in Tokyo, Japan and the Deutsche Forschungsgemeinschaft (NE 534/3-1).

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  1. Institut für Anatomie I, Friedrich-Alexander Universität Erlangen-Nürnberg, Krankenhausstraße 9, 91054, Erlangen, Germany

    Winfried L. Neuhuber & Jürgen Wörl

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  1. Winfried L. Neuhuber
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  2. Jürgen Wörl
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Correspondence to Winfried L. Neuhuber.

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Dedicated to Prof. Dr. Detlev Drenckhahn.

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Neuhuber, W.L., Wörl, J. Enteric co-innervation of striated muscle in the esophagus: still enigmatic?. Histochem Cell Biol 146, 721–735 (2016). https://doi.org/10.1007/s00418-016-1500-1

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