Neuronal pathways and transmission to the lower esophageal sphincter of the guinea pig

doi:10.1016/S0016-5085(98)70145-3

Gastroenterology

Volume 115, Issue 3, September 1998, Pages 661-671

https://doi.org/10.1016/S0016-5085(98)70145-3 Get rights and content

Abstract

Background & Aims: The lower esophageal sphincter (LES) normally controls the opening and closing of the gastroesophageal junction to resist gastric reflux but allow swallowing. Neuronal pathways controlling the guinea pig LES were investigated anatomically and physiologically in isolated preparations. Methods: Intracellular recording from the LES with focal electrical stimulation and retrograde and anterograde neuronal tracing were used. Results: Electrical stimulation on the LES evoked inhibitory junction potentials (IJPs), which were reduced by 60% by 100 μmol/L N-nitro-L-arginine and subsequently blocked by 0.5 μmol/L apamin, unmasking excitatory junction potentials, which were abolished by 1 μmol/L hyoscine. Esophageal or vagal stimulation evoked IJPs, which were blocked by 100 μmol/L hexamethonium. Focal stimulation of the upper stomach evoked IJPs at 5–8 of 20 stimulation sites, which were abolished by cutting between the stimulation site and sphincter. Application of 1,1'-didodecyl-3,3,3',3'-tetramethyl indocarbocyanine perchlorate (DiI) to the gastric sling muscle anterogradely labeled many motor axons in the sling muscle but few in the LES, confirming that the two muscles are separately innervated. DiI on the esophagus labeled nerve fibers, but not cell bodies, in the upper stomach. Conclusions: The inhibitory motor neurons of the LES receive inputs from the vagus nerve, esophagus, and upper stomach.

GASTROENTEROLOGY 1998;115:661-671

Section snippets

Materials and methods

Guinea pigs of both sexes, weighing between 250 and 350 g, were killed in a manner approved by the institutional Animal Ethnics Committee, by cervical dislocation, followed by bleeding from the carotid arteries. The stomach with 3-cm-long esophagus and vagus nerves attached was quickly removed and placed in a Petri dish filled with modified Krebs' solution (composition as follows [in mmol/L]: NaCl, 118; KCl, 4.7; MgSO₄, 1.2; NaHCO₃, 25; NaH₂PO₄, 1.0; CaCl₂, 2.5; and D-glucose, 11). The antrum

Results

After removal of the muscosa, the regions of the smooth and striated muscle layers of the esophagus, LES, and stomach could be observed clearly under the dissecting microscope. The esophageal body appeared to be composed entirely of striated muscle, which had a distinctive pale pink color that abruptly changed to a pale silvery grey color in the thickened smooth muscle of the LES. The gastric smooth muscle aboral to the LES very closely resembled the color of the LES and was recognized by the

Discussion

This study, for the first time using intracellular recording techniques, has shown that the guinea pig LES receives strong inhibitory inputs from enteric inhibitory motor neurons, as previously reported in the guinea pig⁴⁰ and in other species1, 7, 8, 9, 10, 41, 42, 43 using tension or intraluminal pressure recording. The results are also consistent with a recent anatomic study using retrograde tracing and immunohistochemistry.¹¹ The relatively positive resting membrane potentials of the smooth

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^☆: Address requests for reprints to: Shiyong Yuan, Ph.D., Department of Human Physiology and Centre for Neuroscience, Flinders University, G.P.O. Box 2100, Adelaide, South Australia 5001, Australia. Fax: (61) 8-8204-5768.

^☆☆: Supported by a grant from the National Health and Medical Research Council of Australia. Dr. Brookes was supported by a Senior Research Fellowship in Digestive Science from the Gastroenterological Society of Australia.

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Alimentary TractNeuronal pathways and transmission to the lower esophageal sphincter of the guinea pig☆,☆☆

Abstract

Section snippets

Materials and methods

Results

Discussion

Gastroenterology

Gastroenterology

Gastroenterology

J Auton Nerv Syst

J Auton Nerv Syst

J Auton Nerv Syst

Neuroscience

Neuroscience

J Auton Nerv Syst

J Auton Nerv Syst

Euro J Pharmacol

J Auton Nerv Syst

J Auton Nerv Syst

Comp Biochem Physiol

Prog Neurobiol

Baillieres Clin Endocrinol Metab

Neuroscience

Gastroenterology

Neurosci Lett

Gastroenterology

Gastroenterology

Sphincteric function

Esophageal motility

Motor functions of the pharynx and esophagus

Esophageal motor function

The role of the L-arginine-nitric oxide pathway in relaxation of the opossum lower oesophageal sphincter

Br J Pharmacol

Nitric oxide: mediator of nonadrenergic noncholinergic responses of opossum esophageal muscle

Am J Physiol

The role of nitric oxide in inhibitory non-adrenergic, non-cholinergic neurotransmission in the canine lower oesophageal sphincter

Br J Pharmacol

The role of the L-arginine/nitric oxide pathway for relaxation of the human lower oesophageal sphincter

Acta Physiol Scand

Transmission from intramural excitatory nerves to the smooth muscle cells of the guinea-pig taenia coli

J Physiol

An electrophysiological study of the innervation of the smooth muscle of the colon

J Physiol

Conductance change during the inhibitory potential in the guinea-pig taenia coli

J Physiol

Evidence for non-cholinergic, non-adrenergic transmission in the guinea-pig ileum

J Physiol

Neurogenic slow depolarizations and rapid oscillations in the membrane potential of circular muscle of mouse colon

J Physiol

Role of extra- and intracellular calcium in the contractile action of agonists in the guinea-pig ileum

Naunyn Schmiedebergs Arch Pharmacol

Alimentary Tract
Neuronal pathways and transmission to the lower esophageal sphincter of the guinea pig☆,☆☆