Enteric descending and afferent neural signaling stimulated by giant migrating contractions: Essential contributing factors to visceral pain

Sushil K. Sarna

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

We investigated whether strong compression of an intestinal segment by giant migrating contractions (GMCs) initiates pseudoaffective signals from the gut, similar to those initiated by its distension with a balloon. The experiments were performed on conscious dogs by using close intra-arterial infusions of test substances that affect the receptors only in the infused segment. The stimulation of GMCs by close intra-arterial infusion of CGRP or distension of an intestinal segment by balloon increased the heart rate; the increase in heart rate was greater when the balloon distension and GMCs occurred concurrently in separate intestinal segments. The suppression of contractility in the distended segment blocked the increase in heart rate. By contrast, the stimulation of rhythmic phasic contractions (RPCs) or their spontaneous occurrence did not increase the heart rate. The occurrence of GMCs as well as intestinal distension also produced descending inhibition. The descending inhibition was blocked by the inhibition of nitric oxide synthase, but it was unaffected by the inhibition of adenylyl cyclase, purinergic receptors P2X and P2Y, and muscarinic receptors M1 and M2. The synaptic transmission for descending inhibition was mediated primarily by nicotinic receptors and activation of nitric oxide synthase. It was unaffected by the inhibition of tachykinin receptors NK1, NK2, and NK 3; serotonin receptors 5-HT1A, 5-HT2/5-HT 1C, 5-HT3, and 5-HT4; and muscarinic receptors. Our findings show that GMCs, but not RPCs, initiate pseudoaffective signals from the gut. In the presence of visceral hypersensitivity or impaired descending inhibition, the GMCs may become a noxious stimulus.

Original languageEnglish (US)
JournalAmerican Journal of Physiology - Gastrointestinal and Liver Physiology
Volume292
Issue number2
DOIs
StatePublished - Feb 2007

Fingerprint

Visceral Pain
Heart Rate
Intra Arterial Infusions
Nitric Oxide Synthase
Serotonin
Purinergic P2Y Receptors
Purinergic P2X Receptors
Neurokinin-3 Receptors
Receptors, Serotonin, 5-HT4
Muscarinic M2 Receptors
Muscarinic M1 Receptors
Tachykinin Receptors
Nicotinic Receptors
Muscarinic Receptors
Adenylyl Cyclases
Synaptic Transmission
Hypersensitivity
Dogs

Keywords

  • Constipation
  • Functional bowel disorders
  • High-amplitude propagating contractions
  • Inflammatory bowel disease
  • Irritable bowel syndrome
  • Nitric oxide
  • Peristaltic reflex
  • Vasoactive intestinal peptide

ASJC Scopus subject areas

  • Gastroenterology
  • Physiology

Cite this

@article{a127d98aad43469a8de474d2bbf8098f,
title = "Enteric descending and afferent neural signaling stimulated by giant migrating contractions: Essential contributing factors to visceral pain",
abstract = "We investigated whether strong compression of an intestinal segment by giant migrating contractions (GMCs) initiates pseudoaffective signals from the gut, similar to those initiated by its distension with a balloon. The experiments were performed on conscious dogs by using close intra-arterial infusions of test substances that affect the receptors only in the infused segment. The stimulation of GMCs by close intra-arterial infusion of CGRP or distension of an intestinal segment by balloon increased the heart rate; the increase in heart rate was greater when the balloon distension and GMCs occurred concurrently in separate intestinal segments. The suppression of contractility in the distended segment blocked the increase in heart rate. By contrast, the stimulation of rhythmic phasic contractions (RPCs) or their spontaneous occurrence did not increase the heart rate. The occurrence of GMCs as well as intestinal distension also produced descending inhibition. The descending inhibition was blocked by the inhibition of nitric oxide synthase, but it was unaffected by the inhibition of adenylyl cyclase, purinergic receptors P2X and P2Y, and muscarinic receptors M1 and M2. The synaptic transmission for descending inhibition was mediated primarily by nicotinic receptors and activation of nitric oxide synthase. It was unaffected by the inhibition of tachykinin receptors NK1, NK2, and NK 3; serotonin receptors 5-HT1A, 5-HT2/5-HT 1C, 5-HT3, and 5-HT4; and muscarinic receptors. Our findings show that GMCs, but not RPCs, initiate pseudoaffective signals from the gut. In the presence of visceral hypersensitivity or impaired descending inhibition, the GMCs may become a noxious stimulus.",
keywords = "Constipation, Functional bowel disorders, High-amplitude propagating contractions, Inflammatory bowel disease, Irritable bowel syndrome, Nitric oxide, Peristaltic reflex, Vasoactive intestinal peptide",
author = "Sarna, {Sushil K.}",
year = "2007",
month = "2",
doi = "10.1152/ajpgi.00332.2006",
language = "English (US)",
volume = "292",
journal = "American Journal of Physiology - Endocrinology and Metabolism",
issn = "0193-1849",
publisher = "American Physiological Society",
number = "2",

}

TY - JOUR

T1 - Enteric descending and afferent neural signaling stimulated by giant migrating contractions

T2 - Essential contributing factors to visceral pain

AU - Sarna, Sushil K.

PY - 2007/2

Y1 - 2007/2

N2 - We investigated whether strong compression of an intestinal segment by giant migrating contractions (GMCs) initiates pseudoaffective signals from the gut, similar to those initiated by its distension with a balloon. The experiments were performed on conscious dogs by using close intra-arterial infusions of test substances that affect the receptors only in the infused segment. The stimulation of GMCs by close intra-arterial infusion of CGRP or distension of an intestinal segment by balloon increased the heart rate; the increase in heart rate was greater when the balloon distension and GMCs occurred concurrently in separate intestinal segments. The suppression of contractility in the distended segment blocked the increase in heart rate. By contrast, the stimulation of rhythmic phasic contractions (RPCs) or their spontaneous occurrence did not increase the heart rate. The occurrence of GMCs as well as intestinal distension also produced descending inhibition. The descending inhibition was blocked by the inhibition of nitric oxide synthase, but it was unaffected by the inhibition of adenylyl cyclase, purinergic receptors P2X and P2Y, and muscarinic receptors M1 and M2. The synaptic transmission for descending inhibition was mediated primarily by nicotinic receptors and activation of nitric oxide synthase. It was unaffected by the inhibition of tachykinin receptors NK1, NK2, and NK 3; serotonin receptors 5-HT1A, 5-HT2/5-HT 1C, 5-HT3, and 5-HT4; and muscarinic receptors. Our findings show that GMCs, but not RPCs, initiate pseudoaffective signals from the gut. In the presence of visceral hypersensitivity or impaired descending inhibition, the GMCs may become a noxious stimulus.

AB - We investigated whether strong compression of an intestinal segment by giant migrating contractions (GMCs) initiates pseudoaffective signals from the gut, similar to those initiated by its distension with a balloon. The experiments were performed on conscious dogs by using close intra-arterial infusions of test substances that affect the receptors only in the infused segment. The stimulation of GMCs by close intra-arterial infusion of CGRP or distension of an intestinal segment by balloon increased the heart rate; the increase in heart rate was greater when the balloon distension and GMCs occurred concurrently in separate intestinal segments. The suppression of contractility in the distended segment blocked the increase in heart rate. By contrast, the stimulation of rhythmic phasic contractions (RPCs) or their spontaneous occurrence did not increase the heart rate. The occurrence of GMCs as well as intestinal distension also produced descending inhibition. The descending inhibition was blocked by the inhibition of nitric oxide synthase, but it was unaffected by the inhibition of adenylyl cyclase, purinergic receptors P2X and P2Y, and muscarinic receptors M1 and M2. The synaptic transmission for descending inhibition was mediated primarily by nicotinic receptors and activation of nitric oxide synthase. It was unaffected by the inhibition of tachykinin receptors NK1, NK2, and NK 3; serotonin receptors 5-HT1A, 5-HT2/5-HT 1C, 5-HT3, and 5-HT4; and muscarinic receptors. Our findings show that GMCs, but not RPCs, initiate pseudoaffective signals from the gut. In the presence of visceral hypersensitivity or impaired descending inhibition, the GMCs may become a noxious stimulus.

KW - Constipation

KW - Functional bowel disorders

KW - High-amplitude propagating contractions

KW - Inflammatory bowel disease

KW - Irritable bowel syndrome

KW - Nitric oxide

KW - Peristaltic reflex

KW - Vasoactive intestinal peptide

UR - http://www.scopus.com/inward/record.url?scp=33847021192&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33847021192&partnerID=8YFLogxK

U2 - 10.1152/ajpgi.00332.2006

DO - 10.1152/ajpgi.00332.2006

M3 - Article

C2 - 16990445

AN - SCOPUS:33847021192

VL - 292

JO - American Journal of Physiology - Endocrinology and Metabolism

JF - American Journal of Physiology - Endocrinology and Metabolism

SN - 0193-1849

IS - 2

ER -