Naloxone-induced depolarization and synaptic activation of myenteric neurons in morphine-dependent guinea pig ileum

S. M. Johnson, John Williams, M. Costa, J. B. Furness

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

To investigate the cellular basis of opiate dependence, intracellular microelectrodes were used to record from both electrophysiologically defined classes of neurons (S and AH) in myenteric plexus longitudinal muscle preparations from morphine pretreated guinea pigs. These preparations responded to naloxone with the characteristic contraction of the longitudinal smooth muscle, indicative of morphine dependence. Depolarization in response to naloxone was observed in 42% of S neurons, but there were no consistent changes in input resistance. In some cells the depolarization was reduced or abolished after blockade of synaptic transmission, suggesting that it was due in part to the release of an excitatory transmitter producing a slow depolarization in the impaled neuron. Synaptic activation of S neurons during withdrawal was further indicated by the observation that fast postsynaptic potentials appeared after abrupt displacement of morphine from its receptors by naloxone. Morphine withdrawal, therefore, involves both the final motor neurons and interneurons. During naloxone-induced withdrawal, 25% of S neurons discharged action potentials. In contrast, no action potentials were discharged in AH neurons. Furthermore, naloxone did not alter the resting membrane potential, input resistance, soma action potential configuration, or the slow hyperpolarization following a soma spike in AH neurons. The specificity of the withdrawal response for S neurons and the relatively small proportion of neurons involved suggests that morphine withdrawal occurs in quite specific neuronal circuits in the myenteric plexus.

Original languageEnglish (US)
Pages (from-to)595-602
Number of pages8
JournalNeuroscience
Volume21
Issue number2
DOIs
StatePublished - 1987
Externally publishedYes

Fingerprint

Naloxone
Ileum
Morphine
Guinea Pigs
Neurons
Action Potentials
Myenteric Plexus
Carisoprodol
Morphine Dependence
Opioid-Related Disorders
Synaptic Potentials
mu Opioid Receptor
Microelectrodes
Motor Neurons
Interneurons
Synaptic Transmission
Membrane Potentials
Smooth Muscle
Muscles

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Naloxone-induced depolarization and synaptic activation of myenteric neurons in morphine-dependent guinea pig ileum. / Johnson, S. M.; Williams, John; Costa, M.; Furness, J. B.

In: Neuroscience, Vol. 21, No. 2, 1987, p. 595-602.

Research output: Contribution to journalArticle

@article{7cdbac6962964dd0ab152828f87a8128,
title = "Naloxone-induced depolarization and synaptic activation of myenteric neurons in morphine-dependent guinea pig ileum",
abstract = "To investigate the cellular basis of opiate dependence, intracellular microelectrodes were used to record from both electrophysiologically defined classes of neurons (S and AH) in myenteric plexus longitudinal muscle preparations from morphine pretreated guinea pigs. These preparations responded to naloxone with the characteristic contraction of the longitudinal smooth muscle, indicative of morphine dependence. Depolarization in response to naloxone was observed in 42{\%} of S neurons, but there were no consistent changes in input resistance. In some cells the depolarization was reduced or abolished after blockade of synaptic transmission, suggesting that it was due in part to the release of an excitatory transmitter producing a slow depolarization in the impaled neuron. Synaptic activation of S neurons during withdrawal was further indicated by the observation that fast postsynaptic potentials appeared after abrupt displacement of morphine from its receptors by naloxone. Morphine withdrawal, therefore, involves both the final motor neurons and interneurons. During naloxone-induced withdrawal, 25{\%} of S neurons discharged action potentials. In contrast, no action potentials were discharged in AH neurons. Furthermore, naloxone did not alter the resting membrane potential, input resistance, soma action potential configuration, or the slow hyperpolarization following a soma spike in AH neurons. The specificity of the withdrawal response for S neurons and the relatively small proportion of neurons involved suggests that morphine withdrawal occurs in quite specific neuronal circuits in the myenteric plexus.",
author = "Johnson, {S. M.} and John Williams and M. Costa and Furness, {J. B.}",
year = "1987",
doi = "10.1016/0306-4522(87)90145-X",
language = "English (US)",
volume = "21",
pages = "595--602",
journal = "Neuroscience",
issn = "0306-4522",
publisher = "Elsevier Limited",
number = "2",

}

TY - JOUR

T1 - Naloxone-induced depolarization and synaptic activation of myenteric neurons in morphine-dependent guinea pig ileum

AU - Johnson, S. M.

AU - Williams, John

AU - Costa, M.

AU - Furness, J. B.

PY - 1987

Y1 - 1987

N2 - To investigate the cellular basis of opiate dependence, intracellular microelectrodes were used to record from both electrophysiologically defined classes of neurons (S and AH) in myenteric plexus longitudinal muscle preparations from morphine pretreated guinea pigs. These preparations responded to naloxone with the characteristic contraction of the longitudinal smooth muscle, indicative of morphine dependence. Depolarization in response to naloxone was observed in 42% of S neurons, but there were no consistent changes in input resistance. In some cells the depolarization was reduced or abolished after blockade of synaptic transmission, suggesting that it was due in part to the release of an excitatory transmitter producing a slow depolarization in the impaled neuron. Synaptic activation of S neurons during withdrawal was further indicated by the observation that fast postsynaptic potentials appeared after abrupt displacement of morphine from its receptors by naloxone. Morphine withdrawal, therefore, involves both the final motor neurons and interneurons. During naloxone-induced withdrawal, 25% of S neurons discharged action potentials. In contrast, no action potentials were discharged in AH neurons. Furthermore, naloxone did not alter the resting membrane potential, input resistance, soma action potential configuration, or the slow hyperpolarization following a soma spike in AH neurons. The specificity of the withdrawal response for S neurons and the relatively small proportion of neurons involved suggests that morphine withdrawal occurs in quite specific neuronal circuits in the myenteric plexus.

AB - To investigate the cellular basis of opiate dependence, intracellular microelectrodes were used to record from both electrophysiologically defined classes of neurons (S and AH) in myenteric plexus longitudinal muscle preparations from morphine pretreated guinea pigs. These preparations responded to naloxone with the characteristic contraction of the longitudinal smooth muscle, indicative of morphine dependence. Depolarization in response to naloxone was observed in 42% of S neurons, but there were no consistent changes in input resistance. In some cells the depolarization was reduced or abolished after blockade of synaptic transmission, suggesting that it was due in part to the release of an excitatory transmitter producing a slow depolarization in the impaled neuron. Synaptic activation of S neurons during withdrawal was further indicated by the observation that fast postsynaptic potentials appeared after abrupt displacement of morphine from its receptors by naloxone. Morphine withdrawal, therefore, involves both the final motor neurons and interneurons. During naloxone-induced withdrawal, 25% of S neurons discharged action potentials. In contrast, no action potentials were discharged in AH neurons. Furthermore, naloxone did not alter the resting membrane potential, input resistance, soma action potential configuration, or the slow hyperpolarization following a soma spike in AH neurons. The specificity of the withdrawal response for S neurons and the relatively small proportion of neurons involved suggests that morphine withdrawal occurs in quite specific neuronal circuits in the myenteric plexus.

UR - http://www.scopus.com/inward/record.url?scp=0023229387&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0023229387&partnerID=8YFLogxK

U2 - 10.1016/0306-4522(87)90145-X

DO - 10.1016/0306-4522(87)90145-X

M3 - Article

C2 - 3039405

AN - SCOPUS:0023229387

VL - 21

SP - 595

EP - 602

JO - Neuroscience

JF - Neuroscience

SN - 0306-4522

IS - 2

ER -