Mu Opioid Receptor-Positive Neurons in the Dorsal Raphe Nucleus Are Impaired by Morphine Abstinence.

Addiction-related behaviors Chronic morphine Mu opioid signaling Opto-intracranial self-stimulation vTRAP-seq

Journal

Biological psychiatry
ISSN: 1873-2402
Titre abrégé: Biol Psychiatry
Pays: United States
ID NLM: 0213264

Informations de publication

Date de publication:
01 12 2023
Historique:
received: 23 01 2023
revised: 21 06 2023
accepted: 21 06 2023
medline: 3 11 2023
pubmed: 2 7 2023
entrez: 1 7 2023
Statut: ppublish

Résumé

Chronic opioid exposure leads to hedonic deficits and enhanced vulnerability to addiction, which are observed and even strengthen after a period of abstinence, but the underlying circuit mechanisms are poorly understood. In this study, using both molecular and behavioral approaches, we tested the hypothesis that neurons expressing mu opioid receptors (MORs) in the dorsal raphe nucleus (DRN) are involved in addiction vulnerability associated with morphine abstinence. MOR-Cre mice were exposed to chronic morphine and then went through spontaneous withdrawal for 4 weeks, a well-established mouse model of morphine abstinence. We studied DRN-MOR neurons of abstinent mice using 1) viral translating ribosome affinity for transcriptome profiling, 2) fiber photometry to measure neuronal activity, and 3) an opto-intracranial self-stimulation paradigm applied to DRN-MOR neurons to assess responses related to addiction vulnerability including persistence to respond, motivation to obtain the stimulation, self-stimulation despite punishment, and cue-induced reinstatement. DRN-MOR neurons of abstinent animals showed a downregulation of genes involved in ion conductance and MOR-mediated signaling, as well as altered responding to acute morphine. Opto-intracranial self-stimulation data showed that abstinent animals executed more impulsive-like and persistent responses during acquisition and scored higher on addiction-like criteria. Our data suggest that protracted abstinence to chronic morphine leads to reduced MOR function in DRN-MOR neurons and abnormal self-stimulation of these neurons. We propose that DRN-MOR neurons have partially lost their reward-facilitating properties, which in turn may lead to increased propensity to perform addiction-related behaviors.

Sections du résumé

BACKGROUND
Chronic opioid exposure leads to hedonic deficits and enhanced vulnerability to addiction, which are observed and even strengthen after a period of abstinence, but the underlying circuit mechanisms are poorly understood. In this study, using both molecular and behavioral approaches, we tested the hypothesis that neurons expressing mu opioid receptors (MORs) in the dorsal raphe nucleus (DRN) are involved in addiction vulnerability associated with morphine abstinence.
METHODS
MOR-Cre mice were exposed to chronic morphine and then went through spontaneous withdrawal for 4 weeks, a well-established mouse model of morphine abstinence. We studied DRN-MOR neurons of abstinent mice using 1) viral translating ribosome affinity for transcriptome profiling, 2) fiber photometry to measure neuronal activity, and 3) an opto-intracranial self-stimulation paradigm applied to DRN-MOR neurons to assess responses related to addiction vulnerability including persistence to respond, motivation to obtain the stimulation, self-stimulation despite punishment, and cue-induced reinstatement.
RESULTS
DRN-MOR neurons of abstinent animals showed a downregulation of genes involved in ion conductance and MOR-mediated signaling, as well as altered responding to acute morphine. Opto-intracranial self-stimulation data showed that abstinent animals executed more impulsive-like and persistent responses during acquisition and scored higher on addiction-like criteria.
CONCLUSIONS
Our data suggest that protracted abstinence to chronic morphine leads to reduced MOR function in DRN-MOR neurons and abnormal self-stimulation of these neurons. We propose that DRN-MOR neurons have partially lost their reward-facilitating properties, which in turn may lead to increased propensity to perform addiction-related behaviors.

Identifiants

pubmed: 37393045
pii: S0006-3223(23)01397-5
doi: 10.1016/j.biopsych.2023.06.024
pii:
doi:

Substances chimiques

Morphine 76I7G6D29C
Receptors, Opioid, mu 0
Analgesics, Opioid 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

852-862

Informations de copyright

Copyright © 2023 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

Auteurs

Lola Welsch (L)

Douglas Research Center, Department of Psychiatry, McGill University, Montréal, Quebec, Canada; INSERM U1114, University of Strasbourg, Strasbourg, France.

Esther Colantonio (E)

INSERM U1114, University of Strasbourg, Strasbourg, France.

Camille Falconnier (C)

Centre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives UPR3212, Strasbourg, France.

Cédric Champagnol-DiLiberti (C)

INSERM U1114, University of Strasbourg, Strasbourg, France.

Florence Allain (F)

Douglas Research Center, Department of Psychiatry, McGill University, Montréal, Quebec, Canada; INSERM U1114, University of Strasbourg, Strasbourg, France.

Sami Ben Hamida (S)

Douglas Research Center, Department of Psychiatry, McGill University, Montréal, Quebec, Canada; INSERM UMR 1247, Research Group on Alcohol & Pharmacodependences, Université de Picardie Jules Verne, Amiens, France.

Emmanuel Darcq (E)

Douglas Research Center, Department of Psychiatry, McGill University, Montréal, Quebec, Canada; INSERM U1114, University of Strasbourg, Strasbourg, France.

Pierre-Eric Lutz (PE)

Douglas Research Center, Department of Psychiatry, McGill University, Montréal, Quebec, Canada; Centre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives UPR3212, Strasbourg, France.

Brigitte L Kieffer (BL)

Douglas Research Center, Department of Psychiatry, McGill University, Montréal, Quebec, Canada; INSERM U1114, University of Strasbourg, Strasbourg, France. Electronic address: brigitte.kieffer@unistra.fr.

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Classifications MeSH