Disruption of Astrocyte-Dependent Dopamine Control in the Developing Medial Prefrontal Cortex Leads to Excessive Grooming in Mice.


Journal

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

Informations de publication

Date de publication:
01 06 2023
Historique:
received: 19 02 2022
revised: 21 10 2022
accepted: 04 11 2022
medline: 19 5 2023
pubmed: 24 3 2023
entrez: 23 3 2023
Statut: ppublish

Résumé

Astrocytes control synaptic activity by modulating perisynaptic concentrations of ions and neurotransmitters including dopamine (DA) and, as such, could be involved in the modulating aspects of mammalian behavior. We produced a conditional deletion of the vesicular monoamine transporter 2 (VMAT2) specifically in astrocytes (aVMTA2cKO mice) and studied the effects of the lack of VMAT2 in prefrontal cortex (PFC) astrocytes on the regulation of DA levels, PFC circuit functions, and behavioral processes. We found a significant reduction of medial PFC (mPFC) DA levels and excessive grooming and compulsive repetitive behaviors in aVMAT2cKO mice. The mice also developed a synaptic pathology, expressed through increased relative AMPA versus NMDA receptor currents in synapses of the dorsal striatum receiving inputs from the mPFC. Importantly, behavioral and synaptic phenotypes were rescued by re-expression of mPFC VMAT2 and L-DOPA treatment, showing that the deficits were driven by mPFC astrocytes that are critically involved in developmental DA homeostasis. By analyzing human tissue samples, we found that VMAT2 is expressed in human PFC astrocytes, corroborating the potential translational relevance of our observations in mice. Our study shows that impairment of the astrocytic control of DA in the mPFC leads to symptoms resembling obsessive-compulsive spectrum disorders such as trichotillomania and has a profound impact on circuit function and behaviors.

Sections du résumé

BACKGROUND
Astrocytes control synaptic activity by modulating perisynaptic concentrations of ions and neurotransmitters including dopamine (DA) and, as such, could be involved in the modulating aspects of mammalian behavior.
METHODS
We produced a conditional deletion of the vesicular monoamine transporter 2 (VMAT2) specifically in astrocytes (aVMTA2cKO mice) and studied the effects of the lack of VMAT2 in prefrontal cortex (PFC) astrocytes on the regulation of DA levels, PFC circuit functions, and behavioral processes.
RESULTS
We found a significant reduction of medial PFC (mPFC) DA levels and excessive grooming and compulsive repetitive behaviors in aVMAT2cKO mice. The mice also developed a synaptic pathology, expressed through increased relative AMPA versus NMDA receptor currents in synapses of the dorsal striatum receiving inputs from the mPFC. Importantly, behavioral and synaptic phenotypes were rescued by re-expression of mPFC VMAT2 and L-DOPA treatment, showing that the deficits were driven by mPFC astrocytes that are critically involved in developmental DA homeostasis. By analyzing human tissue samples, we found that VMAT2 is expressed in human PFC astrocytes, corroborating the potential translational relevance of our observations in mice.
CONCLUSIONS
Our study shows that impairment of the astrocytic control of DA in the mPFC leads to symptoms resembling obsessive-compulsive spectrum disorders such as trichotillomania and has a profound impact on circuit function and behaviors.

Identifiants

pubmed: 36958999
pii: S0006-3223(22)01798-X
doi: 10.1016/j.biopsych.2022.11.018
pii:
doi:

Substances chimiques

Dopamine VTD58H1Z2X

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

966-975

Informations de copyright

Copyright © 2022 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

Auteurs

Francesco Petrelli (F)

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland.

Tamara Zehnder (T)

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland.

Anthony Laugeray (A)

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland.

Sarah Mondoloni (S)

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland.

Corrado Calì (C)

Department of Neuroscience, University of Torino, Torino, Italy.

Luca Pucci (L)

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland.

Alicia Molinero Perez (A)

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland.

Bianca Maria Bondiolotti (BM)

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland.

Eva De Oliveira Figueiredo (E)

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland.

Glenn Dallerac (G)

Centre de Recherche en Neurobiologie et Neurophysiologie de Marseille, Aix-Marseille Université UMR7286 CNRS, Marseille, France.

Nicole Déglon (N)

Neurosciences Research Center, Laboratory of Neurotherapies and Neuromodulation, Lausanne University Hospital and University of Lausanne, Lausanne, Switzerland.

Bruno Giros (B)

Department of Psychiatry, Douglas Hospital Research Center, McGill University, Montreal, Quebec, Canada.

Lorenzo Magrassi (L)

Neurosurgery, Dipartimento di Scienze Clinico-Chirurgiche e Pediatriche, Università degli Studi di Pavia, Fondazione IRCCS Policlinico S. Matteo, Pavia, Italy.

Jean-Pierre Mothet (JP)

Centre de Recherche en Neurobiologie et Neurophysiologie de Marseille, Aix-Marseille Université UMR7286 CNRS, Marseille, France; "Biophotonics and Synapse Physiopathology" Team, UMR9188 CNRS - ENS Paris Saclay, Orsay, France.

Manuel Mameli (M)

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland.

Linda D Simmler (LD)

Department of Basic Neurosciences, University of Geneva, Geneva, Switzerland. Electronic address: linda.simmler@unige.ch.

Paola Bezzi (P)

Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland; Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy. Electronic address: paola.bezzi@unil.ch.

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Classifications MeSH