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Contrasting forms of cocaine-evoked plasticity control components of relapse

Author

Listed:
  • Vincent Pascoli

    (Medical Faculty, University of Geneva, CH-1211 Geneva, Switzerland)

  • Jean Terrier

    (Medical Faculty, University of Geneva, CH-1211 Geneva, Switzerland)

  • Julie Espallergues

    (INSERM, U661, Montpellier F-34094, France
    CNRS, UMR-5203, Institut de Génomique Fonctionnelle, Montpellier F-34094, France
    Universités de Montpellier 1 & 2, UMR-5203, Montpellier F-34094, France)

  • Emmanuel Valjent

    (INSERM, U661, Montpellier F-34094, France
    CNRS, UMR-5203, Institut de Génomique Fonctionnelle, Montpellier F-34094, France
    Universités de Montpellier 1 & 2, UMR-5203, Montpellier F-34094, France)

  • Eoin Cornelius O’Connor

    (Medical Faculty, University of Geneva, CH-1211 Geneva, Switzerland)

  • Christian Lüscher

    (Medical Faculty, University of Geneva, CH-1211 Geneva, Switzerland
    Clinic of Neurology, Geneva University Hospital, CH-1211 Geneva, Switzerland)

Abstract

Nucleus accumbens neurons serve to integrate information from cortical and limbic regions to direct behaviour. Addictive drugs are proposed to hijack this system, enabling drug-associated cues to trigger relapse to drug seeking. However, the connections affected and proof of causality remain to be established. Here we use a mouse model of delayed cue-associated cocaine seeking with ex vivo electrophysiology in optogenetically delineated circuits. We find that seeking correlates with rectifying AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid) receptor transmission and a reduced AMPA/NMDA (N-methyl-d-aspartate) ratio at medial prefrontal cortex (mPFC) to nucleus accumbens shell D1-receptor medium-sized spiny neurons (D1R-MSNs). In contrast, the AMPA/NMDA ratio increases at ventral hippocampus to D1R-MSNs. Optogenetic reversal of cocaine-evoked plasticity at both inputs abolishes seeking, whereas selective reversal at mPFC or ventral hippocampus synapses impairs response discrimination or reduces response vigour during seeking, respectively. Taken together, we describe how information integration in the nucleus accumbens is commandeered by cocaine at discrete synapses to allow relapse. Our approach holds promise for identifying synaptic causalities in other behavioural disorders.

Suggested Citation

  • Vincent Pascoli & Jean Terrier & Julie Espallergues & Emmanuel Valjent & Eoin Cornelius O’Connor & Christian Lüscher, 2014. "Contrasting forms of cocaine-evoked plasticity control components of relapse," Nature, Nature, vol. 509(7501), pages 459-464, May.
    • Handle: RePEc:nat:nature:v:509:y:2014:i:7501:d:10.1038_nature13257
    DOI: 10.1038/nature13257
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    Cited by:

    1. Himanshu Gangal & Xueyi Xie & Zhenbo Huang & Yifeng Cheng & Xuehua Wang & Jiayi Lu & Xiaowen Zhuang & Amanda Essoh & Yufei Huang & Ruifeng Chen & Laura N. Smith & Rachel J. Smith & Jun Wang, 2023. "Drug reinforcement impairs cognitive flexibility by inhibiting striatal cholinergic neurons," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Brandon W. Hughes & Jessica L. Huebschman & Evgeny Tsvetkov & Benjamin M. Siemsen & Kirsten K. Snyder & Rose Marie Akiki & Daniel J. Wood & Rachel D. Penrod & Michael D. Scofield & Stefano Berto & Mak, 2024. "NPAS4 supports cocaine-conditioned cues in rodents by controlling the cell type-specific activation balance in the nucleus accumbens," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    3. Khairunisa Mohamad Ibrahim & Nicolas Massaly & Hye-Jean Yoon & Rossana Sandoval & Allie J. Widman & Robert J. Heuermann & Sidney Williams & William Post & Sulan Pathiranage & Tania Lintz & Azra Zec & , 2024. "Dorsal hippocampus to nucleus accumbens projections drive reinforcement via activation of accumbal dynorphin neurons," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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