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Transient nicotine exposure in early adolescent male mice freezes their dopamine circuits in an immature state

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  • Lauren M. Reynolds

    (École supérieure de physique et de chimie industrielles de la Ville de Paris (ESPCI Paris)
    Sorbonne Université)

  • Aylin Gulmez

    (École supérieure de physique et de chimie industrielles de la Ville de Paris (ESPCI Paris))

  • Sophie L. Fayad

    (École supérieure de physique et de chimie industrielles de la Ville de Paris (ESPCI Paris)
    Sorbonne Université)

  • Renan Costa Campos

    (CNRS)

  • Daiana Rigoni

    (CNRS)

  • Claire Nguyen

    (Sorbonne Université)

  • Tinaïg Le Borgne

    (École supérieure de physique et de chimie industrielles de la Ville de Paris (ESPCI Paris)
    Sorbonne Université)

  • Thomas Topilko

    (ICM Institut du Cerveau et de la Moelle Epinière)

  • Domitille Rajot

    (ICM Institut du Cerveau et de la Moelle Epinière)

  • Clara Franco

    (Sorbonne Université)

  • Sebastian P. Fernandez

    (CNRS)

  • Fabio Marti

    (École supérieure de physique et de chimie industrielles de la Ville de Paris (ESPCI Paris)
    Sorbonne Université)

  • Nicolas Heck

    (Sorbonne Université)

  • Alexandre Mourot

    (École supérieure de physique et de chimie industrielles de la Ville de Paris (ESPCI Paris)
    Sorbonne Université)

  • Nicolas Renier

    (ICM Institut du Cerveau et de la Moelle Epinière)

  • Jacques Barik

    (CNRS)

  • Philippe Faure

    (École supérieure de physique et de chimie industrielles de la Ville de Paris (ESPCI Paris)
    Sorbonne Université)

Abstract

How nicotine acts on developing neurocircuitry in adolescence to promote later addiction vulnerability remains largely unknown, but may hold the key for informing more effective intervention efforts. We found transient nicotine exposure in early adolescent (PND 21-28) male mice was sufficient to produce a marked vulnerability to nicotine in adulthood (PND 60 + ), associated with disrupted functional connectivity in dopaminergic circuits. These mice showed persistent adolescent-like behavioral and physiological responses to nicotine, suggesting that nicotine exposure in adolescence prolongs an immature, imbalanced state in the function of these circuits. Chemogenetically resetting the balance between the underlying dopamine circuits unmasked the mature behavioral response to acute nicotine in adolescent-exposed mice. Together, our results suggest that the perseverance of a developmental imbalance between dopamine pathways may alter vulnerability profiles for later dopamine-dependent psychopathologies.

Suggested Citation

  • Lauren M. Reynolds & Aylin Gulmez & Sophie L. Fayad & Renan Costa Campos & Daiana Rigoni & Claire Nguyen & Tinaïg Le Borgne & Thomas Topilko & Domitille Rajot & Clara Franco & Sebastian P. Fernandez &, 2024. "Transient nicotine exposure in early adolescent male mice freezes their dopamine circuits in an immature state," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53327-w
    DOI: 10.1038/s41467-024-53327-w
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    References listed on IDEAS

    as
    1. Carole Morel & Sarah E. Montgomery & Long Li & Romain Durand-de Cuttoli & Emily M. Teichman & Barbara Juarez & Nikos Tzavaras & Stacy M. Ku & Meghan E. Flanigan & Min Cai & Jessica J. Walsh & Scott J., 2022. "Midbrain projection to the basolateral amygdala encodes anxiety-like but not depression-like behaviors," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Christie D. Fowler & Qun Lu & Paul M. Johnson & Michael J. Marks & Paul J. Kenny, 2011. "Habenular α5 nicotinic receptor subunit signalling controls nicotine intake," Nature, Nature, vol. 471(7340), pages 597-601, March.
    3. Sebastiano Bariselli & Hanna Hörnberg & Clément Prévost-Solié & Stefano Musardo & Laetitia Hatstatt-Burklé & Peter Scheiffele & Camilla Bellone, 2018. "Role of VTA dopamine neurons and neuroligin 3 in sociability traits related to nonfamiliar conspecific interaction," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    4. Lauren M. Reynolds & Giovanni Hernandez & Del MacGowan & Christina Popescu & Dominique Nouel & Santiago Cuesta & Samuel Burke & Katherine E. Savell & Janet Zhao & Jose Maria Restrepo-Lozano & Michel G, 2023. "Amphetamine disrupts dopamine axon growth in adolescence by a sex-specific mechanism in mice," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
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