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Role of VTA dopamine neurons and neuroligin 3 in sociability traits related to nonfamiliar conspecific interaction

Author

Listed:
  • Sebastiano Bariselli

    (University of Geneva)

  • Hanna Hörnberg

    (Biozentrum of the University of Basel)

  • Clément Prévost-Solié

    (University of Geneva)

  • Stefano Musardo

    (University of Geneva)

  • Laetitia Hatstatt-Burklé

    (Biozentrum of the University of Basel)

  • Peter Scheiffele

    (Biozentrum of the University of Basel)

  • Camilla Bellone

    (University of Geneva)

Abstract

Atypical habituation and aberrant exploration of novel stimuli have been related to the severity of autism spectrum disorders (ASDs), but the underlying neuronal circuits are unknown. Here we show that chemogenetic inhibition of dopamine (DA) neurons of the ventral tegmental area (VTA) attenuates exploration toward nonfamiliar conspecifics and interferes with the reinforcing properties of nonfamiliar conspecific interaction in mice. Exploration of nonfamiliar stimuli is associated with the insertion of GluA2-lacking AMPA receptors at excitatory synapses on VTA DA neurons. These synaptic adaptations persist upon repeated exposure to social stimuli and sustain conspecific interaction. Global or VTA DA neuron-specific loss of the ASD-associated synaptic adhesion molecule neuroligin 3 alters the behavioral response toward nonfamiliar conspecifics and the reinforcing properties of conspecific interaction. These behavioral deficits are accompanied by an aberrant expression of AMPA receptors and an occlusion of synaptic plasticity. Altogether, these findings link impaired exploration of nonfamiliar conspecifics to VTA DA neuron dysfunction in mice.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-05382-3
    DOI: 10.1038/s41467-018-05382-3
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    Cited by:

    1. 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.
    2. Clément Solié & Alessandro Contestabile & Pedro Espinosa & Stefano Musardo & Sebastiano Bariselli & Chieko Huber & Alan Carleton & Camilla Bellone, 2022. "Superior Colliculus to VTA pathway controls orienting response and influences social interaction in mice," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Susanna Molas & Timothy G. Freels & Rubing Zhao-Shea & Timothy Lee & Pablo Gimenez-Gomez & Melanie Barbini & Gilles E. Martin & Andrew R. Tapper, 2024. "Dopamine control of social novelty preference is constrained by an interpeduncular-tegmentum circuit," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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