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A dopaminergic switch for fear to safety transitions

Author

Listed:
  • Ray Luo

    (RIKEN Brain Science Institute
    RIKEN Center for Brain Science)

  • Akira Uematsu

    (RIKEN Brain Science Institute
    RIKEN Center for Brain Science)

  • Adam Weitemier

    (RIKEN Brain Science Institute)

  • Luca Aquili

    (RIKEN Brain Science Institute
    Department of Psychology, Sheffield Hallam University, Sociology & Politics, Heart of the Campus Building, Collegiate Crescent, Collegiate Campus)

  • Jenny Koivumaa

    (RIKEN Brain Science Institute
    RIKEN Center for Brain Science)

  • Thomas J. McHugh

    (RIKEN Brain Science Institute
    RIKEN Center for Brain Science
    University of Tokyo)

  • Joshua P. Johansen

    (RIKEN Brain Science Institute
    RIKEN Center for Brain Science
    University of Tokyo)

Abstract

Overcoming aversive emotional memories requires neural systems that detect when fear responses are no longer appropriate so that they can be extinguished. The midbrain ventral tegmental area (VTA) dopamine system has been implicated in reward and more broadly in signaling when a better-than-expected outcome has occurred. This suggests that it may be important in guiding fear to safety transitions. We report that when an expected aversive outcome does not occur, activity in midbrain dopamine neurons is necessary to extinguish behavioral fear responses and engage molecular signaling events in extinction learning circuits. Furthermore, a specific dopamine projection to the nucleus accumbens medial shell is partially responsible for this effect. In contrast, a separate dopamine projection to the medial prefrontal cortex opposes extinction learning. This demonstrates a novel function for the canonical VTA-dopamine reward system and reveals opposing behavioral roles for different dopamine neuron projections in fear extinction learning.

Suggested Citation

  • Ray Luo & Akira Uematsu & Adam Weitemier & Luca Aquili & Jenny Koivumaa & Thomas J. McHugh & Joshua P. Johansen, 2018. "A dopaminergic switch for fear to safety transitions," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-04784-7
    DOI: 10.1038/s41467-018-04784-7
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    Cited by:

    1. Rodrigo Ordoñez Sierra & Lizeth Katherine Pedraza & Lívia Barcsai & Andrea Pejin & Qun Li & Gábor Kozák & Yuichi Takeuchi & Anett J. Nagy & Magor L. Lőrincz & Orrin Devinsky & György Buzsáki & Antal B, 2023. "Closed-loop brain stimulation augments fear extinction in male rats," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Qi Wang & Jia-Jie Zhu & Lizhao Wang & Yan-Peng Kan & Yan-Mei Liu & Yan-Jiao Wu & Xue Gu & Xin Yi & Ze-Jie Lin & Qin Wang & Jian-Fei Lu & Qin Jiang & Ying Li & Ming-Gang Liu & Nan-Jie Xu & Michael X. Z, 2022. "Insular cortical circuits as an executive gateway to decipher threat or extinction memory via distinct subcortical pathways," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Allen P. F. Chen & Lu Chen & Kaiyo W. Shi & Eileen Cheng & Shaoyu Ge & Qiaojie Xiong, 2023. "Nigrostriatal dopamine modulates the striatal-amygdala pathway in auditory fear conditioning," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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