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Midbrain circuits for defensive behaviour

Author

Listed:
  • Philip Tovote

    (Friedrich Miescher Institute for Biomedical Research)

  • Maria Soledad Esposito

    (Friedrich Miescher Institute for Biomedical Research
    Biozentrum, University of Basel)

  • Paolo Botta

    (Friedrich Miescher Institute for Biomedical Research
    †Present addresses: Champalimaud Centre for the Unknown, Avenida de Brasilia, 1400-038 Lisbon, Portugal (P.B.); Center for Brain Science, Harvard University, Cambridge, Massachusetts 02138, USA (S.B.E.W.).)

  • Fabrice Chaudun

    (INSERM, Neurocentre Magendie, U862)

  • Jonathan P. Fadok

    (Friedrich Miescher Institute for Biomedical Research)

  • Milica Markovic

    (Friedrich Miescher Institute for Biomedical Research)

  • Steffen B. E. Wolff

    (Friedrich Miescher Institute for Biomedical Research
    †Present addresses: Champalimaud Centre for the Unknown, Avenida de Brasilia, 1400-038 Lisbon, Portugal (P.B.); Center for Brain Science, Harvard University, Cambridge, Massachusetts 02138, USA (S.B.E.W.).)

  • Charu Ramakrishnan

    (Stanford University, 318 Campus Drive West)

  • Lief Fenno

    (Stanford University, 318 Campus Drive West)

  • Karl Deisseroth

    (Stanford University, 318 Campus Drive West)

  • Cyril Herry

    (INSERM, Neurocentre Magendie, U862)

  • Silvia Arber

    (Friedrich Miescher Institute for Biomedical Research
    Biozentrum, University of Basel)

  • Andreas Lüthi

    (Friedrich Miescher Institute for Biomedical Research)

Abstract

Survival in threatening situations depends on the selection and rapid execution of an appropriate active or passive defensive response, yet the underlying brain circuitry is not understood. Here we use circuit-based optogenetic, in vivo and in vitro electrophysiological, and neuroanatomical tracing methods to define midbrain periaqueductal grey circuits for specific defensive behaviours. We identify an inhibitory pathway from the central nucleus of the amygdala to the ventrolateral periaqueductal grey that produces freezing by disinhibition of ventrolateral periaqueductal grey excitatory outputs to pre-motor targets in the magnocellular nucleus of the medulla. In addition, we provide evidence for anatomical and functional interaction of this freezing pathway with long-range and local circuits mediating flight. Our data define the neuronal circuitry underlying the execution of freezing, an evolutionarily conserved defensive behaviour, which is expressed by many species including fish, rodents and primates. In humans, dysregulation of this ‘survival circuit’ has been implicated in anxiety-related disorders.

Suggested Citation

  • Philip Tovote & Maria Soledad Esposito & Paolo Botta & Fabrice Chaudun & Jonathan P. Fadok & Milica Markovic & Steffen B. E. Wolff & Charu Ramakrishnan & Lief Fenno & Karl Deisseroth & Cyril Herry & S, 2016. "Midbrain circuits for defensive behaviour," Nature, Nature, vol. 534(7606), pages 206-212, June.
    • Handle: RePEc:nat:nature:v:534:y:2016:i:7606:d:10.1038_nature17996
    DOI: 10.1038/nature17996
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    Cited by:

    1. Jasmin A. Strickland & Michael A. McDannald, 2022. "Brainstem networks construct threat probability and prediction error from neuronal building blocks," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    2. Hong Yu & Xinkuan Xiang & Zongming Chen & Xu Wang & Jiaqi Dai & Xinxin Wang & Pengcheng Huang & Zheng-dong Zhao & Wei L. Shen & Haohong Li, 2021. "Periaqueductal gray neurons encode the sequential motor program in hunting behavior of mice," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    3. Coralie Hérent & Séverine Diem & Giovanni Usseglio & Gilles Fortin & Julien Bouvier, 2023. "Upregulation of breathing rate during running exercise by central locomotor circuits in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. Anna J. Bowen & Y. Waterlily Huang & Jane Y. Chen & Jordan L. Pauli & Carlos A. Campos & Richard D. Palmiter, 2023. "Topographic representation of current and future threats in the mouse nociceptive amygdala," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Jun Wang & Qian Yang & Xue Liu & Jie Li & Ya-Lan Wen & Yuzheng Hu & Tian-Le Xu & Shumin Duan & Han Xu, 2024. "The basal forebrain to lateral habenula circuitry mediates social behavioral maladaptation," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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