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Encoding of conditioned fear in central amygdala inhibitory circuits

Author

Listed:
  • Stephane Ciocchi

    (Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland)

  • Cyril Herry

    (Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland
    Present addresses: INSERM U862, Neurocentre Magendie, 146 Rue Léo-Saignat, 33077 Bordeaux, France (C.H.); Hertie Institute for Clinical Brain Research, 72076 Tübingen, Germany (I.E.).)

  • François Grenier

    (Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland)

  • Steffen B. E. Wolff

    (Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland)

  • Johannes J. Letzkus

    (Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland)

  • Ioannis Vlachos

    (Bernstein Center for Computational Neuroscience, 79104 Freiburg, Germany)

  • Ingrid Ehrlich

    (Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland
    Present addresses: INSERM U862, Neurocentre Magendie, 146 Rue Léo-Saignat, 33077 Bordeaux, France (C.H.); Hertie Institute for Clinical Brain Research, 72076 Tübingen, Germany (I.E.).)

  • Rolf Sprengel

    (Max Planck Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg, Germany)

  • Karl Deisseroth

    (Stanford University)

  • Michael B. Stadler

    (Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland)

  • Christian Müller

    (Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland)

  • Andreas Lüthi

    (Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland)

Abstract

The central amygdala (CEA), a nucleus predominantly composed of GABAergic inhibitory neurons, is essential for fear conditioning. How the acquisition and expression of conditioned fear are encoded within CEA inhibitory circuits is not understood. Using in vivo electrophysiological, optogenetic and pharmacological approaches in mice, we show that neuronal activity in the lateral subdivision of the central amygdala (CEl) is required for fear acquisition, whereas conditioned fear responses are driven by output neurons in the medial subdivision (CEm). Functional circuit analysis revealed that inhibitory CEA microcircuits are highly organized and that cell-type-specific plasticity of phasic and tonic activity in the CEl to CEm pathway may gate fear expression and regulate fear generalization. Our results define the functional architecture of CEA microcircuits and their role in the acquisition and regulation of conditioned fear behaviour.

Suggested Citation

  • Stephane Ciocchi & Cyril Herry & François Grenier & Steffen B. E. Wolff & Johannes J. Letzkus & Ioannis Vlachos & Ingrid Ehrlich & Rolf Sprengel & Karl Deisseroth & Michael B. Stadler & Christian Müll, 2010. "Encoding of conditioned fear in central amygdala inhibitory circuits," Nature, Nature, vol. 468(7321), pages 277-282, November.
    • Handle: RePEc:nat:nature:v:468:y:2010:i:7321:d:10.1038_nature09559
    DOI: 10.1038/nature09559
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    Cited by:

    1. Athina Tzovara & Christoph W Korn & Dominik R Bach, 2018. "Human Pavlovian fear conditioning conforms to probabilistic learning," PLOS Computational Biology, Public Library of Science, vol. 14(8), pages 1-21, August.
    2. Elyashiv Zangen & Shira Hadar & Christopher Lawrence & Mustafa Obeid & Hala Rasras & Ella Hanzin & Ori Aslan & Eyal Zur & Nadav Schulcz & Daniel Cohen-Hatab & Yona Samama & Sarah Nir & Yi Li & Irina D, 2024. "Prefrontal cortex neurons encode ambient light intensity differentially across regions and layers," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. Chloe Hegoburu & Yan Tang & Ruifang Niu & Supriya Ghosh & Rodrigo Triana Del Rio & Isabel de Araujo Salgado & Marios Abatis & David Alexandre Mota Caseiro & Erwin H. Burg & Christophe Grundschober & R, 2024. "Social buffering in rats reduces fear by oxytocin triggering sustained changes in central amygdala neuronal activity," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Danyang Chen & Qianqian Lou & Xiang-Jie Song & Fang Kang & An Liu & Changjian Zheng & Yanhua Li & Di Wang & Sen Qun & Zhi Zhang & Peng Cao & Yan Jin, 2024. "Microglia govern the extinction of acute stress-induced anxiety-like behaviors in male mice," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    5. Jing-Jing Yan & Xiao-Jing Ding & Ting He & Ai-Xiao Chen & Wen Zhang & Zi-Xian Yu & Xin-Yu Cheng & Chuan-Yao Wei & Qiao-Dan Hu & Xiao-Yao Liu & Yan-Li Zhang & Mengge He & Zhi-Yong Xie & Xi Zha & Chun X, 2022. "A circuit from the ventral subiculum to anterior hypothalamic nucleus GABAergic neurons essential for anxiety-like behavioral avoidance," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Masahiro Sawada & Ralph Adolphs & Brian J. Dlouhy & Rick L. Jenison & Ariane E. Rhone & Christopher K. Kovach & Jeremy, D. W. Greenlee & Matthew A. Howard III & Hiroyuki Oya, 2022. "Mapping effective connectivity of human amygdala subdivisions with intracranial stimulation," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    7. 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.
    8. 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.
    9. Camila Demaestri & Margaux Pisciotta & Naira Altunkeser & Georgia Berry & Hannah Hyland & Jocelyn Breton & Anna Darling & Brenna Williams & Kevin G. Bath, 2024. "Central amygdala CRF+ neurons promote heightened threat reactivity following early life adversity in mice," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

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