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Genetic dissection of an amygdala microcircuit that gates conditioned fear

Author

Listed:
  • Wulf Haubensak

    (California Institute of Technology)

  • Prabhat S. Kunwar

    (California Institute of Technology)

  • Haijiang Cai

    (California Institute of Technology)

  • Stephane Ciocchi

    (Friedrich Miescher Institute for Biomedical Research)

  • Nicholas R. Wall

    (Systems Neurobiology Laboratory, The Salk Institute for Biological Studies)

  • Ravikumar Ponnusamy

    (University of California, Los Angeles, Los Angeles, California 90095, USA)

  • Jonathan Biag

    (Laboratory for Neuroimaging, University of California, Los Angeles, Los Angeles, California 90095, USA)

  • Hong-Wei Dong

    (Laboratory for Neuroimaging, University of California, Los Angeles, Los Angeles, California 90095, USA)

  • Karl Deisseroth

    (Stanford University)

  • Edward M. Callaway

    (Systems Neurobiology Laboratory, The Salk Institute for Biological Studies)

  • Michael S. Fanselow

    (University of California, Los Angeles, Los Angeles, California 90095, USA)

  • Andreas Lüthi

    (Friedrich Miescher Institute for Biomedical Research)

  • David J. Anderson

    (California Institute of Technology
    Howard Hughes Medical Institute, California Institute of Technology)

Abstract

The role of different amygdala nuclei (neuroanatomical subdivisions) in processing Pavlovian conditioned fear has been studied extensively, but the function of the heterogeneous neuronal subtypes within these nuclei remains poorly understood. Here we use molecular genetic approaches to map the functional connectivity of a subpopulation of GABA-containing neurons, located in the lateral subdivision of the central amygdala (CEl), which express protein kinase C-δ (PKC-δ). Channelrhodopsin-2-assisted circuit mapping in amygdala slices and cell-specific viral tracing indicate that PKC-δ+ neurons inhibit output neurons in the medial central amygdala (CEm), and also make reciprocal inhibitory synapses with PKC-δ− neurons in CEl. Electrical silencing of PKC-δ+ neurons in vivo suggests that they correspond to physiologically identified units that are inhibited by the conditioned stimulus, called CEloff units. This correspondence, together with behavioural data, defines an inhibitory microcircuit in CEl that gates CEm output to control the level of conditioned freezing.

Suggested Citation

  • Wulf Haubensak & Prabhat S. Kunwar & Haijiang Cai & Stephane Ciocchi & Nicholas R. Wall & Ravikumar Ponnusamy & Jonathan Biag & Hong-Wei Dong & Karl Deisseroth & Edward M. Callaway & Michael S. Fansel, 2010. "Genetic dissection of an amygdala microcircuit that gates conditioned fear," Nature, Nature, vol. 468(7321), pages 270-276, November.
    • Handle: RePEc:nat:nature:v:468:y:2010:i:7321:d:10.1038_nature09553
    DOI: 10.1038/nature09553
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    Cited by:

    1. 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.
    2. Sorinel A Oprisan & Xandre Clementsmith & Tamas Tompa & Antonieta Lavin, 2019. "Dopamine receptor antagonists effects on low-dimensional attractors of local field potentials in optogenetic mice," PLOS ONE, Public Library of Science, vol. 14(10), pages 1-39, October.
    3. Gregory J. Salimando & Sébastien Tremblay & Blake A. Kimmey & Jia Li & Sophie A. Rogers & Jessica A. Wojick & Nora M. McCall & Lisa M. Wooldridge & Amrith Rodrigues & Tito Borner & Kristin L. Gardiner, 2023. "Human OPRM1 and murine Oprm1 promoter driven viral constructs for genetic access to μ-opioidergic cell types," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. Huiling Yu & Liping Chen & Huiyang Lei & Guilin Pi & Rui Xiong & Tao Jiang & Dongqin Wu & Fei Sun & Yang Gao & Yuanhao Li & Wenju Peng & Bingyu Huang & Guoda Song & Xin Wang & Jingru Lv & Zetao Jin & , 2022. "Infralimbic medial prefrontal cortex signalling to calbindin 1 positive neurons in posterior basolateral amygdala suppresses anxiety- and depression-like behaviours," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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