1. Neuroscience
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'Fearful-place' coding in the amygdala-hippocampal network

  1. Mi-Seon Kong
  2. Eun Joo Kim
  3. Sanggeon Park
  4. Larry S Zweifel
  5. Yeowool Huh
  6. Jeiwon Cho  Is a corresponding author
  7. Jeansok John Kim  Is a corresponding author
  1. University of Washington, United States
  2. Korea University of Science & Technology, Republic of Korea
  3. Catholic Kwandong University, Republic of Korea
  4. Ewha Womans University, Republic of Korea
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Cite this article as: eLife 2021;10:e72040 doi: 10.7554/eLife.72040

Abstract

Animals seeking survival needs must be able to assess different locations of threats in their habitat. However, the neural integration of spatial and risk information essential for guiding goal-directed behavior remains poorly understood. Thus, we investigated simultaneous activities of fear-responsive basal amygdala (BA) and place-responsive dorsal hippocampus (dHPC) neurons as rats left the safe nest to search for food in an exposed space and encountered a simulated 'predator'. In this realistic situation, BA cells increased their firing rates and dHPC place cells decreased their spatial stability near the threat. Importantly, only those dHPC cells synchronized with the predator-responsive BA cells remapped significantly as a function of escalating risk location. Moreover, optogenetic stimulation of BA neurons was sufficient to cause spatial avoidance behavior and disrupt place fields. These results suggest a dynamic interaction of BA's fear signalling cells and dHPC's spatial coding cells as animals traverse safe-danger areas of their environment.

Data availability

The data that support the findings of this study are available under the project DOI https://doi.org/10.5061/dryad.2z34tmpn0. The customized analysis tools are deposited on Github https://github.com/KimLab-UW?tab=repositories.

The following data sets were generated
    1. Kim J
    (2021) Customized analysis tools
    Publicly available at Github (https://github.com).

Article and author information

Author details

  1. Mi-Seon Kong

    Department of Psychology and Department of Psychiatry and Behavioral Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8970-7034
  2. Eun Joo Kim

    Psychology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Sanggeon Park

    Neuroscience Program, Korea University of Science & Technology, Daejeon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  4. Larry S Zweifel

    Department of Psychiatry and Behavioral Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3465-5331
  5. Yeowool Huh

    Department of Medical Science and Institute for Bio-Medical Convergence, Catholic Kwandong University, Incheon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  6. Jeiwon Cho

    Department of Brain and Cognitive Sciences, Ewha Womans University, Seoul, Republic of Korea
    For correspondence
    jelectro21@ewha.ac.kr
    Competing interests
    The authors declare that no competing interests exist.
  7. Jeansok John Kim

    Department of Psychology and Program in Neurobiology & Behavior, University of Washington, Seattle, United States
    For correspondence
    jeansokk@u.washington.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7964-106X

Funding

National Institute of Mental Health (MH088073)

  • Jeansok John Kim

National Research Foundation of Korea (NRF-2015M3C7A1028392)

  • Jeiwon Cho

National Research Foundation of Korea (NRF-2019R1A2C2088377)

  • Jeiwon Cho

National Research Foundation of Korea (NRF-2018M3C7A1024736)

  • Yeowool Huh

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experiments in this study were performed in strict compliance with the University of Washington Institutional Animal Care and Use Committee guidelines (protocol #0404-01). Animals were individually housed in a climate-controlled vivarium (accredited by the Association for Assessment and Accreditation of Laboratory Animal Care) with thorough daily health checkup. Surgeries were performed under ketamine and xylazine mixture anesthesia to minimize physical discomfort, and post-operative assessments for injury, distress, and pain were followed.

Reviewing Editor

  1. Joshua Johansen, RIKEN Center for Brain Science, Japan

Publication history

  1. Received: July 8, 2021
  2. Accepted: September 17, 2021
  3. Accepted Manuscript published: September 17, 2021 (version 1)
  4. Version of Record published: October 8, 2021 (version 2)

Copyright

© 2021, Kong et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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