Hippocampal place cell remapping occurs with memory storage of aversive experiences

Abstract

Aversive stimuli can cause hippocampal place cells to remap their firing fields, but it is not known whether remapping plays a role in storing memories of aversive experiences. Here we addressed this question by performing in-vivo calcium imaging of CA1 place cells in freely behaving rats (n=14). Rats were first trained to prefer a short path over a long path for obtaining food reward, then trained to avoid the short path by delivering a mild footshock. Remapping was assessed by comparing place cell population vector similarity before acquisition versus after extinction of avoidance. Some rats received shock after systemic injections of the amnestic drug scopolamine at a dose (1 mg/kg) that impaired avoidance learning but spared spatial tuning and shock-evoked responses of CA1 neurons. Place cells remapped significantly more following remembered than forgotten shocks (drug-free versus scopolamine conditions); shock-induced remapping did not cause place fields to migrate toward or away from the shocked location and was similarly prevalent in cells that were responsive versus non-responsive to shocks. When rats were exposed to a neutral barrier rather than aversive shock, place cells remapped significantly less in response to the barrier. We conclude that place cell remapping occurs in response to events that are remembered rather than merely perceived and forgotten, suggesting that reorganization of hippocampal population codes may play a role in storing memories for aversive events.

Data availability

Source data and code for reproducing the figures are available at: https://github.com/tadblair/tadblair or https://doi.org/10.5068/D1ZT2S

The following data sets were generated

Article and author information

Author details

  1. Garrett J Blair

    Department of Psychology, University of California, Los Angeles, Los Angeles, United States
    For correspondence
    gjb326@nyu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2724-8914
  2. Changliang Guo

    David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Shiyun Wang

    Department of Psychology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Michael S Fanselow

    Department of Psychology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3850-5966
  5. Peyman Golshani

    David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Daniel Aharoni

    Department of Neurology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4931-8514
  7. Hugh T Blair

    Department of Psychology, University of California, Los Angeles, Los Angeles, United States
    For correspondence
    tadblair@ucla.edu
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Science Foundation (NeuroNex 1704708)

  • Garrett J Blair
  • Changliang Guo
  • Peyman Golshani
  • Daniel Aharoni
  • Hugh T Blair

National Institute of Mental Health (RO1-MH062122)

  • Michael S Fanselow

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 experimental procedures were approved by the Chancellor's Animal Research Committee of the University of California, Los Angeles, in accordance with the US National Institutes of Health (NIH) guidelines. protocol #2017-038

Copyright

© 2023, Blair 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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  1. Garrett J Blair
  2. Changliang Guo
  3. Shiyun Wang
  4. Michael S Fanselow
  5. Peyman Golshani
  6. Daniel Aharoni
  7. Hugh T Blair
(2023)
Hippocampal place cell remapping occurs with memory storage of aversive experiences
eLife 12:e80661.
https://doi.org/10.7554/eLife.80661

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https://doi.org/10.7554/eLife.80661

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