Hippocampal place cell remapping occurs with memory storage of aversive experiences

Abstract
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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

1. Blair GJ
2. Guo C
3. Wang S
4. Fanselow MS
5. Golshani P
6. Aharoni D
7. Blair HT
(2023) Hippocampal place cell remapping occurs with memory storage of aversive experiences
Dryad Digital Repository, doi:10.5068/D1ZT2S.

https://doi.org/10.5068/D1ZT2S

Article and author information

Author details

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.

"This ORCID iD identifies the author of this article:" 0000-0003-2724-8914
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.
Shiyun Wang

Department of Psychology, University of California, Los Angeles, Los Angeles, United States

Competing interests
The authors declare that no competing interests exist.
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.

"This ORCID iD identifies the author of this article:" 0000-0002-3850-5966
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.
Daniel Aharoni

Department of Neurology, University of California, Los Angeles, Los Angeles, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4931-8514
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

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.