Hippocampal place cell remapping occurs with memory storage of aversive experiences
- University of California, Los Angeles, United States
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
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Hippocampal place cell remapping occurs with memory storage of aversive experiencesDryad Digital Repository, doi:10.5068/D1ZT2S.
Article and author information
Author details
Michael S Fanselow
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.
Reviewing Editor
- Liset M de la Prida, Instituto Cajal, Spain
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
Version history
- Preprint posted: May 29, 2022 (view preprint)
- Received: May 30, 2022
- Accepted: June 22, 2023
- Accepted Manuscript published: July 19, 2023 (version 1)
- Version of Record published: July 25, 2023 (version 2)
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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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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