Experience-driven rate modulation is reinstated during hippocampal replay

  1. Margot Tirole  Is a corresponding author
  2. Marta Huelin Gorriz  Is a corresponding author
  3. Masahiro Takigawa
  4. Lilia Kukovska
  5. Daniel Bendor  Is a corresponding author
  1. University College London, United Kingdom

Abstract

Replay, the sequential reactivation within a neuronal ensemble, is a central hippocampal mechanism postulated to drive memory processing. While both rate and place representations are used by hippocampal place cells to encode behavioral episodes, replay has been largely defined by only the latter – based on the fidelity of sequential activity across neighboring place fields. Here we show that dorsal CA1 place cells in rats can modulate their firing rate between replay events of two different contexts. This experience-dependent phenomenon mirrors the same pattern of rate modulation observed during behavior and can be used independently from place information within replay sequences to discriminate between contexts. Our results reveal the existence of two complementary neural representations available for memory processes.

Data availability

Data availabilityThe data used in this manuscript are available on DRYAD [doi:10.5061/dryad.ksn02v76h].Code availabilityAll custom-written code is available on GitHub [https://github.com/bendor-lab/analysis-pipeline].

Article and author information

Author details

  1. Margot Tirole

    University College London, London, United Kingdom
    For correspondence
    Margot.tirole.14@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0674-6690
  2. Marta Huelin Gorriz

    University College London, London, United Kingdom
    For correspondence
    Marta.Huelin.16@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0281-0627
  3. Masahiro Takigawa

    University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Lilia Kukovska

    University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Daniel Bendor

    University College London, London, United Kingdom
    For correspondence
    d.bendor@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6621-793X

Funding

Biotechnology and Biological Sciences Research Council (BB/M009513/1)

  • Margot Tirole

Biotechnology and Biological Sciences Research Council (BB/T005475/1)

  • Daniel Bendor

European Research Council (CHIME)

  • Daniel Bendor

Human Frontier Science Program (RGY0067/2016)

  • Daniel Bendor

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 and post operative care were approved and carried out in accordance with the UK Home Office, subject to the restrictions and provisions contained within the Animal Scientific Procedures Act of 1986. Experiments were conducted under PPL P61EA6A72 (Bendor). Animals were deeply anaesthetised under isoflurane anaesthesia (1.5-3% at 2L/min) during surgery, and every effort was made to minimize suffering.

Reviewing Editor

  1. Caleb Kemere, Rice University, United States

Publication history

  1. Preprint posted: July 16, 2021 (view preprint)
  2. Received: March 28, 2022
  3. Accepted: August 12, 2022
  4. Accepted Manuscript published: August 22, 2022 (version 1)
  5. Version of Record published: September 20, 2022 (version 2)

Copyright

© 2022, Tirole 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. Margot Tirole
  2. Marta Huelin Gorriz
  3. Masahiro Takigawa
  4. Lilia Kukovska
  5. Daniel Bendor
(2022)
Experience-driven rate modulation is reinstated during hippocampal replay
eLife 11:e79031.
https://doi.org/10.7554/eLife.79031
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