Learning differentially shapes prefrontal and hippocampal activity during classical conditioning

  1. Jan L Klee  Is a corresponding author
  2. Bryan C Souza
  3. Francesco P Battaglia  Is a corresponding author
  1. Radboud University, Netherlands

Abstract

The ability to use sensory cues to inform goal directed actions is a critical component of behavior. To study how sounds guide anticipatory licking during classical conditioning, we employed high-density electrophysiological recordings from the hippocampal CA1 area and the prefrontal cortex (PFC) in mice. CA1 and PFC neurons undergo distinct learning dependent changes at the single cell level and maintain representations of cue identity at the population level. In addition, reactivation of task-related neuronal assemblies during hippocampal awake Sharp-Wave Ripples (aSWR) changed within individual sessions in CA1 and over the course of multiple sessions in PFC. Despite both areas being highly engaged and synchronized during the task, we found no evidence for coordinated single cell or assembly activity during conditioning trials or aSWR. Taken together, our findings support the notion that persistent firing and reactivation of task-related neural activity patterns in CA1 and PFC support learning during classical conditioning.

Data availability

All data are publicly available on the Donders Repository (https://doi.org/10.34973/hp7x-4241). Analysis scripts can be downloaded via GitHub (https://github.com/chanlukas/AATCstudy).

The following data sets were generated

Article and author information

Author details

  1. Jan L Klee

    Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, Netherlands
    For correspondence
    janlukasklee@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4988-5682
  2. Bryan C Souza

    Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1041-4624
  3. Francesco P Battaglia

    Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, Netherlands
    For correspondence
    fpbattaglia@gmail.com
    Competing interests
    The authors declare that no competing interests exist.

Funding

Studienstiftung des Deutschen Volkes

  • Jan L Klee

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (612.001.853)

  • Bryan C Souza

NWA 'Bio-Art' project

  • Francesco P Battaglia

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

Ethics

Animal experimentation: This study was approved by the Central Commissie Dierproeven (CCD) in the Netherlands and conducted in accordance with the Experiments on Animals Act and the European Directive 2010/63/EU on animal research.

Reviewing Editor

  1. Kaori Takehara-Nishiuch, University of Toronto, Canada

Publication history

  1. Preprint posted: December 3, 2020 (view preprint)
  2. Received: December 4, 2020
  3. Accepted: October 10, 2021
  4. Accepted Manuscript published: October 19, 2021 (version 1)
  5. Version of Record published: October 25, 2021 (version 2)

Copyright

© 2021, Klee 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. Jan L Klee
  2. Bryan C Souza
  3. Francesco P Battaglia
(2021)
Learning differentially shapes prefrontal and hippocampal activity during classical conditioning
eLife 10:e65456.
https://doi.org/10.7554/eLife.65456

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