Inhibition is a prevalent mode of activity in the neocortex around awake hippocampal ripples in mice

  1. Javad Karimi Abadchi
  2. Zahra Rezaei
  3. Thomas Knöpfel
  4. Bruce L McNaughton
  5. Majid H Mohajerani  Is a corresponding author
  1. University of Lethbridge, Canada
  2. Imperial College London, United Kingdom

Abstract

Coordinated peri-ripple activity in the hippocampal-neocortical network is essential for mnemonic information processing in the brain. Hippocampal ripples likely serve different functions in sleep and awake states. Thus, the corresponding neocortical activity patterns may differ in important ways. We addressed this possibility by conducting voltage and glutamate wide-field imaging of the neocortex with concurrent hippocampal electrophysiology in awake mice. Contrary to our previously published sleep results, deactivation and activation were dominant in post-ripple neocortical voltage and glutamate activity, respectively, especially in the agranular retrosplenial cortex (aRSC). Additionally, the spiking activity of aRSC neurons, estimated by two-photon calcium imaging, revealed the existence of two subpopulations of excitatory neurons with opposite peri-ripple modulation patterns: one increases and the other decreases firing rate. These differences in peri-ripple spatiotemporal patterns of neocortical activity in sleep versus awake states might underlie the reported differences in the function of sleep versus awake ripples.

Data availability

The data used to obtain the results of this article have been deposited on Dryad and can be reached via https://doi.org/10.5061/dryad.8kprr4xrk

The following data sets were generated

Article and author information

Author details

  1. Javad Karimi Abadchi

    Canadian Centre for Behavioral Neuroscience, University of Lethbridge, Lethbridge, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4175-7598
  2. Zahra Rezaei

    Canadian Centre for Behavioral Neuroscience, University of Lethbridge, Lethbridge, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Thomas Knöpfel

    Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5718-0765
  4. Bruce L McNaughton

    Canadian Centre for Behavioural Neuroscience, University of Lethbridge, Lethbridge, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Majid H Mohajerani

    Canadian Centre for Behavioral Neuroscience, University of Lethbridge, Lethbridge, Canada
    For correspondence
    mohajerani@uleth.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0964-2977

Funding

Natural Sciences and Engineering Research Council of Canada (40352)

  • Majid H Mohajerani

Alberta Prion Research Institute (43568)

  • Majid H Mohajerani

Canadian Institutes of Health Research (390930)

  • Majid H Mohajerani

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

Reviewing Editor

  1. Adrien Peyrache, McGill University, Canada

Ethics

Animal experimentation: The animal protocol (#2209) was approved by the University of Lethbridge Animal Care Committee and was in accordance with guidelines set forth by the Canadian Council for Animal Care.

Version history

  1. Preprint posted: March 4, 2022 (view preprint)
  2. Received: April 15, 2022
  3. Accepted: January 6, 2023
  4. Accepted Manuscript published: January 16, 2023 (version 1)
  5. Version of Record published: January 25, 2023 (version 2)

Copyright

© 2023, Karimi Abadchi 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. Javad Karimi Abadchi
  2. Zahra Rezaei
  3. Thomas Knöpfel
  4. Bruce L McNaughton
  5. Majid H Mohajerani
(2023)
Inhibition is a prevalent mode of activity in the neocortex around awake hippocampal ripples in mice
eLife 12:e79513.
https://doi.org/10.7554/eLife.79513

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https://doi.org/10.7554/eLife.79513

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