Spatiotemporal patterns of neocortical activity around hippocampal sharp-wave ripples

  1. Javad Karimi Abadchi
  2. Mojtaba Nazari-Ahangarkolaee
  3. Sandra Gattas
  4. Edgar Bermudez-Contreras
  5. Artur Luczak
  6. Bruce L McNaughton  Is a corresponding author
  7. Majid H Mohajerani  Is a corresponding author
  1. University of Lethbridge, Canada
  2. University of California, Irvine, United States

Abstract

A prevalent model is that sharp-wave ripples (SWR) arise 'spontaneously' in CA3 and propagate recent memory traces outward to the neocortex to facilitate memory consolidation there. Using voltage and extracellular glutamate transient recording over widespread regions of mice dorsal neocortex in relation to CA1 multiunit activity (MUA) and SWR, we find that the largest SWR-related modulation occurs in retrosplenial cortex; however, contrary to the unidirectional hypothesis, neocortical activation exhibited a continuum of activation timings relative to SWRs, varying from leading to lagging. Thus, contrary to the model in which SWRs arise 'spontaneously' in the hippocampus, neocortical activation often precedes SWRs and may thus constitute a trigger event in which neocortical information seeds associative reactivation of hippocampal 'indices'. This timing continuum is consistent with a dynamics in which older, more consolidated memories may in fact initiate the hippocampal-neocortical dialog, whereas reactivation of newer memories may be initiated predominantly in the hippocampus.

Data availability

All data analyzed and used to produce the main findings of this study have been deposited on Dryad. Source data files have been provided for Figures 2, 3, 5, and 7.

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.
  2. Mojtaba Nazari-Ahangarkolaee

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

    Department of Electrical Engineering and Computer Science, University of California, Irvine, Irvine, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Edgar Bermudez-Contreras

    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:" 0000-0002-4937-1780
  5. Artur Luczak

    Canadian Center for Behavioural Neuroscience, University of Lethbridge, Lethbridge, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Bruce L McNaughton

    Canadian Centre for Behavioural Neuroscience, University of Lethbridge, Lethbridge, Canada
    For correspondence
    bruce.mcnaughton@uleth.ca
    Competing interests
    The authors declare that no competing interests exist.
  7. 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

Natural Sciences and Engineering Research Council of Canada (1631465)

  • Bruce L McNaughton

Alberta Innovates - Health Solutions

  • Majid H Mohajerani

Canadian Institutes of Health Research (390930)

  • Majid H Mohajerani

Canadian Institutes of Health Research (156040)

  • Bruce L McNaughton

Defense Advanced Research Projects Agency (HR0011-18-2-0021)

  • Bruce L McNaughton

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

Reviewing Editor

  1. Sachin Deshmukh, Indian Institute of Science Bangalore, India

Ethics

Animal experimentation: The animal housing, handling, and surgery protocols (#1812) were approved by the University of Lethbridge Animal Care Committee and were in accordance with guidelines set forth by the Canadian Council for Animal Care.

Version history

  1. Received: September 18, 2019
  2. Accepted: March 11, 2020
  3. Accepted Manuscript published: March 13, 2020 (version 1)
  4. Version of Record published: March 25, 2020 (version 2)
  5. Version of Record updated: March 27, 2020 (version 3)

Copyright

© 2020, 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. Mojtaba Nazari-Ahangarkolaee
  3. Sandra Gattas
  4. Edgar Bermudez-Contreras
  5. Artur Luczak
  6. Bruce L McNaughton
  7. Majid H Mohajerani
(2020)
Spatiotemporal patterns of neocortical activity around hippocampal sharp-wave ripples
eLife 9:e51972.
https://doi.org/10.7554/eLife.51972

Share this article

https://doi.org/10.7554/eLife.51972

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