Parvalbumin-positive interneurons mediate cortical-hippocampal interactions that are necessary for memory consolidation

Abstract

Following learning, increased coupling between spindle oscillations in the medial prefrontal cortex (mPFC) and ripple oscillations in the hippocampus is thought to underlie memory consolidation. However, whether learning-induced increases in ripple-spindle coupling are necessary for successful memory consolidation has not been tested directly. In order to decouple ripple-spindle oscillations, here we chemogenetically inhibited parvalbumin-positive (PV+) interneurons, since their activity is important for regulating the timing of spiking activity during oscillations. We found that contextual fear conditioning increased ripple-spindle coupling in mice. However, inhibition of PV+ cells in either CA1 or mPFC eliminated this learning-induced increase in ripple-spindle coupling without affecting ripple or spindle incidence. Consistent with the hypothesized importance of ripple-spindle coupling in memory consolidation, post-training inhibition of PV+ cells disrupted contextual fear memory consolidation. These results indicate that successful memory consolidation requires coherent hippocampal-neocortical communication mediated by PV+ cells.

Article and author information

Author details

  1. Frances Xia

    Department of Physiology, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. Blake A Richards

    Department of Biological Sciences, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9662-2151
  3. Matthew M Tran

    Department of Biological Sciences, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Sheena A Josselyn

    Department of Physiology, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5451-489X
  5. Kaori Takehara-Nishiuchi

    Department of Cell and Systems Biology, University of Toronto, Toronto, Canada
    For correspondence
    takehara@psych.utoronto.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7282-7838
  6. Paul W Frankland

    Department of Physiology, University of Toronto, Toronto, Canada
    For correspondence
    paul.frankland@sickkids.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1395-3586

Funding

Canadian Institutes of Health Research (FDN143227)

  • Paul W Frankland

Canadian Institutes of Health Research (MOP74650)

  • Sheena A Josselyn

Natural Sciences and Engineering Research Council of Canada (RGPIN-2015-05458)

  • Kaori Takehara-Nishiuchi

Natural Sciences and Engineering Research Council of Canada (RGPIN-2014-04947)

  • Blake A Richards

Natural Sciences and Engineering Research Council of Canada

  • Frances Xia

Natural Sciences and Engineering Research Council of Canada

  • Matthew M Tran

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

Reviewing Editor

  1. Marlene Bartos, University of Freiburg, Germany

Ethics

Animal experimentation: All procedures in this study were approved by the Canadian Council for Animal Care (CCAC) and the Animal Care Committees at the Hospital for Sick Children and the University of Toronto.

Version history

  1. Received: April 17, 2017
  2. Accepted: September 28, 2017
  3. Accepted Manuscript published: September 29, 2017 (version 1)
  4. Version of Record published: October 24, 2017 (version 2)

Copyright

© 2017, Xia 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. Frances Xia
  2. Blake A Richards
  3. Matthew M Tran
  4. Sheena A Josselyn
  5. Kaori Takehara-Nishiuchi
  6. Paul W Frankland
(2017)
Parvalbumin-positive interneurons mediate cortical-hippocampal interactions that are necessary for memory consolidation
eLife 6:e27868.
https://doi.org/10.7554/eLife.27868

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https://doi.org/10.7554/eLife.27868

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