1. Neuroscience
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Distinct hippocampal-cortical memory representations for experiences associated with movement versus immobility

  1. Jai Y Yu
  2. Kenneth Kay
  3. Daniel F Liu
  4. Irene Grossrubatscher
  5. Adrianna Loback
  6. Marielena Sosa
  7. Jason E Chung
  8. Mattias P Karlsson
  9. Margaret C Larkin
  10. Loren M Frank  Is a corresponding author
  1. University of California San Francisco, United States
  2. University of California Berkeley, United States
  3. Princeton University, United States
Research Article
  • Cited 17
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Cite this article as: eLife 2017;6:e27621 doi: 10.7554/eLife.27621

Abstract

While ongoing experience proceeds continuously, memories of past experience are often recalled as episodes with defined beginnings and ends. The neural mechanisms that lead to the formation of discrete episodes from the stream of neural activity patterns representing ongoing experience are unknown. To investigate these mechanisms, we recorded neural activity in the rat hippocampus and prefrontal cortex, structures critical for memory processes. We show that during spatial navigation, hippocampal CA1 place cells maintain a continuous spatial representation across different states of motion (movement and immobility). In contrast, during sharp-wave ripples (SWRs), when representations of experience are transiently reactivated from memory, movement- and immobility-associated activity patterns are most often reactivated separately. Concurrently, distinct hippocampal reactivations of movement- or immobility-associated representations are accompanied by distinct modulation patterns in prefrontal cortex. These findings demonstrate a continuous representation of ongoing experience can be separated into independently reactivated memory representations.

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Article and author information

Author details

  1. Jai Y Yu

    UCSF Center for Integrative Neuroscience, University of California San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Kenneth Kay

    UCSF Center for Integrative Neuroscience, University of California San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Daniel F Liu

    University of California Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Irene Grossrubatscher

    University of California Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Adrianna Loback

    Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Marielena Sosa

    UCSF Center for Integrative Neuroscience, University of California San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Jason E Chung

    UCSF Center for Integrative Neuroscience, University of California San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Mattias P Karlsson

    UCSF Center for Integrative Neuroscience, University of California San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Margaret C Larkin

    UCSF Center for Integrative Neuroscience, University of California San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Loren M Frank

    UCSF Center for Integrative Neuroscience, University of California San Francisco, San Francisco, United States
    For correspondence
    loren@phy.ucsf.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1752-5677

Funding

National Institute of Mental Health (RO1MH105174)

  • Jai Y Yu
  • Kenneth Kay
  • Daniel F Liu
  • Marielena Sosa
  • Jason E Chung
  • Loren M Frank

Jane Coffin Childs Memorial Fund for Medical Research

  • Jai Y Yu

University of California (LF-12-237680)

  • Loren M Frank

Howard Hughes Medical Institute

  • Jai Y Yu
  • Kenneth Kay
  • Loren M Frank

National Institute of Mental Health (R01MH097084)

  • Loren M Frank

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 experiments were conducted in accordance with University of California San Francisco Institutional Animal Care and Use Committee and US National Institutes of Health guidelines. The protocol was approved by the Institutional Animal Care and Use Committee, approval number AN110101-03B. All surgical procedures were performed under anesthesia and every effort was made to minimize suffering.

Reviewing Editor

  1. Neil Burgess, University College London, United Kingdom

Publication history

  1. Received: April 9, 2017
  2. Accepted: July 31, 2017
  3. Accepted Manuscript published: August 3, 2017 (version 1)
  4. Version of Record published: August 25, 2017 (version 2)

Copyright

© 2017, Yu 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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