Distinct memory engrams in the infralimbic cortex of rats control opposing environmental actions on a learned behavior

  1. Nobuyoshi Suto  Is a corresponding author
  2. Amanda Laque
  3. Genna L De Ness
  4. Grant E Wagner
  5. Debbie Watry
  6. Tony Kerr
  7. Eisuke Koya
  8. Mark R Mayford
  9. Bruce T Hope  Is a corresponding author
  10. Friedbert Weiss  Is a corresponding author
  1. The Scripps Research Institute, United States
  2. University of Sussex, United Kingdom
  3. University of California San Diego, United States
  4. National Institute on Drug Abuse, United States

Abstract

Conflicting evidence exists regarding the role of infralimbic cortex (IL) in the environmental control of appetitive behavior. Inhibition of IL, irrespective of its intrinsic neural activity, attenuates not only the ability of environmental cues predictive of reward availability to promote reward seeking, but also the ability of environmental cues predictive of reward omission to suppress this behavior. Here we report that such bidirectional behavioral modulation in rats is mediated by functionally distinct units of neurons (neural ensembles) that are concurrently localized within the same IL brain area but selectively reactive to different environmental cues. Ensemble-specific neural activity is thought to function as a memory engram representing a learned association between environment and behavior. Our findings establish the causal evidence for the concurrent existence of two distinct engrams within a single brain site, each mediating opposing environmental actions on a learned behavior.

Article and author information

Author details

  1. Nobuyoshi Suto

    Department of Molecular and Cellular Neuroscience, The Scripps Research Institute, La Jolla, United States
    For correspondence
    nsuto@scripps.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8994-2592
  2. Amanda Laque

    Department of Molecular and Cellular Neuroscience, The Scripps Research Institute, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Genna L De Ness

    Department of Molecular and Cellular Neuroscience, The Scripps Research Institute, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Grant E Wagner

    Department of Molecular and Cellular Neuroscience, The Scripps Research Institute, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Debbie Watry

    Department of Molecular and Cellular Neuroscience, The Scripps Research Institute, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Tony Kerr

    Department of Molecular and Cellular Neuroscience, The Scripps Research Institute, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Eisuke Koya

    Sussex School of Psychology, University of Sussex, Brighton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Mark R Mayford

    Department of Psychiatry, University of California San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Bruce T Hope

    Behavioral Neuroscience Branch, National Institute on Drug Abuse, Baltimore, United States
    For correspondence
    bhope@intra.nida.nih.gov
    Competing interests
    The authors declare that no competing interests exist.
  10. Friedbert Weiss

    Department of Molecular and Cellular Neuroscience, The Scripps Research Institute, La Jolla, United States
    For correspondence
    bweiss@scripps.edu
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institute on Drug Abuse (R21DA033533)

  • Nobuyoshi Suto

National Institute on Alcohol Abuse and Alcoholism (R01AA023183)

  • Nobuyoshi Suto

National Institute on Drug Abuse (R01DA037294)

  • Nobuyoshi Suto

National Institute on Alcohol Abuse and Alcoholism (R01AA021549)

  • Friedbert Weiss

National Institute on Drug Abuse (ZIADA000467)

  • Bruce T Hope

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

Reviewing Editor

  1. Howard Eichenbaum, Boston University, United States

Ethics

Animal experimentation: All experimental procedures were conducted in adherence to the National Institutes of Health Guide for the Care and Use of Laboratory Animals and were approved by the Institutional Animal Care and Use Committee of The Scripps Research Institute. (animal protocol #12-0032).

Version history

  1. Received: September 28, 2016
  2. Accepted: December 9, 2016
  3. Accepted Manuscript published: December 10, 2016 (version 1)
  4. Version of Record published: December 30, 2016 (version 2)

Copyright

© 2016, Suto 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. Nobuyoshi Suto
  2. Amanda Laque
  3. Genna L De Ness
  4. Grant E Wagner
  5. Debbie Watry
  6. Tony Kerr
  7. Eisuke Koya
  8. Mark R Mayford
  9. Bruce T Hope
  10. Friedbert Weiss
(2016)
Distinct memory engrams in the infralimbic cortex of rats control opposing environmental actions on a learned behavior
eLife 5:e21920.
https://doi.org/10.7554/eLife.21920

Share this article

https://doi.org/10.7554/eLife.21920

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