Distinct recruitment of dorsomedial and dorsolateral striatum erodes with extended training

  1. Youna Vandaele  Is a corresponding author
  2. Nagaraj R Mahajan
  3. David Joshua Ottenheimer
  4. Jocelyn M Richard
  5. Shreesh P Mysore
  6. Patricia H Janak  Is a corresponding author
  1. Johns Hopkins University, United States
  2. University of Minnesota, United States

Abstract

Hypotheses of striatal orchestration of behavior ascribe distinct functions to striatal subregions, with the dorsolateral striatum (DLS) especially implicated in habitual and skilled performance. Thus neural activity patterns recorded from the DLS, but not the dorsomedial striatum (DMS), should be correlated with habitual and automatized performance. Here, we recorded DMS and DLS neural activity in rats during training in a task promoting habitual lever pressing. Despite improving performance across sessions, clear changes in corresponding neural activity patterns were not evident in DMS or DLS during early training. Although DMS and DLS activity patterns were distinct during early training, their activity was similar following extended training. Finally, performance after extended training was not associated with DMS disengagement, as would be predicted from prior work. These results suggest that behavioral sequences may continue to engage both striatal regions long after initial acquisition, when skilled performance is consolidated.

Data availability

Behavioral and single unit recording data have been deposited on G-Node, as well as the Matlab codes used to analyze the data and generate the figures.

The following data sets were generated

Article and author information

Author details

  1. Youna Vandaele

    Department of Psychological and Brain Sciences, Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, United States
    For correspondence
    youna.vandaele@jhu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8389-8850
  2. Nagaraj R Mahajan

    Department of Electrical and Computer Engineering, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. David Joshua Ottenheimer

    The Solomon H Snyder Department of Neuroscience, Johns Hopkins School of Medicine, Johns Hopkins University, Balitmore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4882-1898
  4. Jocelyn M Richard

    Department of Neuroscience, University of Minnesota, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5750-0418
  5. Shreesh P Mysore

    Department of Psychological and Brain Sciences, Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7781-8252
  6. Patricia H Janak

    Department of Psychological and Brain Sciences, Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, United States
    For correspondence
    patricia.janak@jhu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3333-9049

Funding

National Institute for Health Research (R01DA035943)

  • Patricia H Janak

National Institute on Alcohol Abuse and Alcoholism (R01AA026306)

  • Patricia H Janak

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

Reviewing Editor

  1. Naoshige Uchida, Harvard University, United States

Ethics

Animal experimentation: This study was carried out in accordance with the recommendations of the Guide for the Care and Use of Laboratory Animals (National Research Council, 1996), and was approved by the institutional animal care and use committee of Johns Hopkins University (protocols #RA17A244).

Version history

  1. Received: June 20, 2019
  2. Accepted: October 16, 2019
  3. Accepted Manuscript published: October 17, 2019 (version 1)
  4. Version of Record published: October 31, 2019 (version 2)

Copyright

© 2019, Vandaele 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. Youna Vandaele
  2. Nagaraj R Mahajan
  3. David Joshua Ottenheimer
  4. Jocelyn M Richard
  5. Shreesh P Mysore
  6. Patricia H Janak
(2019)
Distinct recruitment of dorsomedial and dorsolateral striatum erodes with extended training
eLife 8:e49536.
https://doi.org/10.7554/eLife.49536

Share this article

https://doi.org/10.7554/eLife.49536

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