Abstract

Neural activity in the mammalian cortex has been studied extensively during decision tasks, and recent work aims to identify under what conditions cortex is actually necessary for these tasks. We discovered that mice with distinct cognitive experiences, beyond sensory and motor learning, use different cortical areas and neural activity patterns to solve the same navigation decision task, revealing past learning as a critical determinant of whether cortex is necessary for goal-directed navigation. We used optogenetics and calcium imaging to study the necessity and neural activity of multiple cortical areas in mice with different training histories. Posterior parietal cortex and retrosplenial cortex were mostly dispensable for accurate performance of a simple navigation task. In contrast, these areas were essential for the same simple task when mice were previously trained on complex tasks with delay periods or association switches. Multi-area calcium imaging showed that, in mice with complex-task experience, single-neuron activity had higher selectivity and neuron-neuron correlations were weaker, leading to codes with higher task information. Therefore, past experience is a key factor in determining whether cortical areas have a causal role in goal-directed navigation.

Data availability

Data have been deposited in Dryad with the DOI: https://doi.org/10.5061/dryad.34tmpg4nr.

The following data sets were generated

Article and author information

Author details

  1. Charlotte Arlt

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Roberto Barroso-Luque

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Shinichiro Kira

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Carissa A Bruno

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7126-2185
  5. Ningjing Xia

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Selmaan N Chettih

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Sofia Soares

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Noah L Pettit

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Christopher D Harvey

    Department of Neurobiology, Harvard Medical School, Boston, United States
    For correspondence
    harvey@hms.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9850-2268

Funding

National Institutes of Health (R01 MH107620)

  • Christopher D Harvey

JSPS Overseas Research Fellowship

  • Shinichiro Kira

EMBO Postdoctoral Fellowship

  • Sofia Soares

Stuart H.Q. & Victoria Quan Fellowship

  • Noah L Pettit

National Institutes of Health (R01 NS089521)

  • Christopher D Harvey

National Institutes of Health (R01 NS108410)

  • Christopher D Harvey

National Institutes of Health (DP1 MH125776)

  • Christopher D Harvey

Louis Perry Jones Postdoctoral Fellowship

  • Charlotte Arlt

Alice and Joseph Brooks Postdoctoral Fellowship

  • Charlotte Arlt

Uehara Foundation Research Fellowship

  • Shinichiro Kira

Leonard and Isabelle Goldenson Postdoctoral Fellowship

  • Shinichiro Kira

NARSAD Young Investigator Grant

  • Shinichiro Kira

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

Reviewing Editor

  1. Mathieu Wolff, CNRS, University of Bordeaux, France

Ethics

Animal experimentation: All experimental procedures were approved by the Harvard Medical School Institutional Animal Care and Use Committee (protocol # 00000073-6) and were performed in compliance with the Guide for the Care and Use of Laboratory Animals.

Version history

  1. Received: December 2, 2021
  2. Preprint posted: December 10, 2021 (view preprint)
  3. Accepted: June 22, 2022
  4. Accepted Manuscript published: June 23, 2022 (version 1)
  5. Version of Record published: July 6, 2022 (version 2)

Copyright

© 2022, Arlt 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. Charlotte Arlt
  2. Roberto Barroso-Luque
  3. Shinichiro Kira
  4. Carissa A Bruno
  5. Ningjing Xia
  6. Selmaan N Chettih
  7. Sofia Soares
  8. Noah L Pettit
  9. Christopher D Harvey
(2022)
Cognitive experience alters cortical involvement in goal-directed navigation
eLife 11:e76051.
https://doi.org/10.7554/eLife.76051

Share this article

https://doi.org/10.7554/eLife.76051

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