1. Neuroscience
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Stable and dynamic representations of value in the prefrontal cortex

  1. Pierre Enel  Is a corresponding author
  2. Joni D Wallis
  3. Erin L Rich
  1. Icahn School of Medicine at Mount Sinai, United States
  2. University of California, Berkeley, United States
Research Article
  • Cited 11
  • Views 2,993
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Cite this article as: eLife 2020;9:e54313 doi: 10.7554/eLife.54313

Abstract

Optimal decision-making requires that stimulus-value associations are kept up to date by constantly comparing the expected value of a stimulus with its experienced outcome. To do this, value information must be held in mind when a stimulus and outcome are separated in time. However, little is known about the neural mechanisms of working memory (WM) for value. Contradicting theories have suggested WM requires either persistent or transient neuronal activity, with stable or dynamic representations respectively. To test these hypotheses, we recorded neuronal activity in the orbitofrontal and anterior cingulate cortex of two monkeys performing a valuation task. We found that features of all hypotheses were simultaneously present in prefrontal activity, and no single hypothesis was exclusively supported. Instead, mixed dynamics supported robust, time invariant value representations while also encoding the information in a temporally specific manner. We suggest that this hybrid coding is a critical mechanism supporting flexible cognitive abilities.

Data availability

The neural recording data analyzed in this paper is available online at https://doi.org/10.5061/dryad.4j0zpc88b

The following data sets were generated

Article and author information

Author details

  1. Pierre Enel

    Department of Neurosience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, United States
    For correspondence
    pierre.enel@mssm.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8983-6223
  2. Joni D Wallis

    Helen Wills Neuroscience Institute, Department of Psychology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Erin L Rich

    Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institute of Mental Health (R01-MH121448)

  • Joni D Wallis

National Institute of Mental Health (R01-MH097990)

  • Joni D Wallis

Hilda and Preston Davis Foundation (Postdoctoral fellowship)

  • Erin L Rich

National Institute on Drug Abuse (K08-DA039051)

  • Erin L Rich

National Institute of Mental Health (R01-MH117763)

  • Joni D Wallis

Whitehall Foundation Research Grant (Postdoctoral fellowship)

  • Erin L Rich

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health (Assurance Number A3084-01). All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (Protocol Number R283) of the University of California at Berkeley. All surgery was performed under isoflurane anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. Geoffrey Schoenbaum, National Institute on Drug Abuse, National Institutes of Health, United States

Publication history

  1. Received: December 10, 2019
  2. Accepted: July 6, 2020
  3. Accepted Manuscript published: July 6, 2020 (version 1)
  4. Accepted Manuscript updated: July 8, 2020 (version 2)
  5. Version of Record published: July 29, 2020 (version 3)

Copyright

© 2020, Enel 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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