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Dopamine neuron ensembles signal the content of sensory prediction errors

  1. Thomas Stalnaker  Is a corresponding author
  2. James D Howard
  3. Yuji K Takahashi
  4. Samuel J Gershman
  5. Thorsten Kahnt
  6. Geoffrey Schoenbaum  Is a corresponding author
  1. National Institute on Drug Abuse, National Institutes of Health, United States
  2. Northwestern University, United States
  3. Harvard University, United States
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Cite this article as: eLife 2019;8:e49315 doi: 10.7554/eLife.49315

Abstract

Dopamine neurons respond to errors in predicting value-neutral sensory information. These data, combined with causal evidence that dopamine transients support sensory-based associative learning, suggest that the dopamine system signals a multidimensional prediction error. Yet such complexity is not evident in individual neuron or average neural activity. How then do downstream areas know what to learn in response to these signals? One possibility is that information about content is contained in the pattern of firing across many dopamine neurons. Consistent with this, here we show that the pattern of firing across a small group of dopamine neurons recorded in rats signals the identity of a mis-predicted sensory event. Further, this same information is reflected in the BOLD response elicited by sensory prediction errors in human midbrain. These data provide evidence that ensembles of dopamine neurons provide highly specific teaching signals, opening new possibilities for how this system might contribute to learning.

Article and author information

Author details

  1. Thomas Stalnaker

    Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health, Baltimore, United States
    For correspondence
    thomas.stalnaker@nih.gov
    Competing interests
    No competing interests declared.
  2. James D Howard

    Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9309-3773
  3. Yuji K Takahashi

    Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health, Baltimore, United States
    Competing interests
    No competing interests declared.
  4. Samuel J Gershman

    Department of Psychology, Harvard University, Cambridge, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6546-3298
  5. Thorsten Kahnt

    Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, United States
    Competing interests
    Thorsten Kahnt, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3575-2670
  6. Geoffrey Schoenbaum

    Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health, Baltimore, United States
    For correspondence
    geoffrey.schoenbaum@nih.gov
    Competing interests
    Geoffrey Schoenbaum, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8180-0701

Funding

National Institute on Drug Abuse (ZIA-DA000587)

  • Geoffrey Schoenbaum

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. All of the animals were handled according to approved institutional animal care and use committee protocols of the NIH. The protocol (#18-CNRB-108) was approved by the NIDA-IRP ACUC. All surgery was performed under isoflurane anesthesia, and every effort was made to minimize suffering.

Human subjects: Subjects gave informed consent to participate in the experiment. The protocol (#STU00098371) and consent forms were approved by Northwestern University's Institutional Review Board.

Reviewing Editor

  1. Kate M Wassum, University of California, Los Angeles, United States

Publication history

  1. Received: August 2, 2019
  2. Accepted: October 28, 2019
  3. Accepted Manuscript published: November 1, 2019 (version 1)
  4. Version of Record published: November 8, 2019 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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