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Dopamine neuron ensembles signal the content of sensory prediction errors

Thomas A. Stalnaker, View ORCID ProfileJames D. Howard, Yuji K. Takahashi, View ORCID ProfileSamuel J. Gershman, View ORCID ProfileThorsten Kahnt, View ORCID ProfileGeoffrey Schoenbaum
doi: https://doi.org/10.1101/723908
Thomas A. Stalnaker
Intramural Research program of the National Institute on Drug Abuse, NIH
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  • For correspondence: thomas.stalnaker@nih.gov james.howard@northwestern.edu thorsten.kahnt@northwestern.edu geoffrey.schoenbaum@nih.gov
James D. Howard
Department of Neurology, Feinberg School of Medicine, Northwestern University
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  • ORCID record for James D. Howard
  • For correspondence: thomas.stalnaker@nih.gov james.howard@northwestern.edu thorsten.kahnt@northwestern.edu geoffrey.schoenbaum@nih.gov
Yuji K. Takahashi
Intramural Research program of the National Institute on Drug Abuse, NIH
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Samuel J. Gershman
Department of Psychology and Center for Brain Science, Harvard University
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Thorsten Kahnt
Department of Neurology, Feinberg School of Medicine, Northwestern University
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  • For correspondence: thomas.stalnaker@nih.gov james.howard@northwestern.edu thorsten.kahnt@northwestern.edu geoffrey.schoenbaum@nih.gov
Geoffrey Schoenbaum
Intramural Research program of the National Institute on Drug Abuse, NIHDepartment of Anatomy and Neurobiology, University of Maryland School of MedicineDepartment of Neuroscience, Johns Hopkins School of Medicine
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  • ORCID record for Geoffrey Schoenbaum
  • For correspondence: thomas.stalnaker@nih.gov james.howard@northwestern.edu thorsten.kahnt@northwestern.edu geoffrey.schoenbaum@nih.gov
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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.

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  • ↵* shared first or senior authorship

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted August 02, 2019.
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Dopamine neuron ensembles signal the content of sensory prediction errors
Thomas A. Stalnaker, James D. Howard, Yuji K. Takahashi, Samuel J. Gershman, Thorsten Kahnt, Geoffrey Schoenbaum
bioRxiv 723908; doi: https://doi.org/10.1101/723908
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Dopamine neuron ensembles signal the content of sensory prediction errors
Thomas A. Stalnaker, James D. Howard, Yuji K. Takahashi, Samuel J. Gershman, Thorsten Kahnt, Geoffrey Schoenbaum
bioRxiv 723908; doi: https://doi.org/10.1101/723908

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