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Temporally organized representations of reward and risk in the human brain

Author

Listed:
  • Vincent Man

    (California Institute of Technology)

  • Jeffrey Cockburn

    (California Institute of Technology)

  • Oliver Flouty

    (University of South Florida)

  • Phillip E. Gander

    (University of Iowa Hospitals and Clinics
    University of Iowa Hospitals and Clinics
    University of Iowa Carver College of Medicine)

  • Masahiro Sawada

    (University of Iowa Hospitals and Clinics)

  • Christopher K. Kovach

    (University of Iowa Hospitals and Clinics
    University of Nebraska Medical Center)

  • Hiroto Kawasaki

    (University of Iowa Hospitals and Clinics)

  • Hiroyuki Oya

    (University of Iowa Hospitals and Clinics
    University of Iowa Carver College of Medicine)

  • Matthew A. Howard III

    (University of Iowa Hospitals and Clinics
    University of Iowa Carver College of Medicine)

  • John P. O’Doherty

    (California Institute of Technology
    California Institute of Technology)

Abstract

The value and uncertainty associated with choice alternatives constitute critical features relevant for decisions. However, the manner in which reward and risk representations are temporally organized in the brain remains elusive. Here we leverage the spatiotemporal precision of intracranial electroencephalography, along with a simple card game designed to elicit the unfolding computation of a set of reward and risk variables, to uncover this temporal organization. Reward outcome representations across wide-spread regions follow a sequential order along the anteroposterior axis of the brain. In contrast, expected value can be decoded from multiple regions at the same time, and error signals in both reward and risk domains reflect a mixture of sequential and parallel encoding. We further highlight the role of the anterior insula in generalizing between reward prediction error and risk prediction error codes. Together our results emphasize the importance of neural dynamics for understanding value-based decisions under uncertainty.

Suggested Citation

  • Vincent Man & Jeffrey Cockburn & Oliver Flouty & Phillip E. Gander & Masahiro Sawada & Christopher K. Kovach & Hiroto Kawasaki & Hiroyuki Oya & Matthew A. Howard III & John P. O’Doherty, 2024. "Temporally organized representations of reward and risk in the human brain," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46094-1
    DOI: 10.1038/s41467-024-46094-1
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    References listed on IDEAS

    as
    1. Harry Markowitz, 1952. "The Utility of Wealth," Journal of Political Economy, University of Chicago Press, vol. 60(2), pages 151-151.
    2. Rongjun Yu & Wu Zhou & Xiaolin Zhou, 2011. "Rapid Processing of Both Reward Probability and Reward Uncertainty in the Human Anterior Cingulate Cortex," PLOS ONE, Public Library of Science, vol. 6(12), pages 1-7, December.
    3. Colin W. Hoy & David R. Quiroga-Martinez & Eduardo Sandoval & David King-Stephens & Kenneth D. Laxer & Peter Weber & Jack J. Lin & Robert T. Knight, 2023. "Asymmetric coding of reward prediction errors in human insula and dorsomedial prefrontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Tomas G. Aquino & Jeffrey Cockburn & Adam N. Mamelak & Ueli Rutishauser & John P. O’Doherty, 2023. "Neurons in human pre-supplementary motor area encode key computations for value-based choice," Nature Human Behaviour, Nature, vol. 7(6), pages 970-985, June.
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