1. Neuroscience

Competing neural representations of choice shape evidence accumulation in humans

  1. Krista Alexandria Marie Bond  Is a corresponding author
  2. Javier Rasero Daparte
  3. Raghav Madan
  4. Jyotika Bahuguna
  5. Jonathan E Rubin
  6. Timothy Verstynen  Is a corresponding author
  1. Carnegie Mellon University, United States
  2. University of Washington, United States
  3. University of Pittsburgh, United States
https://doi.org/10.7554/eLife.85223
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  1. Krista Alexandria Marie Bond
  2. Javier Rasero Daparte
  3. Raghav Madan
  4. Jyotika Bahuguna
  5. Jonathan E Rubin
  6. Timothy Verstynen
(2023)
Competing neural representations of choice shape evidence accumulation in humans
eLife 12:e85223.
https://doi.org/10.7554/eLife.85223
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Abstract

Making adaptive choices in dynamic environments requires flexible decision policies. Previously, we showed how the evidence accumulation process that drives decisions shifts when outcome contingencies change (1). Using in silico experiments, here we show how the cortico-basal ganglia-thalamic (CBGT) circuits can feasibly implement shifts in the evidence accumulation process. When action contingencies change, dopaminergic plasticity redirects the balance of power, both within and between action representations, to divert the flow of evidence from one option to another. This model predicts that when competition between action representations is highest, the rate of evidence accumulation is lowest. This prediction was validated in in vivo experiments on human subjects, using fMRI, which showed that 1) evoked hemodynamic responses can reliably predict trialwise choices and 2) competition between action representations, measured using a classifier model, tracked with changes in the rate of evidence accumulation. These results paint a holistic picture of how CBGT circuits manage and adapt the evidence accumulation process in mammals.

Data availability

Behavioral data and computational derivatives are publically available here: https://github.com/kalexandriabond/competing-representations-shape-evidence-accumulation. Raw and preprocessed hemodynamic data, in addition to physiological measurements collected for quality control, are available here: https://openneuro.org/datasets/ds004283/versions/1.0.3.

The following data sets were generated

Article and author information

Author details

  1. Krista Alexandria Marie Bond

    Department of Psychology, Carnegie Mellon University, Pittsburgh, United States
    For correspondence
    kbond@andrew.cmu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1492-6798

  2. Javier Rasero Daparte

    Department of Psychology, Carnegie Mellon University, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Raghav Madan

    Department of Biomedical and Health Informatics, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9790-393X

  4. Jyotika Bahuguna

    Department of Psychology, Carnegie Mellon University, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2858-5325

  5. Jonathan E Rubin

    Department of Mathematics, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1513-1551

  6. Timothy Verstynen

    Department of Psychology, Carnegie Mellon University, Pittsburgh, United States
    For correspondence
    timothyv@andrew.cmu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4720-0336

Funding

Air Force Research Laboratory (180119)

  • Timothy Verstynen

National Institutes of Health (CRCNS: R01DA053014)

  • Timothy Verstynen

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

Ethics

Human subjects: All procedures were approved by the Carnegie Mellon University Institutional Review Board (Approval Code: 2018_00000195).All research participants provided informed consent to participate in the study and consent to publish any research findings based on their provided data.

Copyright

© 2023, Bond 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. Krista Alexandria Marie Bond
  2. Javier Rasero Daparte
  3. Raghav Madan
  4. Jyotika Bahuguna
  5. Jonathan E Rubin
  6. Timothy Verstynen
(2023)
Competing neural representations of choice shape evidence accumulation in humans
eLife 12:e85223.
https://doi.org/10.7554/eLife.85223

Share this article

https://doi.org/10.7554/eLife.85223

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