Pallidal neuromodulation of the explore/exploit trade-off in decision-making

  1. Ana Luisa de A. Marcelino
  2. Owen Gray
  3. Bassam Al-Fatly
  4. William Gilmour
  5. J Douglas Steele
  6. Andrea A Kühn
  7. Tom Gilbertson  Is a corresponding author
  1. Charité - Universitätsmedizin Berlin, Germany
  2. University of Dundee, United Kingdom

Abstract

Every decision that we make involves a conflict between exploiting our current knowledge of an action's value or exploring alternative courses of action that might lead to a better, or worse outcome. The sub-cortical nuclei that make up the basal ganglia have been proposed as a neural circuit that may contribute to resolving this explore-exploit 'dilemma'. To test this hypothesis, we examined the effects of neuromodulating the basal ganglia's output nucleus, the globus pallidus interna, in patients who had undergone deep brain stimulation (DBS) for isolated dystonia. Neuromodulation enhanced the number of exploratory choices to the lower value option in a 2-armed bandit probabilistic reversal-learning task. Enhanced exploration was explained by a reduction in the rate of evidence accumulation (drift rate) in a reinforcement learning drift diffusion model. We estimated the functional connectivity profile between the stimulating DBS electrode and the rest of the brain using a normative functional connectome derived from heathy controls. Variation in the extent of neuromodulation induced exploration between patients was associated with functional connectivity from the stimulation electrode site to a distributed brain functional network. We conclude that the basal ganglia's output nucleus, the globus pallidus interna, can adaptively modify decision choice when faced with the dilemma to explore or exploit.

Data availability

Raw choice and reaction time data, computational model parameter estimates, simulated data and r-maps from connectivity analysis are available via the Open Science Framework https://osf.io/fs36g/

The following data sets were generated

Article and author information

Author details

  1. Ana Luisa de A. Marcelino

    Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3291-7222
  2. Owen Gray

    Division of Imaging Science and Technology, University of Dundee, Dundee, United Kingdom
    Competing interests
    No competing interests declared.
  3. Bassam Al-Fatly

    Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0067-6177
  4. William Gilmour

    Division of Imaging Science and Technology, University of Dundee, Dundee, United Kingdom
    Competing interests
    No competing interests declared.
  5. J Douglas Steele

    Division of Imaging Science and Technology, University of Dundee, Dundee, United Kingdom
    Competing interests
    No competing interests declared.
  6. Andrea A Kühn

    Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    Andrea A Kühn, has received from honoraria from Boston Scientific, Medtronic and Teva..
  7. Tom Gilbertson

    Division of Imaging Science and Technology, University of Dundee, Dundee, United Kingdom
    For correspondence
    tgilbertson@dundee.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9866-1565

Funding

Chief Scientist Office

  • Tom Gilbertson

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

Reviewing Editor

  1. Birte U Forstmann, University of Amsterdam, Netherlands

Ethics

Human subjects: The which was approved by the local ethics committee (Charité - Universitätsmedizin Berlin, EA1/179/20).

Version history

  1. Received: April 21, 2022
  2. Preprint posted: April 22, 2022 (view preprint)
  3. Accepted: February 1, 2023
  4. Accepted Manuscript published: February 2, 2023 (version 1)
  5. Version of Record published: February 20, 2023 (version 2)

Copyright

© 2023, de A. Marcelino 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. Ana Luisa de A. Marcelino
  2. Owen Gray
  3. Bassam Al-Fatly
  4. William Gilmour
  5. J Douglas Steele
  6. Andrea A Kühn
  7. Tom Gilbertson
(2023)
Pallidal neuromodulation of the explore/exploit trade-off in decision-making
eLife 12:e79642.
https://doi.org/10.7554/eLife.79642

Share this article

https://doi.org/10.7554/eLife.79642

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