Distinct mechanisms mediate speed-accuracy adjustments in cortico-subthalamic networks

  1. Damian M Herz
  2. Huiling Tan
  3. John-Stuart Brittain
  4. Petra Fischer
  5. Binith Cheeran
  6. Alexander L Green
  7. James FitzGerald
  8. Tipu Z Aziz
  9. Keyoumars Ashkan
  10. Simon Little
  11. Thomas Foltynie
  12. Patricia Limousin
  13. Ludvic Zrinzo
  14. Rafal Bogacz
  15. Peter Brown  Is a corresponding author
  1. University of Oxford, United Kingdom
  2. Kings College London, United Kingdom
  3. University College London Institute of Neurology, United Kingdom

Abstract

Optimal decision-making requires balancing fast but error-prone and more accurate but slower decisions through adjustments of decision thresholds. Here, we demonstrate two distinct correlates of such speed-accuracy adjustments by recording subthalamic nucleus (STN) activity and electroencephalography in eleven Parkinson’s disease patients during a perceptual decision-making task; STN low-frequency oscillatory (LFO) activity (2-8 Hz), coupled to activity at prefrontal electrode Fz, and STN beta activity (13-30 Hz) coupled to electrodes C3/C4 close to motor cortex. These two correlates not only differed in their cortical topography and spectral characteristics, but also in the relative timing of recruitment and in their precise relationship with decision thresholds. Increases of STN LFO power preceding the response predicted increased thresholds only after accuracy instructions, while cue-induced reductions of STN beta power decreased thresholds irrespective of instructions. These findings indicate that distinct neural mechanisms determine whether a decision will be made in haste or with caution.

Data availability

The following data sets were generated
    1. Damian Herz
    (2017) Neural correlates of speed-accuracy adjustments in the subthalamic nucleus
    Publicly available at Oxford University Research Archive (uuid: 09bef38c-999f-4fb7-aa46-14eda3123571).

Article and author information

Author details

  1. Damian M Herz

    Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Huiling Tan

    Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8038-3029
  3. John-Stuart Brittain

    Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Petra Fischer

    Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5585-8977
  5. Binith Cheeran

    Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Alexander L Green

    Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. James FitzGerald

    Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Tipu Z Aziz

    Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Keyoumars Ashkan

    Department of Neurosurgery, Kings College Hospital, Kings College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. Simon Little

    Unit of Functional Neurosurgery, Sobell Department of Motor Neuroscience and Movement Disorders, University College London Institute of Neurology, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  11. Thomas Foltynie

    Unit of Functional Neurosurgery, Sobell Department of Motor Neuroscience and Movement Disorders, University College London Institute of Neurology, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  12. Patricia Limousin

    Unit of Functional Neurosurgery, Sobell Department of Motor Neuroscience and Movement Disorders, University College London Institute of Neurology, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  13. Ludvic Zrinzo

    Unit of Functional Neurosurgery, Sobell Department of Motor Neuroscience and Movement Disorders, University College London Institute of Neurology, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  14. Rafal Bogacz

    Medical Research Council Brain Network Dynamics Unit, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  15. Peter Brown

    Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom
    For correspondence
    peter.brown@ndcn.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5201-3044

Funding

Medical Research Council (MC_UU_12024/1)

  • Peter Brown

Horizon 2020 Framework Programme (655605)

  • Damian M Herz

Parkinson Appeal UK

  • Thomas Foltynie
  • Patricia Limousin
  • Ludvic Zrinzo

Monument Trust

  • Thomas Foltynie
  • Patricia Limousin
  • Ludvic Zrinzo

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

Ethics

Human subjects: In accordance with the declaration of Helsinki, participants gave written informed consent to participate in the study, which was approved by the local ethics committee (Oxfordshire REC A).

Reviewing Editor

  1. Peter Lakatos, NYU, United States

Publication history

  1. Received: September 13, 2016
  2. Accepted: January 15, 2017
  3. Accepted Manuscript published: January 31, 2017 (version 1)
  4. Version of Record published: February 1, 2017 (version 2)

Copyright

© 2017, Herz 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. Damian M Herz
  2. Huiling Tan
  3. John-Stuart Brittain
  4. Petra Fischer
  5. Binith Cheeran
  6. Alexander L Green
  7. James FitzGerald
  8. Tipu Z Aziz
  9. Keyoumars Ashkan
  10. Simon Little
  11. Thomas Foltynie
  12. Patricia Limousin
  13. Ludvic Zrinzo
  14. Rafal Bogacz
  15. Peter Brown
(2017)
Distinct mechanisms mediate speed-accuracy adjustments in cortico-subthalamic networks
eLife 6:e21481.
https://doi.org/10.7554/eLife.21481
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