Non-selective inhibition of inappropriate motor-tendencies during response-conflict by a fronto-subthalamic mechanism

  1. Jan R Wessel  Is a corresponding author
  2. Darcy A Waller
  3. Jeremy DW Greenlee
  1. University of Iowa Hospitals and Clinics, United States
  2. University of Iowa, United States

Abstract

To effectively interact with their environment, humans must often select actions from multiple incompatible options. Existing theories propose that during motoric response-conflict, inappropriate motor activity is actively (and perhaps non-selectively) suppressed by an inhibitory fronto-basal ganglia mechanism. We here tested this theory across three experiments. First, using scalp-EEG, we found that both outright action-stopping and response-conflict during action-selection invoke low-frequency activity of a common fronto-central source, whose activity relates to trial-by-trial behavioral indices of inhibition in both tasks. Second, using simultaneous intracranial recordings from the basal ganglia and motor cortex, we found that response-conflict increases the influence of the subthalamic nucleus on M1-representations of incorrect response-tendencies. Finally, using transcranial magnetic stimulation, we found that during the same time period when conflict-related STN-to-M1 communication is increased, cortico-spinal excitability is broadly suppressed. Together, these findings demonstrate that fronto-BG networks buttress action-selection under response-conflict by rapidly and non-selectively net-inhibiting inappropriate motor tendencies.

Data availability

The experimental code, data, and analysis routines underlying this research can be found on the Open Science Framework at the following URL: https://osf.io/k3ypt/.

The following data sets were generated

Article and author information

Author details

  1. Jan R Wessel

    Department of Neurology, University of Iowa Hospitals and Clinics, Iowa City, United States
    For correspondence
    jan-wessel@uiowa.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7298-6601
  2. Darcy A Waller

    Department of Psychological and Brain Sciences, University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jeremy DW Greenlee

    Department of Neurosurgery, University of Iowa Hospitals and Clinics, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institute of Neurological Disorders and Stroke (R01 NS102201)

  • Jan R Wessel

National Science Foundation (CAREER 1752355)

  • Jan R Wessel

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

Ethics

Human subjects: Informed consent was collected from all subjects and all procedures were approved by the local ethics committee at the University of Iowa (IRB #201511709, IRB # 201402720, IRB #201612707).

Reviewing Editor

  1. Timothy Verstynen, Carnegie Mellon University, United States

Publication history

  1. Received: October 18, 2018
  2. Accepted: May 6, 2019
  3. Accepted Manuscript published: May 7, 2019 (version 1)
  4. Version of Record published: May 23, 2019 (version 2)

Copyright

© 2019, Wessel 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. Jan R Wessel
  2. Darcy A Waller
  3. Jeremy DW Greenlee
(2019)
Non-selective inhibition of inappropriate motor-tendencies during response-conflict by a fronto-subthalamic mechanism
eLife 8:e42959.
https://doi.org/10.7554/eLife.42959
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