Altered basal ganglia output during self-restraint

  1. Bon-Mi Gu  Is a corresponding author
  2. Joshua D Berke
  1. Stanford University, United States
  2. University of California, San Francisco, United States

Abstract

Suppressing actions is essential for flexible behavior. Multiple neural circuits involved in behavioral inhibition converge upon a key basal ganglia output nucleus, the substantia nigra pars reticulata (SNr). To examine how changes in basal ganglia output contribute to self-restraint, we recorded SNr neurons during a proactive behavioral inhibition task. Rats responded to Go! cues with rapid leftward or rightward movements, but also prepared to cancel one of these movement directions on trials when a Stop! cue might occur. This action restraint - visible as direction-selective slowing of reaction times - altered both rates and patterns of SNr spiking. Overall firing rate was elevated before the Go! cue, and this effect was driven by a subpopulation of direction-selective SNr neurons. In neural state space, this corresponded to a shift away from the restrained movement. SNr neurons also showed more variable inter-spike-intervals during proactive inhibition. This corresponded to more variable state-space trajectories, which may slow reaction times via reduced preparation to move. These findings open new perspectives on how basal ganglia dynamics contribute to movement preparation and cognitive control.

Data availability

Electrophysiology data with behaviors and the codes used for the analysis will be available at figshare (https://figshare.com/, DOI:10.6084/m9.figshare.20409858).

The following data sets were generated

Article and author information

Author details

  1. Bon-Mi Gu

    Department of Neurology and Neurological Sciences, Stanford University, Stanford, United States
    For correspondence
    bonmigu@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3060-0803
  2. Joshua D Berke

    Department of Neurology, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1436-6823

Funding

National Institute of Mental Health (R01MH101697)

  • Joshua D Berke

National Institute of Neurological Disorders and Stroke (R01NS123516)

  • Joshua D Berke

CHDI Foundation (A-13733)

  • Joshua D Berke

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

Reviewing Editor

  1. Aryn H Gittis, Carnegie Mellon University, United States

Ethics

Animal experimentation: All animal experiments were approved by the University of California, San Francisco Committee for the Use and Care of Animals (#AN181071).

Version history

  1. Preprint posted: April 25, 2022 (view preprint)
  2. Received: July 25, 2022
  3. Accepted: October 31, 2022
  4. Accepted Manuscript published: November 2, 2022 (version 1)
  5. Version of Record published: November 15, 2022 (version 2)

Copyright

© 2022, Gu & Berke

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. Bon-Mi Gu
  2. Joshua D Berke
(2022)
Altered basal ganglia output during self-restraint
eLife 11:e82143.
https://doi.org/10.7554/eLife.82143

Share this article

https://doi.org/10.7554/eLife.82143

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