Mechanisms that allow cortical preparatory activity without inappropriate movement

  1. Timothy R Darlington  Is a corresponding author
  2. Stephen G Lisberger
  1. Duke University School of Medicine, United States

Abstract

We reveal a novel mechanism that explains how preparatory activity can evolve in motor-related cortical areas without prematurely inducing movement. The smooth eye movement region of the frontal eye fields (FEFSEM) is a critical node in the neural circuit controlling smooth pursuit eye movement. Preparatory activity evolves in the monkey FEFSEM during fixation in parallel with an objective measure of visual-motor gain. We propose that the use of FEFSEM output as a gain signal rather than a movement command allows for preparation to progress in pursuit without causing movement. We also show that preparatory modulation of firing rate in FEFSEM predicts movement, providing evidence against the 'movement-null' space hypothesis as an explanation of how preparatory activity can progress without movement. Finally, there is a partial reorganization of FEFSEM population activity between preparation and movement that would allow for a directionally non-specific component of preparatory visual-motor gain enhancement in pursuit.

Data availability

Source data have been provided for each figure.

Article and author information

Author details

  1. Timothy R Darlington

    Department of Neurobiology, Duke University School of Medicine, Durham, United States
    For correspondence
    trd12@duke.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5534-7552
  2. Stephen G Lisberger

    Department of Neurobiology, Duke University School of Medicine, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7859-4361

Funding

National Institutes of Health (R01-EY027373)

  • Stephen G Lisberger

National Institutes of Health (F30-EY027684)

  • Timothy R Darlington

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

Ethics

Animal experimentation: All procedures received prior approval by Duke's Institutional Animal Care and Use Committee (protocol A085-18-04) and were in compliance with the National Institutes of Health's Guide for the Care and Use of Laboratory Animals.

Reviewing Editor

  1. Kunlin Wei, Peking University, China

Version history

  1. Received: August 8, 2019
  2. Accepted: February 20, 2020
  3. Accepted Manuscript published: February 21, 2020 (version 1)
  4. Version of Record published: March 6, 2020 (version 2)

Copyright

© 2020, Darlington & Lisberger

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. Timothy R Darlington
  2. Stephen G Lisberger
(2020)
Mechanisms that allow cortical preparatory activity without inappropriate movement
eLife 9:e50962.
https://doi.org/10.7554/eLife.50962

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https://doi.org/10.7554/eLife.50962

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