Conservation of preparatory neural events in monkey motor cortex regardless of how movement is initiated

  1. Antonio Homero Lara
  2. Gamaleldin F Elsayed
  3. Andrew J Zimnik
  4. John Cunningham
  5. Mark M Churchland  Is a corresponding author
  1. Columbia University Medical Center, United States
  2. Columbia University, United States

Abstract

A time-consuming preparatory stage is hypothesized to precede voluntary movement. A putative neural substrate of motor preparation occurs when a delay separates instruction and execution cues. When readiness is sustained during the delay, sustained neural activity is observed in motor and premotor areas. Yet whether delay-period activity reflects an essential preparatory stage is controversial. In particular, it has remained ambiguous whether delay-period-like activity appears before non-delayed movements. To overcome that ambiguity, we leveraged a recently developed analysis method that parses population responses into putatively preparatory and movement-related components. We examined cortical responses when reaches were initiated after an imposed delay, at a self-chosen time, or reactively with low latency and no delay. Putatively preparatory events were conserved across all contexts. Our findings support the hypothesis that an appropriate 'preparatory state' is consistently achieved before movement onset. However, our results reveal that this process can consume surprisingly little time.

Data availability

The data supporting this work is available via Dryad (http://dx.doi.org/10.5061/dryad.cf66jb7).

The following data sets were generated

Article and author information

Author details

  1. Antonio Homero Lara

    Department of Neuroscience, Columbia University Medical Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Gamaleldin F Elsayed

    Department of Neuroscience, Columbia University Medical Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Andrew J Zimnik

    Department of Neuroscience, Columbia University Medical Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. John Cunningham

    Center for Theoretical Neuroscience, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Mark M Churchland

    Department of Neuroscience, Columbia University Medical Center, New York, United States
    For correspondence
    mc3502@columbia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9123-6526

Funding

Alfred P. Sloan Foundation

  • Mark M Churchland

Kavli Foundation

  • Mark M Churchland

Klingenstein Third Generation Foundation

  • Mark M Churchland

Kinship Foundation

  • Mark M Churchland

National Institute of Neurological Disorders and Stroke (NS092350)

  • Antonio Homero Lara

Gatsby Charitable Foundation

  • John Cunningham
  • Mark M Churchland

Simons Foundation (SCGB#325171)

  • John Cunningham
  • Mark M Churchland

Simons Foundation (SCGB#325233)

  • John Cunningham
  • Mark M Churchland

Grossman Center for the Statistics of Mind

  • John Cunningham
  • Mark M Churchland

McKnight Endowment Fund for Neuroscience

  • John Cunningham
  • Mark M Churchland

National Institute of Neurological Disorders and Stroke (DP2 NS083037)

  • Mark M Churchland

National Institute of Neurological Disorders and Stroke (R01NS100066)

  • John Cunningham
  • Mark M Churchland

National Institute of Neurological Disorders and Stroke (NS104649)

  • John Cunningham
  • Mark M Churchland

National Eye Institute (P30 EY-019007)

  • Mark M Churchland

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 were in accord with the US National Institutes of Health guidelines and were approved by the Columbia University Institutional Animal Care and Use Committee (AC-AAAQ7409).

Reviewing Editor

  1. Jennifer L Raymond, Stanford School of Medicine, United States

Publication history

  1. Received: September 8, 2017
  2. Accepted: July 26, 2018
  3. Accepted Manuscript published: August 22, 2018 (version 1)
  4. Version of Record published: August 28, 2018 (version 2)

Copyright

© 2018, Lara 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. Antonio Homero Lara
  2. Gamaleldin F Elsayed
  3. Andrew J Zimnik
  4. John Cunningham
  5. Mark M Churchland
(2018)
Conservation of preparatory neural events in monkey motor cortex regardless of how movement is initiated
eLife 7:e31826.
https://doi.org/10.7554/eLife.31826

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