Independent representations of ipsilateral and contralateral limbs in primary motor cortex

Abstract

Several lines of research demonstrate that primary motor cortex (M1) is principally involved in controlling the contralateral side of the body. However, M1 activity has been correlated with both contralateral and ipsilateral limb movements. Why does ipsilaterally-related activity not cause contralateral motor output? To address this question, we trained monkeys to counter mechanical loads applied to their right and left limbs. We found >50% of M1 neurons had load-related activity for both limbs. Contralateral loads evoked changes in activity ~10ms sooner than ipsilateral loads. We also found corresponding population activities were distinct, with contralateral activity residing in a subspace that was orthogonal to the ipsilateral activity. Thus, neural responses for the contralateral limb can be extracted without interference from the activity for the ipsilateral limb, and vice versa. Our results show that M1 activity unrelated to downstream motor targets can be segregated from activity related to the downstream motor output.

Data availability

Neural and kinematic data have been submitted to the Dryad repository and can be accessed at https://dx.doi.org/10.5061/dryad.06nr12f

The following data sets were generated

Article and author information

Author details

  1. Ethan A Heming

    Centre for Neuroscience Studies, Queen's University, Kingston, Canada
    Competing interests
    No competing interests declared.
  2. Kevin P Cross

    Centre for Neuroscience Studies, Queen's University, Kingston, Canada
    For correspondence
    13kc18@queensu.ca
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9820-1043
  3. Tomohiko Takei

    Centre for Neuroscience Studies, Queen's University, Kingston, Canada
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6429-5798
  4. Douglas J Cook

    Centre for Neuroscience Studies, Queen's University, Kingston, Canada
    Competing interests
    No competing interests declared.
  5. Stephen H Scott

    Centre for Neuroscience Studies, Queen's University, Kingston, Canada
    Competing interests
    Stephen H Scott, Co-founder and chief scientific officer of Kinarm which commercializes the robot used in the study.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8821-1843

Funding

Canadian Institutes of Health Research (CIHR MOP 84403)

  • Stephen H Scott

Canadian Institutes of Health Research (CIHR PJT 153445)

  • Stephen H Scott

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

Reviewing Editor

  1. Jörn Diedrichsen, University of Western Ontario, Canada

Ethics

Animal experimentation: Studies were approved by the Queen's University Research Ethics Board and Animal Care Committee (#Scott-2010-035).

Version history

  1. Received: May 3, 2019
  2. Accepted: October 17, 2019
  3. Accepted Manuscript published: October 18, 2019 (version 1)
  4. Version of Record published: November 1, 2019 (version 2)

Copyright

© 2019, Heming 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.

Metrics

  • 4,244
    Page views
  • 352
    Downloads
  • 28
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Ethan A Heming
  2. Kevin P Cross
  3. Tomohiko Takei
  4. Douglas J Cook
  5. Stephen H Scott
(2019)
Independent representations of ipsilateral and contralateral limbs in primary motor cortex
eLife 8:e48190.
https://doi.org/10.7554/eLife.48190

Share this article

https://doi.org/10.7554/eLife.48190

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.