Motor actions are spatially organized in motor and dorsal premotor cortex

  1. Nicholas G Chehade
  2. Omar A Gharbawie  Is a corresponding author
  1. University of Pittsburgh, United States

Abstract

Frontal motor areas are central to controlling voluntary movements. In non-human primates, the motor areas contain independent, somatotopic, representations of the forelimb (i.e., motor maps). But are the neural codes for actions spatially organized within those forelimb representations? Addressing this question would provide insight into the poorly understood structure-function relationships of the cortical motor system. Here, we tackle the problem using high resolution optical imaging and motor mapping in motor (M1) and dorsal premotor (PMd) cortex. Two macaque monkeys performed an instructed reach-to-grasp task while cortical activity was recorded with intrinsic signal optical imaging (ISOI). The spatial extent of activity in M1 and PMd was then quantified in relation to the forelimb motor maps, which we obtained from the same hemisphere with intracortical microstimulation. ISOI showed that task-related activity was concentrated in patches that collectively overlapped <40% of the M1 and PMd forelimb representations. The spatial organization of the patches was consistent across task conditions despite small variations in forelimb use. Nevertheless, the largest condition differences in forelimb use were reflected in the magnitude of cortical activity. Distinct time course profiles from patches in arm zones and patches in hand zones suggest functional differences within the forelimb representations. The results collectively support an organizational framework wherein the forelimb representations contain subzones enriched with neurons tuned for specific actions. Thus, the often-overlooked spatial dimension of neural activity appears to be an important organizing feature of the neural code in frontal motor areas.

Data availability

All data and code used in this paper is posted on OSF.DOI: 10.17605/OSF.IO/7SGBEhttps://osf.io/7sgbe/

The following data sets were generated

Article and author information

Author details

  1. Nicholas G Chehade

    Department of Neurobiology, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Omar A Gharbawie

    Department of Neurobiology, University of Pittsburgh, Pittsburgh, United States
    For correspondence
    omar@pitt.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2744-9305

Funding

National Institutes of Health (R01 NS105697)

  • Omar A Gharbawie

Whitehall Foundation (2017-12-94)

  • Omar A Gharbawie

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 approved by the University of Pittsburgh Animal Care and Use Committees (protocol #21049001) and followed the guidelines of the National Institutes of Health guide for the care and use of laboratory animals.

Copyright

© 2023, Chehade & Gharbawie

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

  • 1,084
    views
  • 189
    downloads
  • 4
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Nicholas G Chehade
  2. Omar A Gharbawie
(2023)
Motor actions are spatially organized in motor and dorsal premotor cortex
eLife 12:e83196.
https://doi.org/10.7554/eLife.83196

Share this article

https://doi.org/10.7554/eLife.83196

Further reading

    1. Neuroscience
    Yiheng Zhang, Yun Chen ... He Cui
    Research Article

    Although recent studies suggest that activity in the motor cortex, in addition to generating motor outputs, receives substantial information regarding sensory inputs, it is still unclear how sensory context adjusts the motor commands. Here, we recorded population neural activity in the motor cortex via microelectrode arrays while monkeys performed flexible manual interceptions of moving targets. During this task, which requires predictive sensorimotor control, the activity of most neurons in the motor cortex encoding upcoming movements was influenced by ongoing target motion. Single-trial neural states at the movement onset formed staggered orbital geometries, suggesting that target motion modulates peri-movement activity in an orthogonal manner. This neural geometry was further evaluated with a representational model and recurrent neural networks (RNNs) with task-specific input-output mapping. We propose that the sensorimotor dynamics can be derived from neuronal mixed sensorimotor selectivity and dynamic interaction between modulations.

    1. Genetics and Genomics
    2. Neuroscience
    Martina Rudgalvyte, Zehan Hu ... Dominique A Glauser
    Research Article

    Thermal nociception in Caenorhabditis elegans is regulated by the Ca²+/calmodulin-dependent protein kinase CMK-1, but its downstream effectors have remained unclear. Here, we combined in vitro kinase assays with mass-spectrometry-based phosphoproteomics to identify hundreds of CMK-1 substrates, including the calcineurin A subunit TAX-6, phosphorylated within its conserved regulatory domain. Genetic and pharmacological analyses reveal multiple antagonistic interactions between CMK-1 and calcineurin signaling in modulating both naive thermal responsiveness and adaptation to repeated noxious stimuli. Cell-specific manipulations indicate that CMK-1 acts in AFD and ASER thermo-sensory neurons, while TAX-6 functions in FLP thermo-sensory neurons and downstream interneurons. Since CMK-1 and TAX-6 act in distinct cell types, the phosphorylation observed in vitro might not directly underlie the behavioral phenotype. Instead, the opposing effects seem to arise from their distributed roles within the sensory circuit. Overall, our study provides (1) a resource of candidate CMK-1 targets for further dissecting CaM kinase signaling and (2) evidence of a previously unrecognized, circuit-level antagonism between CMK-1 and calcineurin pathways. These findings highlight a complex interplay of signaling modules that modulate thermal nociception and adaptation, offering new insights into potentially conserved mechanisms that shape nociceptive plasticity and pain (de)sensitization in more complex nervous systems.