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Developmental 'awakening' of primary motor cortex to the sensory consequences of movement

  1. James C Dooley  Is a corresponding author
  2. Mark S Blumberg
  1. University of Iowa, United States
Research Article
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Cite this article as: eLife 2018;7:e41841 doi: 10.7554/eLife.41841

Abstract

Before primary motor cortex (M1) develops its motor functions, it functions like a somatosensory area. Here, by recording from neurons in the forelimb representation of M1 in postnatal day (P) 8-12 rats, we demonstrate a rapid shift in its sensory responses. At P8-10, M1 neurons respond overwhelmingly to feedback from sleep-related twitches of the forelimb, but the same neurons do not respond to wake-related movements. By P12, M1 neurons suddenly respond to wake movements, a transition that results from opening the sensory gate in the external cuneate nucleus. Also at P12, fewer M1 neurons respond to individual twitches, but the full complement of twitch-related feedback observed at P8 is unmasked through local disinhibition. Finally, through P12, M1 sensory responses originate in the deep thalamorecipient layers, not primary somatosensory cortex. These findings demonstrate that M1 initially establishes a sensory framework upon which its later-emerging role in motor control is built.

Data availability

Data represented in all figures is summarized in the included tables. Because of the large amount of data in the present publication (over 1,000 neurons across over 50 animals, along with thousands of behaviorally scored twitches and wake movements) our raw data (neural firing timecodes and behavioral event timecodes) have been uploaded to Dryad at DOI: https://doi.org/10.5061/dryad.8231nj1. Custom MATLAB scripts for generating and fitting perievent histograms to twitch and wake movement models can be found on github (https://github.com/jcdooley/Dooley_and_Blumberg_2018).

The following data sets were generated
    1. Dooley J
    2. Blumberg M
    (2018) Data from: Developmental
    Dryad Digital Repository, doi:10.5061/dryad.8231nj1.

Article and author information

Author details

  1. James C Dooley

    Department of Psychological and Brain Sciences, University of Iowa, Iowa City, United States
    For correspondence
    james-c-dooley@uiowa.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9868-9840
  2. Mark S Blumberg

    Department of Psychological and Brain Sciences, University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6969-2955

Funding

National Institutes of Health (R37-HD081168)

  • Mark S Blumberg

National Institutes of Health (F32-NS101858)

  • James C Dooley

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 experiments were conducted in accordance with the National Institutes of Health (NIH) Guide for the Care and Use of Laboratory Animals (NIH Publication No. 80-23) and were approved by the Institutional Animal Care and Use Committee of the University of Iowa (protocol # 7011955).

Reviewing Editor

  1. John H Martin, CCNY/CUNY School of Medicine, United States

Publication history

  1. Received: September 9, 2018
  2. Accepted: December 19, 2018
  3. Accepted Manuscript published: December 21, 2018 (version 1)
  4. Version of Record published: January 4, 2019 (version 2)

Copyright

© 2018, Dooley & Blumberg

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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