Abstract

Mammalian cerebral cortex is accepted as being critical for voluntary motor control, but what functions depend on cortex is still unclear. Here we used rapid, reversible optogenetic inhibition to test the role of cortex during a head-fixed task in which mice reach, grab, and eat a food pellet. Sudden cortical inhibition blocked initiation or froze execution of this skilled prehension behavior, but left untrained forelimb movements unaffected. Unexpectedly, kinematically normal prehension occurred immediately after cortical inhibition even during rest periods lacking cue and pellet. This 'rebound' prehension was only evoked in trained and food-deprived animals, suggesting that a motivation-gated motor engram sufficient to evoke prehension is activated at inhibition's end. These results demonstrate the necessity and sufficiency of cortical activity for enacting a learned skill.

Article and author information

Author details

  1. Jian-Zhong Guo

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Austin R Graves

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Wendy W Guo

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jihong Zheng

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Allen Lee

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Juan Rodríguez-González

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Nuo Li

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. John J Macklin

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. James W Phillips

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Brett D Mensh

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Kristin Branson

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Adam W Hantman

    Hantman Lab, Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    hantmana@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Michael Hausser, University College London, United Kingdom

Ethics

Animal experimentation: Animal procedures were performed in accordance with protocols (13-99) approved by the Institutional Animal Care and Use Committee (IACUC) of the Janelia Research Campus.

Version history

  1. Received: August 11, 2015
  2. Accepted: December 1, 2015
  3. Accepted Manuscript published: December 2, 2015 (version 1)
  4. Version of Record published: February 1, 2016 (version 2)
  5. Version of Record updated: June 16, 2016 (version 3)
  6. Version of Record updated: October 20, 2016 (version 4)

Copyright

© 2015, Guo 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

  • 13,821
    views
  • 2,321
    downloads
  • 189
    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. Jian-Zhong Guo
  2. Austin R Graves
  3. Wendy W Guo
  4. Jihong Zheng
  5. Allen Lee
  6. Juan Rodríguez-González
  7. Nuo Li
  8. John J Macklin
  9. James W Phillips
  10. Brett D Mensh
  11. Kristin Branson
  12. Adam W Hantman
(2015)
Cortex commands the performance of skilled movement
eLife 4:e10774.
https://doi.org/10.7554/eLife.10774

Share this article

https://doi.org/10.7554/eLife.10774

Further reading

    1. Genetics and Genomics
    2. Neuroscience
    Kenneth Chiou, Noah Snyder-Mackler
    Insight

    Single-cell RNA sequencing reveals the extent to which marmosets carry genetically distinct cells from their siblings.