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Cortex commands the performance of skilled movement

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Cite this article as: eLife 2015;4:e10774 doi: 10.7554/eLife.10774

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.

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.

Reviewing Editor

  1. Michael Hausser, University College London, United Kingdom

Publication 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.

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Further reading

    1. Neuroscience
    Maude Bouchard et al.
    Research Article Updated

    Sleep slow waves are studied for their role in brain plasticity, homeostatic regulation, and their changes during aging. Here, we address the possibility that two types of slow waves co-exist in humans. Thirty young and 29 older adults underwent a night of polysomnographic recordings. Using the transition frequency, slow waves with a slow transition (slow switchers) and those with a fast transition (fast switchers) were discovered. Slow switchers had a high electroencephalography (EEG) connectivity along their depolarization transition while fast switchers had a lower connectivity dynamics and dissipated faster during the night. Aging was associated with lower temporal dissipation of sleep pressure in slow and fast switchers and lower EEG connectivity at the microscale of the oscillations, suggesting a decreased flexibility in the connectivity network of older individuals. Our findings show that two different types of slow waves with possible distinct underlying functions coexist in the slow wave spectrum.