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.

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  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

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    Probing memory of a complex visual image within a few hundred milliseconds after its disappearance reveals significantly greater fidelity of recall than if the probe is delayed by as little as a second. Classically interpreted, the former taps into a detailed but rapidly decaying visual sensory or ‘iconic’ memory (IM), while the latter relies on capacity-limited but comparatively stable visual working memory (VWM). While iconic decay and VWM capacity have been extensively studied independently, currently no single framework quantitatively accounts for the dynamics of memory fidelity over these time scales. Here, we extend a stationary neural population model of VWM with a temporal dimension, incorporating rapid sensory-driven accumulation of activity encoding each visual feature in memory, and a slower accumulation of internal error that causes memorized features to randomly drift over time. Instead of facilitating read-out from an independent sensory store, an early cue benefits recall by lifting the effective limit on VWM signal strength imposed when multiple items compete for representation, allowing memory for the cued item to be supplemented with information from the decaying sensory trace. Empirical measurements of human recall dynamics validate these predictions while excluding alternative model architectures. A key conclusion is that differences in capacity classically thought to distinguish IM and VWM are in fact contingent upon a single resource-limited WM store.