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A synergy-based hand control is encoded in human motor cortical areas

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Cite this article as: eLife 2016;5:e13420 doi: 10.7554/eLife.13420

Abstract

How the human brain controls hand movements to carry out different tasks is still debated. The concept of synergy has been proposed to indicate functional modules that may simplify the control of hand postures by simultaneously recruiting sets of muscles and joints. However, whether and to what extent synergic hand postures are encoded as such at a cortical level remains unknown. Here, we combined kinematic, electromyography, and brain activity measures obtained by functional magnetic resonance imaging while subjects performed a variety of movements towards virtual objects. Hand postural information, encoded through kinematic synergies, were represented in cortical areas devoted to hand motor control and successfully discriminated individual grasping movements, significantly outperforming alternative somatotopic or muscle-based models. Importantly, hand postural synergies were predicted by neural activation patterns within primary motor cortex. These findings support a novel cortical organization for hand movement control and open potential applications for brain-computer interfaces and neuroprostheses.

Article and author information

Author details

  1. Andrea Leo

    Laboratory of Clinical Biochemistry and Molecular Biology, University of Pisa, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
  2. Giacomo Handjaras

    Laboratory of Clinical Biochemistry and Molecular Biology, University of Pisa, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
  3. Matteo Bianchi

    Research Center 'E. Piaggio', University of Pisa, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
  4. Hamal Marino

    Research Center 'E. Piaggio', University of Pisa, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
  5. Marco Gabiccini

    Research Center 'E. Piaggio', University of Pisa, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
  6. Andrea Guidi

    Research Center 'E. Piaggio', University of Pisa, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
  7. Enzo Pasquale Scilingo

    Research Center 'E. Piaggio', University of Pisa, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
  8. Pietro Pietrini

    Laboratory of Clinical Biochemistry and Molecular Biology, University of Pisa, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
  9. Antonio Bicchi

    Research Center 'E. Piaggio', University of Pisa, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
  10. Marco Santello

    School of Biological and Health Systems Engineering, Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Emiliano Ricciardi

    Laboratory of Clinical Biochemistry and Molecular Biology, University of Pisa, Pisa, Italy
    For correspondence
    emiliano.ricciardi@bioclinica.unipi.it
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Human subjects: This study was approved by the Ethical Committee at the University of Pisa, Italy. Participants received a detailed explanation of all the study procedures and risks and provided a written informed consent according to the protocol approved by the University of Pisa Ethical Committee (1616/2003). All participants retained the right to withdraw from the study at any moment.

Reviewing Editor

  1. Jody C Culham, University of Western Ontario, Canada

Publication history

  1. Received: December 9, 2015
  2. Accepted: February 13, 2016
  3. Accepted Manuscript published: February 15, 2016 (version 1)
  4. Version of Record published: February 29, 2016 (version 2)

Copyright

© 2016, Leo 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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