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New Research, Sensory and Motor Systems

The representation of finger movement and force in human motor and premotor cortices

Robert D. Flint, Matthew C. Tate, Kejun Li, Jessica W. Templer, Joshua M. Rosenow, Chethan Pandarinath and Marc W. Slutzky
eNeuro 7 August 2020, ENEURO.0063-20.2020; DOI: https://doi.org/10.1523/ENEURO.0063-20.2020
Robert D. Flint
1Department of Neurology, Northwestern University, Chicago IL 60611, USA
2Shirley Ryan AbilityLab, Northwestern University, Chicago IL 60611, USA
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  • ORCID record for Robert D. Flint
Matthew C. Tate
1Department of Neurology, Northwestern University, Chicago IL 60611, USA
3Department of Neurological Surgery, Northwestern University, Chicago IL 60611, USA
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Kejun Li
4Computation and Neural Systems Program, California Institute of Technology, Pasadena, California 91125, USA
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Jessica W. Templer
1Department of Neurology, Northwestern University, Chicago IL 60611, USA
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Joshua M. Rosenow
1Department of Neurology, Northwestern University, Chicago IL 60611, USA
3Department of Neurological Surgery, Northwestern University, Chicago IL 60611, USA
5Department of Physical Medicine & Rehabilitation, Northwestern University, Chicago IL 60611, USA
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Chethan Pandarinath
6Department of Biomedical Engineering, Emory University and Georgia Institute of Technology, Atlanta GA 30322, USA
7Department of Neurosurgery, Emory University, Atlanta GA 30322, USA
8Emory Neuromodulation and Technology Innovation Center (ENTICe), Emory University, Atlanta GA 30322, USA
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Marc W. Slutzky
1Department of Neurology, Northwestern University, Chicago IL 60611, USA
2Shirley Ryan AbilityLab, Northwestern University, Chicago IL 60611, USA
5Department of Physical Medicine & Rehabilitation, Northwestern University, Chicago IL 60611, USA
9Department of Physiology, Northwestern University, Chicago IL 60611, USA
10Department of Biomedical Engineering, Northwestern University, Chicago IL 60611, USA
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Abstract

The ability to grasp and manipulate objects requires controlling both finger movement kinematics and isometric force in rapid succession. Previous work suggests that these behavioral modes are controlled separately, but it is unknown whether the cerebral cortex represents them differently. Here, we asked the question of how movement and force were represented cortically, when executed sequentially with the same finger. We recorded high-density electrocorticography (ECoG) from the motor and premotor cortices of seven human subjects performing a movement-force motor task. We decoded finger movement (0.7±0.3 fractional variance accounted for; FVAF) and force (0.7±0.2 FVAF) with high accuracy, yet found different spatial representations. In addition, we used a state-of-the-art deep learning method to uncover smooth, repeatable trajectories through ECoG state space during the movement-force task. We also summarized ECoG across trials and participants by developing a new metric, the neural vector angle. Thus, state-space techniques can help to investigate broad cortical networks. Finally, we were able to classify the behavioral mode from neural signals with high accuracy (90±6%). Thus, finger movement and force appear to have distinct representations in motor/premotor cortices. These results inform our understanding of the neural control of movement, as well as the design of grasp brain-machine interfaces.

Significance Statement The human ability to manipulate objects is central to our daily lives and requires control of both grasping movement and force. Here, we explored how these motor activities are represented at the level of the cortex. Understanding these representations will influence the design of brain-machine interfaces (BMIs) to restore function after paralysis. We recorded electrocorticography (ECoG) from seven human subjects who performed a sequential movement-force motor task. We found differences between the cortical representations of movement and force using decoding methods, deep learning, and a new neural ensemble metric. Thus, ECoG could be used in a BMI to control both movement and force behaviors. These results can potentially accelerate the translation of BMIs for individuals with paralysis.

  • Cortex
  • Electrocorticography
  • Grasp
  • Human
  • Kinematic
  • Kinetic

Footnotes

  • Authors report no conflict of interest

  • Craig H. Neilsen Foundation [fellowship]; Emory College Computational Neuroscience [training grant]; Burroughs Wellcome Fund (BWF); Collaborative Research Travel Grant; National Science Foundation (NSF); NCS 1835364; Emory Neuromodulation Technology Innovation Center; Doris Duke Charitable Foundation (DDCF) [Clinical Scientist Development Award]; Northwestern Memorial Foundation Dixon Translational Research Grant [NIH UL1RR025741]; HHS | National Institutes of Health (NIH) [R01NS094748]

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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The representation of finger movement and force in human motor and premotor cortices
Robert D. Flint, Matthew C. Tate, Kejun Li, Jessica W. Templer, Joshua M. Rosenow, Chethan Pandarinath, Marc W. Slutzky
eNeuro 7 August 2020, ENEURO.0063-20.2020; DOI: 10.1523/ENEURO.0063-20.2020

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The representation of finger movement and force in human motor and premotor cortices
Robert D. Flint, Matthew C. Tate, Kejun Li, Jessica W. Templer, Joshua M. Rosenow, Chethan Pandarinath, Marc W. Slutzky
eNeuro 7 August 2020, ENEURO.0063-20.2020; DOI: 10.1523/ENEURO.0063-20.2020
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Keywords

  • cortex
  • electrocorticography
  • grasp
  • human
  • kinematic
  • kinetic

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