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      The Representation of Finger Movement and Force in Human Motor and Premotor Cortices

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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 (NVA). 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 (BMIs).

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          Most cited references46

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          BCI2000: a general-purpose brain-computer interface (BCI) system.

          Many laboratories have begun to develop brain-computer interface (BCI) systems that provide communication and control capabilities to people with severe motor disabilities. Further progress and realization of practical applications depends on systematic evaluations and comparisons of different brain signals, recording methods, processing algorithms, output formats, and operating protocols. However, the typical BCI system is designed specifically for one particular BCI method and is, therefore, not suited to the systematic studies that are essential for continued progress. In response to this problem, we have developed a documented general-purpose BCI research and development platform called BCI2000. BCI2000 can incorporate alone or in combination any brain signals, signal processing methods, output devices, and operating protocols. This report is intended to describe to investigators, biomedical engineers, and computer scientists the concepts that the BC12000 system is based upon and gives examples of successful BCI implementations using this system. To date, we have used BCI2000 to create BCI systems for a variety of brain signals, processing methods, and applications. The data show that these systems function well in online operation and that BCI2000 satisfies the stringent real-time requirements of BCI systems. By substantially reducing labor and cost, BCI2000 facilitates the implementation of different BCI systems and other psychophysiological experiments. It is available with full documentation and free of charge for research or educational purposes and is currently being used in a variety of studies by many research groups.
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            Neural population dynamics during reaching

            Most theories of motor cortex have assumed that neural activity represents movement parameters. This view derives from an analogous approach to primary visual cortex, where neural activity represents patterns of light. Yet it is unclear how well that analogy holds. Single-neuron responses in motor cortex appear strikingly complex, and there is marked disagreement regarding which movement parameters are represented. A better analogy might be with other motor systems, where a common principle is rhythmic neural activity. We found that motor cortex responses during reaching contain a brief but strong oscillatory component, something quite unexpected for a non-periodic behavior. Oscillation amplitude and phase followed naturally from the preparatory state, suggesting a mechanistic role for preparatory neural activity. These results demonstrate unexpected yet surprisingly simple structure in the population response. That underlying structure explains many of the confusing features of individual-neuron responses.
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              Restoring cortical control of functional movement in a human with quadriplegia.

              Millions of people worldwide suffer from diseases that lead to paralysis through disruption of signal pathways between the brain and the muscles. Neuroprosthetic devices are designed to restore lost function and could be used to form an electronic 'neural bypass' to circumvent disconnected pathways in the nervous system. It has previously been shown that intracortically recorded signals can be decoded to extract information related to motion, allowing non-human primates and paralysed humans to control computers and robotic arms through imagined movements. In non-human primates, these types of signal have also been used to drive activation of chemically paralysed arm muscles. Here we show that intracortically recorded signals can be linked in real-time to muscle activation to restore movement in a paralysed human. We used a chronically implanted intracortical microelectrode array to record multiunit activity from the motor cortex in a study participant with quadriplegia from cervical spinal cord injury. We applied machine-learning algorithms to decode the neuronal activity and control activation of the participant's forearm muscles through a custom-built high-resolution neuromuscular electrical stimulation system. The system provided isolated finger movements and the participant achieved continuous cortical control of six different wrist and hand motions. Furthermore, he was able to use the system to complete functional tasks relevant to daily living. Clinical assessment showed that, when using the system, his motor impairment improved from the fifth to the sixth cervical (C5-C6) to the seventh cervical to first thoracic (C7-T1) level unilaterally, conferring on him the critical abilities to grasp, manipulate, and release objects. This is the first demonstration to our knowledge of successful control of muscle activation using intracortically recorded signals in a paralysed human. These results have significant implications in advancing neuroprosthetic technology for people worldwide living with the effects of paralysis.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                3 August 2020
                14 August 2020
                Jul-Aug 2020
                : 7
                : 4
                : ENEURO.0063-20.2020
                Affiliations
                [1 ]Department of Neurology, Northwestern University , Chicago, IL 60611
                [2 ]Shirley Ryan AbilityLab, Chicago, IL 60611
                [3 ]Department of Neurological Surgery, Northwestern University , Chicago, IL 60611
                [4 ]Computation and Neural Systems Program, California Institute of Technology , Pasadena, CA 91125
                [5 ]Department of Physical Medicine and Rehabilitation, Northwestern University , Chicago, IL 60611
                [6 ]Department of Biomedical Engineering, Emory University and Georgia Institute of Technology , Atlanta, GA 30322
                [7 ]Department of Neurosurgery, Emory University , Atlanta, GA 30322
                [8 ]Emory Neuromodulation and Technology Innovation Center (ENTICe), Emory University , Atlanta, GA 30322
                [9 ]Department of Physiology, Northwestern University , Chicago, IL 60611
                [10 ]Department of Biomedical Engineering, Northwestern University , Chicago, IL 60611
                Author notes

                The authors declare no competing financial interests.

                Author contributions: R.D.F. and M.W.S. designed research; R.D.F., M.C.T., J.W.T., J.M.R., and M.W.S. performed research; R.D.F., K.L., C.P., and M.W.S. analyzed data; R.D.F., K.L., C.P., and M.W.S. wrote the paper.

                This work was supported by the Craig H. Neilsen Foundation Fellowship (R.D.F.); an Emory College Computational Neuroscience training grant (K.L.); Burroughs Wellcome Fund Collaborative Research Travel Grant (C.P.); the National Science Foundation Grant NCS 1835364 (to C.P.); the Emory Neuromodulation Technology Innovation Center (C.P.); the Doris Duke Charitable Foundation Clinical Scientist Development Award (M.W.S.); The Northwestern Memorial Foundation Dixon Translational Research Grant Program, supported in part by National Institutes of Health (NIH) Grant UL1RR025741 (to M.W.S.); the Department of Health and Human Services NIH Grant R01NS094748 (to M.W.S.).

                Correspondence should be addressed to Robert D. Flint at r-flint@ 123456northwestern.edu .
                Author information
                https://orcid.org/0000-0002-0281-5778
                https://orcid.org/0000-0003-2269-7729
                Article
                eN-NWR-0063-20
                10.1523/ENEURO.0063-20.2020
                7438059
                32769159
                04eb92e1-3366-42d6-8a2d-d187b3b7beb0
                Copyright © 2020 Flint et al.

                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.

                History
                : 19 February 2020
                : 6 May 2020
                : 21 May 2020
                Page count
                Figures: 6, Tables: 2, Equations: 15, References: 50, Pages: 15, Words: 00
                Funding
                Funded by: http://doi.org/10.13039/100005191Craig H. Neilsen Foundation
                Award ID: fellowship
                Funded by: Emory College Computational Neuroscience
                Award ID: training grant
                Funded by: http://doi.org/10.13039/100000861Burroughs Wellcome Fund (BWF)
                Award ID: Collaborative Research Travel Grant
                Funded by: http://doi.org/10.13039/100000001National Science Foundation (NSF)
                Award ID: NCS 1835364
                Funded by: Emory Neuromodulation Technology Innovation Center
                Funded by: http://doi.org/10.13039/100000862Doris Duke Charitable Foundation (DDCF)
                Award ID: Clinical Scientist Development Award
                Funded by: Northwestern Memorial Foundation Dixon Translational Research Grant
                Award ID: NIH UL1RR025741
                Funded by: http://doi.org/10.13039/100000002HHS | National Institutes of Health (NIH)
                Award ID: R01NS094748
                Categories
                8
                Research Article: New Research
                Sensory and Motor Systems
                Custom metadata
                July/August 2020

                cortex,electrocorticography,grasp,human,kinematic,kinetic
                cortex, electrocorticography, grasp, human, kinematic, kinetic

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