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Neural Representation of Observed, Imagined, and Attempted Grasping Force in Motor Cortex of Individuals with Chronic Tetraplegia

Hybrid kinetic and kinematic intracortical brain-computer interfaces (iBCIs) have the potential to restore functional grasping and object interaction capabilities in individuals with tetraplegia. This requires an understanding of how kinetic information is represented in neural activity, and how thi...

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Autores principales: Rastogi, Anisha, Vargas-Irwin, Carlos E., Willett, Francis R., Abreu, Jessica, Crowder, Douglas C., Murphy, Brian A., Memberg, William D., Miller, Jonathan P., Sweet, Jennifer A., Walter, Benjamin L., Cash, Sydney S., Rezaii, Paymon G., Franco, Brian, Saab, Jad, Stavisky, Sergey D., Shenoy, Krishna V., Henderson, Jaimie M., Hochberg, Leigh R., Kirsch, Robert F., Ajiboye, A. Bolu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6989675/
https://www.ncbi.nlm.nih.gov/pubmed/31996696
http://dx.doi.org/10.1038/s41598-020-58097-1
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author Rastogi, Anisha
Vargas-Irwin, Carlos E.
Willett, Francis R.
Abreu, Jessica
Crowder, Douglas C.
Murphy, Brian A.
Memberg, William D.
Miller, Jonathan P.
Sweet, Jennifer A.
Walter, Benjamin L.
Cash, Sydney S.
Rezaii, Paymon G.
Franco, Brian
Saab, Jad
Stavisky, Sergey D.
Shenoy, Krishna V.
Henderson, Jaimie M.
Hochberg, Leigh R.
Kirsch, Robert F.
Ajiboye, A. Bolu
author_facet Rastogi, Anisha
Vargas-Irwin, Carlos E.
Willett, Francis R.
Abreu, Jessica
Crowder, Douglas C.
Murphy, Brian A.
Memberg, William D.
Miller, Jonathan P.
Sweet, Jennifer A.
Walter, Benjamin L.
Cash, Sydney S.
Rezaii, Paymon G.
Franco, Brian
Saab, Jad
Stavisky, Sergey D.
Shenoy, Krishna V.
Henderson, Jaimie M.
Hochberg, Leigh R.
Kirsch, Robert F.
Ajiboye, A. Bolu
author_sort Rastogi, Anisha
collection PubMed
description Hybrid kinetic and kinematic intracortical brain-computer interfaces (iBCIs) have the potential to restore functional grasping and object interaction capabilities in individuals with tetraplegia. This requires an understanding of how kinetic information is represented in neural activity, and how this representation is affected by non-motor parameters such as volitional state (VoS), namely, whether one observes, imagines, or attempts an action. To this end, this work investigates how motor cortical neural activity changes when three human participants with tetraplegia observe, imagine, and attempt to produce three discrete hand grasping forces with the dominant hand. We show that force representation follows the same VoS-related trends as previously shown for directional arm movements; namely, that attempted force production recruits more neural activity compared to observed or imagined force production. Additionally, VoS-modulated neural activity to a greater extent than grasping force. Neural representation of forces was lower than expected, possibly due to compromised somatosensory pathways in individuals with tetraplegia, which have been shown to influence motor cortical activity. Nevertheless, attempted forces (but not always observed or imagined forces) could be decoded significantly above chance, thereby potentially providing relevant information towards the development of a hybrid kinetic and kinematic iBCI.
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spelling pubmed-69896752020-02-05 Neural Representation of Observed, Imagined, and Attempted Grasping Force in Motor Cortex of Individuals with Chronic Tetraplegia Rastogi, Anisha Vargas-Irwin, Carlos E. Willett, Francis R. Abreu, Jessica Crowder, Douglas C. Murphy, Brian A. Memberg, William D. Miller, Jonathan P. Sweet, Jennifer A. Walter, Benjamin L. Cash, Sydney S. Rezaii, Paymon G. Franco, Brian Saab, Jad Stavisky, Sergey D. Shenoy, Krishna V. Henderson, Jaimie M. Hochberg, Leigh R. Kirsch, Robert F. Ajiboye, A. Bolu Sci Rep Article Hybrid kinetic and kinematic intracortical brain-computer interfaces (iBCIs) have the potential to restore functional grasping and object interaction capabilities in individuals with tetraplegia. This requires an understanding of how kinetic information is represented in neural activity, and how this representation is affected by non-motor parameters such as volitional state (VoS), namely, whether one observes, imagines, or attempts an action. To this end, this work investigates how motor cortical neural activity changes when three human participants with tetraplegia observe, imagine, and attempt to produce three discrete hand grasping forces with the dominant hand. We show that force representation follows the same VoS-related trends as previously shown for directional arm movements; namely, that attempted force production recruits more neural activity compared to observed or imagined force production. Additionally, VoS-modulated neural activity to a greater extent than grasping force. Neural representation of forces was lower than expected, possibly due to compromised somatosensory pathways in individuals with tetraplegia, which have been shown to influence motor cortical activity. Nevertheless, attempted forces (but not always observed or imagined forces) could be decoded significantly above chance, thereby potentially providing relevant information towards the development of a hybrid kinetic and kinematic iBCI. Nature Publishing Group UK 2020-01-29 /pmc/articles/PMC6989675/ /pubmed/31996696 http://dx.doi.org/10.1038/s41598-020-58097-1 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Rastogi, Anisha
Vargas-Irwin, Carlos E.
Willett, Francis R.
Abreu, Jessica
Crowder, Douglas C.
Murphy, Brian A.
Memberg, William D.
Miller, Jonathan P.
Sweet, Jennifer A.
Walter, Benjamin L.
Cash, Sydney S.
Rezaii, Paymon G.
Franco, Brian
Saab, Jad
Stavisky, Sergey D.
Shenoy, Krishna V.
Henderson, Jaimie M.
Hochberg, Leigh R.
Kirsch, Robert F.
Ajiboye, A. Bolu
Neural Representation of Observed, Imagined, and Attempted Grasping Force in Motor Cortex of Individuals with Chronic Tetraplegia
title Neural Representation of Observed, Imagined, and Attempted Grasping Force in Motor Cortex of Individuals with Chronic Tetraplegia
title_full Neural Representation of Observed, Imagined, and Attempted Grasping Force in Motor Cortex of Individuals with Chronic Tetraplegia
title_fullStr Neural Representation of Observed, Imagined, and Attempted Grasping Force in Motor Cortex of Individuals with Chronic Tetraplegia
title_full_unstemmed Neural Representation of Observed, Imagined, and Attempted Grasping Force in Motor Cortex of Individuals with Chronic Tetraplegia
title_short Neural Representation of Observed, Imagined, and Attempted Grasping Force in Motor Cortex of Individuals with Chronic Tetraplegia
title_sort neural representation of observed, imagined, and attempted grasping force in motor cortex of individuals with chronic tetraplegia
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6989675/
https://www.ncbi.nlm.nih.gov/pubmed/31996696
http://dx.doi.org/10.1038/s41598-020-58097-1
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