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Decoding of the spike timing of primary afferents during voluntary arm movements in monkeys

Understanding the mechanisms of encoding forelimb kinematics in the activity of peripheral afferents is essential for developing a somatosensory neuroprosthesis. To investigate whether the spike timing of dorsal root ganglion (DRG) neurons could be estimated from the forelimb kinematics of behaving...

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Autores principales: Umeda, Tatsuya, Watanabe, Hidenori, Sato, Masa-aki, Kawato, Mitsuo, Isa, Tadashi, Nishimura, Yukio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4023037/
https://www.ncbi.nlm.nih.gov/pubmed/24860416
http://dx.doi.org/10.3389/fnins.2014.00097
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author Umeda, Tatsuya
Watanabe, Hidenori
Sato, Masa-aki
Kawato, Mitsuo
Isa, Tadashi
Nishimura, Yukio
author_facet Umeda, Tatsuya
Watanabe, Hidenori
Sato, Masa-aki
Kawato, Mitsuo
Isa, Tadashi
Nishimura, Yukio
author_sort Umeda, Tatsuya
collection PubMed
description Understanding the mechanisms of encoding forelimb kinematics in the activity of peripheral afferents is essential for developing a somatosensory neuroprosthesis. To investigate whether the spike timing of dorsal root ganglion (DRG) neurons could be estimated from the forelimb kinematics of behaving monkeys, we implanted two multi-electrode arrays chronically in the DRGs at the level of the cervical segments in two monkeys. Neuronal activity during voluntary reach-to-grasp movements were recorded simultaneously with the trajectories of hand/arm movements, which were tracked in three-dimensional space using a motion capture system. Sixteen and 13 neurons, including muscle spindles, skin receptors, and tendon organ afferents, were recorded in the two monkeys, respectively. We were able to reconstruct forelimb joint kinematics from the temporal firing pattern of a subset of DRG neurons using sparse linear regression (SLiR) analysis, suggesting that DRG neuronal ensembles encoded information about joint kinematics. Furthermore, we estimated the spike timing of the DRG neuronal ensembles from joint kinematics using an integrate-and-fire model (IF) incorporating the SLiR algorithm. The temporal change of firing frequency of a subpopulation of neurons was reconstructed precisely from forelimb kinematics using the SLiR. The estimated firing pattern of the DRG neuronal ensembles encoded forelimb joint angles and velocities as precisely as the originally recorded neuronal activity. These results suggest that a simple model can be used to generate an accurate estimate of the spike timing of DRG neuronal ensembles from forelimb joint kinematics, and is useful for designing a proprioceptive decoder in a brain machine interface.
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spelling pubmed-40230372014-05-23 Decoding of the spike timing of primary afferents during voluntary arm movements in monkeys Umeda, Tatsuya Watanabe, Hidenori Sato, Masa-aki Kawato, Mitsuo Isa, Tadashi Nishimura, Yukio Front Neurosci Neuroscience Understanding the mechanisms of encoding forelimb kinematics in the activity of peripheral afferents is essential for developing a somatosensory neuroprosthesis. To investigate whether the spike timing of dorsal root ganglion (DRG) neurons could be estimated from the forelimb kinematics of behaving monkeys, we implanted two multi-electrode arrays chronically in the DRGs at the level of the cervical segments in two monkeys. Neuronal activity during voluntary reach-to-grasp movements were recorded simultaneously with the trajectories of hand/arm movements, which were tracked in three-dimensional space using a motion capture system. Sixteen and 13 neurons, including muscle spindles, skin receptors, and tendon organ afferents, were recorded in the two monkeys, respectively. We were able to reconstruct forelimb joint kinematics from the temporal firing pattern of a subset of DRG neurons using sparse linear regression (SLiR) analysis, suggesting that DRG neuronal ensembles encoded information about joint kinematics. Furthermore, we estimated the spike timing of the DRG neuronal ensembles from joint kinematics using an integrate-and-fire model (IF) incorporating the SLiR algorithm. The temporal change of firing frequency of a subpopulation of neurons was reconstructed precisely from forelimb kinematics using the SLiR. The estimated firing pattern of the DRG neuronal ensembles encoded forelimb joint angles and velocities as precisely as the originally recorded neuronal activity. These results suggest that a simple model can be used to generate an accurate estimate of the spike timing of DRG neuronal ensembles from forelimb joint kinematics, and is useful for designing a proprioceptive decoder in a brain machine interface. Frontiers Media S.A. 2014-05-09 /pmc/articles/PMC4023037/ /pubmed/24860416 http://dx.doi.org/10.3389/fnins.2014.00097 Text en Copyright © 2014 Umeda, Watanabe, Sato, Kawato, Isa and Nishimura. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Umeda, Tatsuya
Watanabe, Hidenori
Sato, Masa-aki
Kawato, Mitsuo
Isa, Tadashi
Nishimura, Yukio
Decoding of the spike timing of primary afferents during voluntary arm movements in monkeys
title Decoding of the spike timing of primary afferents during voluntary arm movements in monkeys
title_full Decoding of the spike timing of primary afferents during voluntary arm movements in monkeys
title_fullStr Decoding of the spike timing of primary afferents during voluntary arm movements in monkeys
title_full_unstemmed Decoding of the spike timing of primary afferents during voluntary arm movements in monkeys
title_short Decoding of the spike timing of primary afferents during voluntary arm movements in monkeys
title_sort decoding of the spike timing of primary afferents during voluntary arm movements in monkeys
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4023037/
https://www.ncbi.nlm.nih.gov/pubmed/24860416
http://dx.doi.org/10.3389/fnins.2014.00097
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