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Different contributions of primary motor cortex, reticular formation, and spinal cord to fractionated muscle activation

Coordinated movement requires patterned activation of muscles. In this study, we examined differences in selective activation of primate upper limb muscles by cortical and subcortical regions. Five macaque monkeys were trained to perform a reach and grasp task, and electromyogram (EMG) was recorded...

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Detalles Bibliográficos
Autores principales: Zaaimi, Boubker, Dean, Lauren R., Baker, Stuart N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Physiological Society 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5866475/
https://www.ncbi.nlm.nih.gov/pubmed/29046427
http://dx.doi.org/10.1152/jn.00672.2017
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author Zaaimi, Boubker
Dean, Lauren R.
Baker, Stuart N.
author_facet Zaaimi, Boubker
Dean, Lauren R.
Baker, Stuart N.
author_sort Zaaimi, Boubker
collection PubMed
description Coordinated movement requires patterned activation of muscles. In this study, we examined differences in selective activation of primate upper limb muscles by cortical and subcortical regions. Five macaque monkeys were trained to perform a reach and grasp task, and electromyogram (EMG) was recorded from 10 to 24 muscles while weak single-pulse stimuli were delivered through microelectrodes inserted in the motor cortex (M1), reticular formation (RF), or cervical spinal cord (SC). Stimulus intensity was adjusted to a level just above threshold. Stimulus-evoked effects were assessed from averages of rectified EMG. M1, RF, and SC activated 1.5 ± 0.9, 1.9 ± 0.8, and 2.5 ± 1.6 muscles per site (means ± SD); only M1 and SC differed significantly. In between recording sessions, natural muscle activity in the home cage was recorded using a miniature data logger. A novel analysis assessed how well natural activity could be reconstructed by stimulus-evoked responses. This provided two measures: normalized vector length L, reflecting how closely aligned natural and stimulus-evoked activity were, and normalized residual R, measuring the fraction of natural activity not reachable using stimulus-evoked patterns. Average values for M1, RF, and SC were L = 119.1 ± 9.6, 105.9 ± 6.2, and 109.3 ± 8.4% and R = 50.3 ± 4.9, 56.4 ± 3.5, and 51.5 ± 4.8%, respectively. RF was significantly different from M1 and SC on both measurements. RF is thus able to generate an approximation to the motor output with less activation than required by M1 and SC, but M1 and SC are more precise in reaching the exact activation pattern required. Cortical, brainstem, and spinal centers likely play distinct roles, as they cooperate to generate voluntary movements. NEW & NOTEWORTHY Brainstem reticular formation, primary motor cortex, and cervical spinal cord intermediate zone can all activate primate upper limb muscles. However, brainstem output is more efficient but less precise in producing natural patterns of motor output than motor cortex or spinal cord. We suggest that gross muscle synergies from the reticular formation are sculpted and refined by motor cortex and spinal circuits to reach the finely fractionated output characteristic of dexterous primate upper limb movements.
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spelling pubmed-58664752018-03-26 Different contributions of primary motor cortex, reticular formation, and spinal cord to fractionated muscle activation Zaaimi, Boubker Dean, Lauren R. Baker, Stuart N. J Neurophysiol Research Article Coordinated movement requires patterned activation of muscles. In this study, we examined differences in selective activation of primate upper limb muscles by cortical and subcortical regions. Five macaque monkeys were trained to perform a reach and grasp task, and electromyogram (EMG) was recorded from 10 to 24 muscles while weak single-pulse stimuli were delivered through microelectrodes inserted in the motor cortex (M1), reticular formation (RF), or cervical spinal cord (SC). Stimulus intensity was adjusted to a level just above threshold. Stimulus-evoked effects were assessed from averages of rectified EMG. M1, RF, and SC activated 1.5 ± 0.9, 1.9 ± 0.8, and 2.5 ± 1.6 muscles per site (means ± SD); only M1 and SC differed significantly. In between recording sessions, natural muscle activity in the home cage was recorded using a miniature data logger. A novel analysis assessed how well natural activity could be reconstructed by stimulus-evoked responses. This provided two measures: normalized vector length L, reflecting how closely aligned natural and stimulus-evoked activity were, and normalized residual R, measuring the fraction of natural activity not reachable using stimulus-evoked patterns. Average values for M1, RF, and SC were L = 119.1 ± 9.6, 105.9 ± 6.2, and 109.3 ± 8.4% and R = 50.3 ± 4.9, 56.4 ± 3.5, and 51.5 ± 4.8%, respectively. RF was significantly different from M1 and SC on both measurements. RF is thus able to generate an approximation to the motor output with less activation than required by M1 and SC, but M1 and SC are more precise in reaching the exact activation pattern required. Cortical, brainstem, and spinal centers likely play distinct roles, as they cooperate to generate voluntary movements. NEW & NOTEWORTHY Brainstem reticular formation, primary motor cortex, and cervical spinal cord intermediate zone can all activate primate upper limb muscles. However, brainstem output is more efficient but less precise in producing natural patterns of motor output than motor cortex or spinal cord. We suggest that gross muscle synergies from the reticular formation are sculpted and refined by motor cortex and spinal circuits to reach the finely fractionated output characteristic of dexterous primate upper limb movements. American Physiological Society 2018-01-01 2017-10-18 /pmc/articles/PMC5866475/ /pubmed/29046427 http://dx.doi.org/10.1152/jn.00672.2017 Text en Copyright © 2018 the American Physiological Society http://creativecommons.org/licenses/by/4.0/deed.en_US Licensed under Creative Commons Attribution CC-BY 4.0 (http://creativecommons.org/licenses/by/4.0/deed.en_US) : © the American Physiological Society.
spellingShingle Research Article
Zaaimi, Boubker
Dean, Lauren R.
Baker, Stuart N.
Different contributions of primary motor cortex, reticular formation, and spinal cord to fractionated muscle activation
title Different contributions of primary motor cortex, reticular formation, and spinal cord to fractionated muscle activation
title_full Different contributions of primary motor cortex, reticular formation, and spinal cord to fractionated muscle activation
title_fullStr Different contributions of primary motor cortex, reticular formation, and spinal cord to fractionated muscle activation
title_full_unstemmed Different contributions of primary motor cortex, reticular formation, and spinal cord to fractionated muscle activation
title_short Different contributions of primary motor cortex, reticular formation, and spinal cord to fractionated muscle activation
title_sort different contributions of primary motor cortex, reticular formation, and spinal cord to fractionated muscle activation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5866475/
https://www.ncbi.nlm.nih.gov/pubmed/29046427
http://dx.doi.org/10.1152/jn.00672.2017
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