Proximal and distal spinal neurons innervating multiple synergist and antagonist motor pools

Ronzano, Remi; Lancelin, Camille; Bhumbra, G. S.; Brownstone, Robert M.; Beato, Marco

doi:10.7554/elife.70858

Cited by 32 publications

(27 citation statements)

References 69 publications

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“…These results suggest that the neural control of movements may be hierarchically organized, where motor neuron synergies are controlled instead of individual motor neurons (Loeb et al, 1999). Thus, spinal circuits involving premotor neurons and interneurons may span across motor nuclei to transmit these correlated inputs to synergist muscles (Levine et al, 2014; Takei et al, 2017; Ronzano et al, 2021). However, as motor neurons are the final common pathways where inputs from supraspinal centers and afferent fibers converge, we cannot make any inference about the origin of the correlated inputs though several candidates exist.…”

Section: Discussionmentioning

confidence: 99%

Two motor neuron synergies, invariant across ankle joint angles, activate the triceps surae during plantarflexion

Levine

Avrillon

Farina

et al. 2022

Preprint

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Recent studies have suggested that the central nervous system generates movements by controlling groups of motor neurons (synergies) that do not always align with muscle anatomy. In this study, we determined whether these synergies are robust across tasks with different mechanical constraints. We identified motor neuron synergies using principal component analysis (PCA) and cross-correlations between smoothed discharge rates of motor neurons. In Part 1, we used simulations to validate these methods. The results suggested that PCA can accurately identity the number of common inputs and classify motor neurons according to the synaptic weights of the common inputs they receive. Moreover, the results confirmed that cross-correlation can separate pairs of motor neurons that receive common inputs from those that do not receive common inputs. In Part 2, sixteen individuals performed plantarflexion at three ankle angles while recording high-density surface electromyography from the gastrocnemius lateralis (GL) and medialis (GM) and the soleus (SOL) muscles. We identified and tracked the same motor units across angles. PCA revealed two motor neuron synergies, primarily grouping motor neurons innervating GL-SOL and GM-SOL. These motor neuron synergies were relatively stable with 74.0% of motor neurons classified in the same synergy across angles. Cross-correlation demonstrated that only 13.9% of pairs of motor neurons maintained a non-significant level of correlation across angles, confirming the large presence of common inputs. Overall, these results highlighted the modularity of movement control at the motor neuron level, which may ensure a sensible reduction of computational resources for movement control.

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Section: Discussionmentioning

confidence: 99%

Two motor neuron synergies, invariant across ankle joint angles, activate the triceps surae during plantarflexion

Levine

Avrillon

Farina

et al. 2022

Preprint

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“…These functionally distinct groups of muscles may have differences in motoneuronal properties (i.e., intrinsic motoneuron properties, relative distribution of synaptic inputs from various descending and spinal pathways, etc.) 23 that alter their susceptibility to AIH-induced changes in strength.…”

Section: Discussionmentioning

confidence: 99%

Acute intermittent hypoxia enhances volitional elbow strength, and modulates spatial distribution of muscle activation patterns in persons with chronic incomplete spinal cord injury

Afsharipour

Pearcey

Rymer

et al. 2022

Preprint

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Background: Acute intermittent hypoxia (AIH) is an emerging technique for facilitating neural plasticity in individuals with major neurological deficits. In people with chronic incomplete spinal cord injury (iSCI), a single sequence of AIH enhances motor function such as hand grip strength and ankle plantarflexion torque, but the underlying mechanisms are not yet clear. Objective: To examine how AIH-induced changes in magnitude and spatial distribution of electromyography (EMG) activity over the surface of the biceps and triceps brachii muscles contributes to improved strength. Methods: Seven individuals with iSCI visited the laboratory on two occasions, at least a week apart, and received either AIH or Sham AIH intervention in a randomized order. AIH consisted of 15 brief (~60s) periods of low oxygen (fraction of inspired O2 = 0.09) alternating with 60s of normoxia, whereas Sham AIH consisted of repeated exposures to normoxic gas mixtures. Muscle activity of biceps and triceps brachii was recorded with high-density surface EMG during maximal elbow flexion and extension contractions. We used these EMG recordings to generate spatial maps which distinguished active muscle regions prior to and 60 minutes after AIH or Sham AIH. Results: After an AIH sequence, elbow flexion and extension forces increased by 91.7 +/- 33.5% and 51.7 +/- 21.9% from baseline, respectively, whereas there was no difference after Sham AIH exposure. Changes in strength were associated with an altered spatial distribution of EMG activity and increased root mean squared EMG amplitude in both biceps and triceps brachii muscles. Conclusions: These data suggest that altered motor unit activation profiles may underlie improved volitional strength after a single dose of AIH and warrant further investigation using single motor unit analysis techniques to further elucidate mechanisms of AIH-induced plasticity.

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“…These pathways originate in two distinct anatomical portions of the premotor cortex (Haruno et al, 2012), and are regulated by intracortical excitatory connections (Ethier et al, 2007). Moreover, these pathways may project to spinal premotor interneurons innervating motor pools of multiple antagonist muscles (Ronzano et al, 2021) selectively recruited during torque or stiffness generation.…”

Section: Discussionmentioning

confidence: 99%

Independent synaptic inputs to motor neurons driving antagonist muscles

Borzelli

Vieira

Botter

et al. 2022

Preprint

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The CNS may produce the same endpoint trajectory or torque profile with different muscle activation patterns. What differentiates these patterns is the presence of co-contraction, which does not contribute to joint torque generation but allows to modulate mechanical impedance. Whether co-contraction is controlled through the same synaptic input to motor neurons involved in generating joint torque is still unclear. We hypothesized that co-contraction is controlled through a specific synaptic input, independent from that underlying the control of torque. To test this hypothesis, we asked participants to concurrently generate multi-directional isometric forces at the hand and to modulate the co-contraction of arm muscles to displace and stabilize a virtual end-effector. The firings of motor units were identified through decomposition of High-Density EMGs collected from two antagonist muscles, Biceps Brachii and Triceps Brachii. We found significant peaks in the coherence between the neural drive to the two muscles, suggesting the existence of a common input modulating co-contraction across different exerted forces. Moreover, the within-muscle coherence computed after removing the component synchronized with the drive to the antagonist muscle or with the exerted force revealed two subsets of motor neurons that were selectively recruited to generate joint torque or modulate co-contraction. This study is the first to directly investigate the extent of shared versus independent control of antagonist muscles at the motor neuron level in a task involving concurrent force generation and modulation of co-contraction.

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Proximal and distal spinal neurons innervating multiple synergist and antagonist motor pools

Cited by 32 publications

References 69 publications

Two motor neuron synergies, invariant across ankle joint angles, activate the triceps surae during plantarflexion

Two motor neuron synergies, invariant across ankle joint angles, activate the triceps surae during plantarflexion

Acute intermittent hypoxia enhances volitional elbow strength, and modulates spatial distribution of muscle activation patterns in persons with chronic incomplete spinal cord injury

Independent synaptic inputs to motor neurons driving antagonist muscles

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