Voluntary co‐contraction of ankle muscles alters motor unit discharge characteristics and reduces estimates of persistent inward currents

Motoneuronal persistent inward currents (PICs) are facilitated by neuromodulatory inputs but are highly sensitive to local inhibitory circuits. Estimates of PICs are reduced by group Ia reciprocal inhibition, and increased with the diffuse actions of neuromodulators released during remote muscle contraction. However, it remains unknown how motoneurons function in the presence of simultaneous excitatory and inhibitory commands. To probe this topic, we investigated motor unit discharge patterns and estimated PICs during voluntary co-contraction of ankle muscles, which simultaneously demands the contraction of agonist-antagonist pairs. Twenty participants performed triangular ramps of both co-contraction (simultaneous dorsiflexion and plantar flexion) and isometric dorsiflexion to a peak of 30% of their maximum muscle activity from a maximal voluntary contraction. Motor unit spike trains were decomposed from high-density surface EMG activity recorded from tibialis anterior using blind source separation algorithms. Voluntary co-contraction altered motor unit discharge rate characteristics. Discharge rate at recruitment and peak discharge rate were modestly reduced (∼6% change; P < 0.001; d = 0.22) and increased (∼2% change; P = 0.001, d = -0.19), respectively, in the entire dataset but no changes were observed when motor units were tracked across conditions. The largest effects during co-contraction were that estimates of PICs (ΔF) were reduced by ∼20% (4.47 vs. 5.57 pulses per second during isometric dorsiflexion; P < 0.001, d = 0.641). These findings suggest that, during voluntary co-contraction, the inhibitory input from the antagonist muscle overcomes the additional excitatory and neuromodulatory drive that may occur due to the co-contraction of the antagonist muscle, which constrains PIC behaviour. KEY POINTS: Voluntary co-contraction is a unique motor behaviour that concurrently provides excitatory and inhibitory synaptic input to motoneurons. Co-contraction of agonist-antagonist pairs alters agonist motor unit discharge characteristics, consistent with reductions in persistent inward current magnitude.

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Publication Details

Journal
The Journal of Physiology
Published
2024-08-19
DOI
https://doi.org/10.1113/jp286539
Citations
12
Primary Topic
Muscle activation and electromyography studies
Type
article
Field-Weighted Citation Impact
2.21

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article

Voluntary co‐contraction of ankle muscles alters motor unit discharge characteristics and reduces estimates of persistent inward currents

Francesco Negro, Gregory E. P. Pearcey, C. J. Heckman, Matheus Machado Gomes et al.
12 citations
The Journal of Physiology
Muscle activation and electromyography studies
2.21
article

Voluntary co‐contraction of ankle muscles alters motor unit discharge characteristics and reduces estimates of persistent inward currents

Francesco Negro, Gregory E. P. Pearcey, C. J. Heckman, Matheus Machado Gomes, James A. Beauchamp, Sophia T. Jenz
article en
12 citations

Abstract

Motoneuronal persistent inward currents (PICs) are facilitated by neuromodulatory inputs but are highly sensitive to local inhibitory circuits. Estimates of PICs are reduced by group Ia reciprocal inhibition, and increased with the diffuse actions of neuromodulators released during remote muscle contraction. However, it remains unknown how motoneurons function in the presence of simultaneous excitatory and inhibitory commands. To probe this topic, we investigated motor unit discharge patterns and estimated PICs during voluntary co-contraction of ankle muscles, which simultaneously demands the contraction of agonist-antagonist pairs. Twenty participants performed triangular ramps of both co-contraction (simultaneous dorsiflexion and plantar flexion) and isometric dorsiflexion to a peak of 30% of their maximum muscle activity from a maximal voluntary contraction. Motor unit spike trains were decomposed from high-density surface EMG activity recorded from tibialis anterior using blind source separation algorithms. Voluntary co-contraction altered motor unit discharge rate characteristics. Discharge rate at recruitment and peak discharge rate were modestly reduced (∼6% change; P < 0.001; d = 0.22) and increased (∼2% change; P = 0.001, d = -0.19), respectively, in the entire dataset but no changes were observed when motor units were tracked across conditions. The largest effects during co-contraction were that estimates of PICs (ΔF) were reduced by ∼20% (4.47 vs. 5.57 pulses per second during isometric dorsiflexion; P < 0.001, d = 0.641). These findings suggest that, during voluntary co-contraction, the inhibitory input from the antagonist muscle overcomes the additional excitatory and neuromodulatory drive that may occur due to the co-contraction of the antagonist muscle, which constrains PIC behaviour. KEY POINTS: Voluntary co-contraction is a unique motor behaviour that concurrently provides excitatory and inhibitory synaptic input to motoneurons. Co-contraction of agonist-antagonist pairs alters agonist motor unit discharge characteristics, consistent with reductions in persistent inward current magnitude.

The Journal of PhysiologyVol. 602(17)
Northwestern University (US), Memorial University of Newfoundland (CA), Universidade de Ribeirão Preto (BR), Universidade de São Paulo (BR), McCormick (United States) (US), University of Brescia (IT)
Fundação de Amparo à Pesquisa do Estado de São Paulo, Universidade de São Paulo, Universidade Estadual Paulista, National Institutes of Health, Natural Sciences and Engineering Research Council of Canada, National Institute of Neurological Disorders and Stroke
Openalex Percentile: Top 12%
Muscle activation and electromyography studies
2.21
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