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

Author:

Gomes Matheus M.12ORCID,Jenz Sophia T.1ORCID,Beauchamp James A.13ORCID,Negro Francesco4ORCID,Heckman C. J.1ORCID,Pearcey Gregory E. P.15ORCID

Affiliation:

1. Department of Physical Therapy and Human Movement Sciences, Feinberg School of Medicine Northwestern University Chicago Illinois USA

2. School of Physical Education and Sport of Ribeirão Preto University of São Paulo Ribeirão Preto Brazil

3. Department of Biomedical Engineering, McCormick School of Engineering Northwestern University Chicago Illinois USA

4. Department of Clinical and Experimental Sciences Universita degli Studi di Brescia Brescia Italy

5. School of Human Kinetics and Recreation Memorial University of Newfoundland St. John's Canada

Abstract

AbstractMotoneuronal 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. imageKey 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.

Funder

Fundação de Amparo à Pesquisa do Estado de São Paulo

Publisher

Wiley

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