Muscle contractile properties directly influence shared synaptic inputs to spinal motor neurons

Author:

Cabral Hélio V.1ORCID,Inglis J. Greig1ORCID,Cudicio Alessandro1ORCID,Cogliati Marta1ORCID,Orizio Claudio1,Yavuz Utku S.2,Negro Francesco1ORCID

Affiliation:

1. Department of Clinical and Experimental Sciences Università degli Studi di Brescia Brescia Italy

2. Biomedical Signals and Systems University of Twente Enschede Netherlands

Abstract

AbstractAlpha band oscillations in shared synaptic inputs to the alpha motor neuron pool can be considered an involuntary source of noise that hinders precise voluntary force production. This study investigated the impact of changing muscle length on the shared synaptic oscillations to spinal motor neurons, particularly in the physiological tremor band. Fourteen healthy individuals performed low‐level dorsiflexion contractions at ankle joint angles of 90° and 130°, while high‐density surface electromyography (HDsEMG) was recorded from the tibialis anterior (TA). We decomposed the HDsEMG into motor units spike trains and calculated the motor units’ coherence within the delta (1–5 Hz), alpha (5–15 Hz), and beta (15–35 Hz) bands. Additionally, force steadiness and force spectral power within the tremor band were quantified. Results showed no significant differences in force steadiness between 90° and 130°. In contrast, alpha band oscillations in both synaptic inputs and force output decreased as the length of the TA was moved from shorter (90°) to longer (130°), with no changes in delta and beta bands. In a second set of experiments (10 participants), evoked twitches were recorded with the ankle joint at 90° and 130°, revealing longer twitch durations in the longer TA muscle length condition compared to the shorter. These experimental results, supported by a simple computational simulation, suggest that increasing muscle length enhances the muscle's low‐pass filtering properties, influencing the oscillations generated by the Ia afferent feedback loop. Therefore, this study provides valuable insights into the interplay between muscle biomechanics and neural oscillations. imageKey points We investigated whether changes in muscle length, achieved by changing joint position, could influence common synaptic oscillations to spinal motor neurons, particularly in the tremor band (5–15 Hz). Our results demonstrate that changing muscle length from shorter to longer induces reductions in the magnitude of alpha band oscillations in common synaptic inputs. Importantly, these reductions were reflected in the oscillations of muscle force output within the alpha band. Longer twitch durations were observed in the longer muscle length condition compared to the shorter, suggesting that increasing muscle length enhances the muscle's low‐pass filtering properties. Changes in the peripheral contractile properties of motor units due to changes in muscle length significantly influence the transmission of shared synaptic inputs into muscle force output. These findings prove the interplay between muscle mechanics and neural adaptations.

Funder

HORIZON EUROPE European Research Council

Publisher

Wiley

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