Heterogeneous distribution of inhibitory inputs among motor units as a key mechanism for motor adaptations to pain

Abstract

Pain significantly influences movement, yet the precise neural mechanisms underlying the wide range of observed motor adaptations remain unclear. This study combined experimental data and in silico models to investigate the contribution of inhibitory and neuromodulatory inputs to motor unit behaviour during submaximal contractions performed in the presence of pain. Specifically, we aimed to unravel the distribution pattern of inhibitory inputs to the motor unit pool. Seventeen participants performed isometric knee extension tasks under three conditions: Control, Pain (induced by injecting hypertonic saline into the infra-patellar fat pad), and Washout. We identified large samples of motor units in the vastus lateralis (up to 53/participant) from high-density electromyographic signals, which led to three key observations. First, while motor unit discharge rates significantly decreased during Pain, a substantial proportion of motor units (14.8-24.8%) did not show this decrease and, in some cases, even exhibited an increase. Second, using complementary approaches we showed that pain did not alter the amplification and prolongation effects of persistent inward currents on motor unit discharge, providing evidence that neuromodulatory drive to motor neurons remained unchanged. Third, we observed a significant reduction in the proportion of common inputs to motor units during Pain. To explore potential neurophysiological mechanisms underlying these experimental results, we simulated the behaviour of motor unit pools with varying distribution patterns of inhibitory inputs. Our simulation supports the hypothesis of a non-homogeneous distribution of inhibitory inputs, independent of motor unit size, as a key neural mechanism underlying motor adaptations to experimental pain.