Neural filtering of physiological tremor oscillations to spinal motor neurons mediates short-term acquisition of a skill learning task

Abstract

Skill acquisition of force-matching tasks is mediated by adaptations of spinal and supraspinal pathways to alpha motoneurons. In this study, we estimated the shared synaptic contributions of these pathways to understand the neural mechanisms behind the short-term acquisition of a new force-matching task. High-density surface electromyography (HDsEMG) was acquired from the first dorsal interosseous (FDI; 7 males and 6 females) and tibialis anterior (TA; 7 males and 4 females) while participants performed 15 trials of an isometric force-matching task. For two selected trials (pre- and post-skill acquisition), we decomposed the HDsEMG into motor unit spike trains, tracked motor units between trials, and calculated the mean discharge rate and the coefficient of variation of inter-spike interval (CoVISI). We also quantified the ratio (post/pre) of the area under the curve of motor units coherence within delta, alpha, and beta bands. For both muscles, improvements in force-matching were accompanied by a significant increase in the mean discharge rate and a decrease in CoVISI. In addition, the area under the curve within the alpha band significantly decreased by ~22% and ~13% for the TA and FDI muscles, respectively, with no changes in the delta or beta bands. Our results indicate that the short-term acquisition of a new force-matching skill is mediated by the attenuation of shared synaptic noise oscillations unrelated to the target force fluctuations. In other words, the central nervous system acts as a matched filter to modulate the synaptic weights of shared inputs and suppress neural components unrelated to the specific task.