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

Abstract

The acquisition of a motor skill involves 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 underlying 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) during 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 post/pre ratio of motor units coherence within delta, alpha, and beta bands. Improvements in force-matching were accompanied by a significant increase in the mean discharge rate and a decrease in CoVISI for both muscles. Moreover, the area under the curve within alpha band decreased by [~]22% and [~]13% for the TA and FDI muscles, respectively, with no changes in the delta or beta bands. These reductions correlated significantly with increased coupling between force/neural drive and target oscillations. These results suggest that the short-term acquisition of a new force-matching skill is mediated by the attenuation of tremor oscillations in the shared synaptic inputs. 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. Supported by simulations, a plausible mechanism behind these alpha band reductions may involve spinal interneurons phase-cancelling descending oscillations.