Decoding firings of a large population of human motor units from high-density surface electromyogram in response to transcranial magnetic stimulation.

We describe a novel application of methodology for high-density surface electromyography (HDsEMG) decomposition to identify motor unit (MU) firings in response to transcranial magnetic stimulation (TMS). The method is based on the MU filter estimation from HDsEMG decomposition with convolution kernel compensation during voluntary isometric contractions and its application to contractions elicited by TMS. First, we simulated synthetic HDsEMG signals during voluntary contractions followed by simulated motor evoked potentials (MEPs) recruiting an increasing proportion of the motor pool. The estimation of MU filters from voluntary contractions and their application to elicited contractions resulted in high (>90%) precision and sensitivity of MU firings during MEPs. Subsequently, we conducted three experiments in humans. From HDsEMG recordings in first dorsal interosseous and tibialis anterior muscles, we demonstrated an increase in the number of identified MUs during MEPs evoked with increasing stimulation intensity, low variability in the MU firing latency and a proportion of MEP energy accounted for by decomposition similar to voluntary contractions. A negative relationship between the MU recruitment threshold and the number of identified MU firings was exhibited during the MEP recruitment curve, suggesting orderly MU recruitment. During isometric dorsiflexion we also showed a negative association between voluntary MU firing rate and the number of firings of the identified MUs during MEPs, suggesting a decrease in the probability of MU firing during MEPs with increased background MU firing rate. We demonstrate accurate identification of a large population of MU firings in a broad recruitment range in response to TMS via non-invasive HDsEMG recordings. KEY POINTS: Transcranial magnetic stimulation (TMS) of the scalp produces multiple descending volleys, exciting motor pools in a diffuse manner. The characteristics of a motor pool response to TMS have been previously investigated with intramuscular electromyography (EMG), but this is limited in its capacity to detect many motor units (MUs) that constitute a motor evoked potential (MEP) in response to TMS. By simulating synthetic signals with known MU firing patterns, and recording high-density EMG signals from two human muscles, we show the feasibility of identifying firings of many MUs that comprise a MEP. We demonstrate the identification of firings of a large population of MUs in the broad recruitment range, up to maximal MEP amplitude, with fewer required stimuli compared to intramuscular EMG recordings. The methodology demonstrates an emerging possibility to study responses to TMS on a level of individual MUs in a non-invasive manner.