Bandpass corticospinal transmission during repetitive TMS revealed by motor unit recordings

Abstract

We employed a noninvasive high-density surface electromyography (HDsEMG) framework to track spinal motor neuron responses during repetitive transcranial magnetic stimulation (rTMS) and characterize the transmission of rhythmic corticospinal inputs to the alpha motor neuron pool. Eleven healthy individuals performed isometric thumb flexion while rTMS was delivered over the motor cortex at five frequencies (5, 10, 20, 30, and 50 Hz) and three subthreshold intensities (50%, 60%, and 70% of resting motor threshold). Motor units were decomposed from HDsEMG before stimulation and tracked during rTMS, allowing input-output coupling between the stimulation train and individual motor unit and cumulative spike train activity to be quantified. rTMS inputs were significantly transmitted at all frequencies except 5 Hz, indicating widespread corticospinal coupling. At the motor neuron population level, corticospinal transmission preserved the spectral components of the rTMS input and exhibited intensity-dependent increases in coupling strength, consistent with approximately linear transmission. The estimated corticospinal transmission exhibited a bandpass-like profile, with transmission between 20 and 50 Hz significantly greater than at lower and higher frequency ranges. Transmitted rTMS inputs induced frequency-specific increases in the common synaptic input to motor neurons, with oscillations at the stimulation frequency significantly enhanced during rTMS compared with before stimulation. Computational simulations reproduced this frequency selectivity only when excitatory and inhibitory postsynaptic inputs were combined. These findings reveal frequency-selective, approximately linear corticospinal transmission during rTMS and establish a noninvasive framework for assessing corticospinal function, with potential application as a tool for tracking changes associated with neurological disease and response to neurorehabilitation.