Bandpass corticospinal transmission during repetitive TMS revealed by motor unit recordings

We employed a noninvasive high-density surface electromyography (HDsEMG) framework to track spinal motor neuron responses during repetitive transcranial magnetic stimulation (rTMS) and characterize corticospinal transmission of different stimulation frequencies and intensities to the alpha motor neuron pool. Eleven healthy individuals performed isometric thumb flexion at 10% of maximal voluntary contraction 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 signals before stimulation and tracked during rTMS. Input-output coupling was quantified using coherence between the rTMS train and individual motor unit spike trains or the cumulative spike train (CST), with shuffled spike trains used as surrogate controls. rTMS inputs were robustly transmitted to spinal motor neurons for all frequencies except 5 Hz, indicating widespread corticospinal coupling. Transmission behaved linearly, with CST output spectra reproducing input frequencies and scaling proportionally with stimulation intensity. The estimated transfer function revealed a bandpass-like profile, with maximal transmission between 10 and 60 Hz. Transmitted inputs also induced oscillatory components in the common synaptic input to motor neurons at stimulation frequency. Simulations indicated that this frequency selectivity emerges from balanced excitatory and inhibitory inputs to the motor neuron pool, with specific synaptic dynamics. These findings demonstrate that corticospinal transmission during rTMS acts as a frequency-selective linear system and provide a framework for assessing and modulating corticospinal pathways, with potential application as tool for tracking disease progression and neurorehabilitation. Highlights- HDsEMG decomposition tracks spinal motor neuron activity during rTMS. - Corticospinal transmission scales with rTMS stimulation intensity. - Corticospinal pathways act as a frequency-selective system. - rTMS transfer function shows maximal transmission at 10-60 Hz. - EPSP-IPSP interactions explain bandpass corticospinal transmission during rTMS.