State- and Identity-Dependent Motor Neuron Excitability Shapes Cutaneous Long-Latency Reflexes

Abstract

Neuromuscular reflexes elicited by sensory nerve stimulation provide valuable insights into neural motor control pathways. Analysis at the level of individual motor units (MUs) is feasible via electromyographic decomposition, but the factors shaping MU-specific reflex responses remain poorly understood. We investigated long-latency responses to cutaneous electrical stimulation in a large population of tibialis anterior MUs from nine healthy subjects during isometric ankle dorsiflexion at 10-30% of maximum voluntary contraction. Individual MU reflex responses differed markedly. Using 1000 stimulation pulses per trial, substantially more than the 150-300 typically reported in previous studies, provided more reliable estimates of cutaneous reflex characteristics. Across the motor pool, reflex magnitude increased with force level (p < 0.001) while excitation probability correlated significantly with MU recruitment threshold in 78% of subjects (p = 0.012). Furthermore, excitation probability increased systematically with contraction intensity (p < 0.001) for individually tracked MUs. Post-excitatory depression (PED) magnitude correlated significantly with excitation probability (r = 0.50, p < 0.001) of individual MUs. A targeted reflex-removal analysis, validated by MU simulations incorporating realistic excitation probabilities into ordinary firing patterns, reduced the PED by 84.2% in simulated data but only by 34.7% in recorded units. These findings suggest that the PED is a complex, hybrid phenomenon, resulting from synchronization-induced discharge resetting and additional independent inhibitory components. These findings demonstrate that MU-level reflex excitability to somatosensory input is influenced by state- and identity-dependent motor neuron characteristics, underscoring the importance of using sufficient stimulation pulses for reliable reflex measures and MU population analysis.