An axonal sodium current gates motoneuron doublets and force amplification

Brief high-frequency bursts of action potentials shape neural coding. In spinal motoneurons, they appear as doublets, closely spaced spike pairs observed for a century that amplify muscle force nonlinearly through the catch-like property. However, the cellular and anatomical origins of doublets remain unresolved. Combining intracellular recordings, a conductance-based model, and human motor unit and force data, we show that initial and repetitive doublets arise from the same mechanism. Both spikes are initiated at the axon initial segment, but the second is driven by a slowly inactivating persistent sodium current at the first node of Ranvier, which returns toward the initial segment and sums with somatic persistent sodium current and the calcium-mediated afterdepolarization. Blocking any of these currents abolishes the doublet, and monoaminergic facilitation of persistent sodium determines whether doublets occur. Human motor units discharged repetitive doublets during voluntary contraction, with the intra-doublet interval lengthening over time as set by the inactivation of the somatic persistent sodium current, and produced nonlinear increases in force. Because monoaminergic drive both gates the doublet and sets how its interval evolves, neuromodulation shapes not only the gain but also the timing of motoneuron output.