An axonal sodium current gates motoneuron doublets and force amplification

Abstract

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 persistent sodium (NaP) current at the first node of Ranvier, which returns toward the initial segment and sums with somatic NaP current, the calcium-mediated afterdepolarization, and the passive membrane response. In our model, blocking any of these active currents abolishes the doublet, and monoaminergic facilitation of NaP determines whether doublets occur. Human motor units discharged repetitive doublets whose interval lengthened over time, a time course set by inactivation of the somatic NaP 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.