K(v)3.1 uses a timely resurgent K(+) current to secure action potential repolarization

High-frequency action potential (AP) transmission is essential for rapid information processing in the central nervous system. Voltage-dependent K(v)3 channels play an important role in this process thanks to their high activation threshold and fast closure kinetics, which reduce the neuron's refractory period. However, premature K(v)3 channel closure leads to incomplete membrane repolarization, preventing sustainable AP propagation. Here, we demonstrate that K(v)3.1b channels solve this problem by producing resurgent K(+) currents during repolarization, thus ensuring enough repolarizing power to terminate each AP. Unlike previously described resurgent Na(+) and K(+) currents, K(v)3.1b's resurgent current does not originate from recovery of channel block or inactivation but results from a unique combination of steep voltage-dependent gating kinetics and ultra-fast voltage-sensor relaxation. These distinct properties are readily transferrable onto an orthologue K(v) channel by transplanting the voltage-sensor's S3–S4 loop, providing molecular insights into the mechanism by which K(v)3 channels contribute to high-frequency AP transmission.