Neurons of the inferior olive (IO) fire action potentials with large, long-lasting afterdepolarizations (ADPs). Broader ADPs support more spikes in climbing fibre axons and evoke longer bursts of complex spikes in Purkinje cells, which affect the magnitude and sign of cerebellar synaptic plasticity. In the present study, we investigated the ionic mechanisms that regulate IO action potential waveforms by making whole-cell recordings in brainstem slices from C57BL6/J mice. IO spikes evoked from rest had ADPs of ∼30 ms. After 500-ms hyperpolarizations, however, evoked action potentials were brief (1-2 ms), lacking ADPs altogether. Because such preconditioning should maximally recruit depolarizing Ih and T-type currents and minimize repolarizing Ca-dependent currents known to shape the ADP, the rapid action potential downstroke suggested additional, dominant recovery of voltage-gated K currents at negative voltages. Under voltage clamp, outward currents evoked from -98 mV included large, voltage-gated, rapidly inactivating 'A-type' K currents. These currents had a steep availability curve with half-inactivation at -85 mV, suitable for recruitment by small hyperpolarizations. The fast decay time constant increased with depolarization, as is typical of KV4 channels. The KV4 channel blocker AmmTx3 almost eliminated inactivating currents and broadened action potentials evoked from strongly negative potentials by ∼8-fold. Optogenetic stimulation of inhibitory cerebellar nucleo-olivary terminals hyperpolarized IO cells sufficiently to abolish the ADP. The data support the idea that currents through KV4 channels control action potential waveforms in IO cells, shortening ADPs during synaptic inhibition or troughs of membrane potential oscillations, thereby controlling the number of climbing fibre action potentials that propagate to the cerebellum. KEY POINTS Neurons in the mouse inferior olive (IO) express a large, inactivating, voltage-gated A-type K current carried by KV4 channels. IO action potentials evoked from rest have large, long afterdepolarizations that disappear with pre-spike hyperpolarizations of 5-15 mV. The steep voltage-sensitivity and rapid recovery of KV4 channels regulates the duration of the afterdepolarization over more than one order of magnitude. Factors such as synaptic inhibition are sufficient to recruit KV4 channels and eliminate afterdepolarization (ADP). By controlling the ADP, KV4 channels can set the number of climbing fibre action potentials relayed to the cerebellum and regulate plasticity implicated in motor learning.