K⁺ channels shape individual action potentials and determine their pattern of firing. In auditory relays, both high- and low-voltage activated K⁺ channels (HVA and LVA) are critical for preservation of auditory timing cues. We have examined how these channels participate in firing in the medial nucleus of the trapezoid body. Principal cells at physiological temperature were voltage clamped using spike waveforms previously recorded in response to calyceal firing. Current components were isolated by digital subtraction of traces recorded in the channel antagonists dendrotoxin-I or tetraethylammonium. During orthodromic spikes delivered at 300 Hz and 600 Hz, both currents activated with a slight delay, peaking just after the crest of the spike. The decay of HVA was sufficiently fast to match the time course of the spike. By contrast, with 300 Hz stimuli, LVA continued to decay after the spikes reached a stable inter-spike potential. Although LVA currents partially inactivate during prolonged voltage steps, their peak amplitudes remained stable or increased during trains of spike-like stimuli. At 600 Hz, LVA did not fully deactivate between the spikes, and therefore generated a leak current. In order to determine the effect of blocking LVA channels on spiking, pre-recorded postsynaptic conductances were injected, with and without dendrotoxin-I. After block of LVA channels, strong synaptic conductances produced broader spikes, greater spike jitter, and prolonged depolarized states. HVA blockade with tetraethylammonium also broadened spikes but led to less error in timing. These results reveal multiple roles for LVA channels in spike repolarization and timing during synaptic activity.