Neurons of the avian nucleus magnocellularis (NM) relay auditory information from the VIIIth nerve to other parts of the auditory system. To examine the cellular properties that permit NM neurons to transmit reliably the temporal characteristics of the acoustic stimulus, we performed whole-cell recordings in neurons of the chick NM using an in vitro thin slice preparation. NM neurons exhibited strong outward rectification near resting potential; the voltage responses to depolarizing current steps were substantially smaller than to equivalent hyperpolarizing steps. Suprathreshold current steps evoked only a single action potential at the start of the step. In contrast, stimulation with trains of brief current pulses evoked repetitive firing that was phase-locked to the stimulus cycle. The number of action potentials evoked by the pulses during the train decreased with increasing stimulus rate. Voltage-clamp experiments revealed a rapidly activating, slowly inactivating, outward current with a threshold near - 65 mV. During depolarizing voltage steps, the outward current rose sigmoidally to a peak and then decayed slowly, reaching steady state within 5 sec. Application of 200 microM 4-aminopyridine (4-AP) reduced the peak of the outward current by 84%, leaving a small, persistent component. Under current clamp, application of 200 microM 4-AP reduced the outward rectification and increased the amplitude and duration of the action potentials. Moreover, NM neurons could no longer sustain firing during high rates of stimulation with the current pulses: increased temporal summation of the potentials caused sufficient depolarization to inactivate the sodium conductance underlying the action potential. These results suggest that the outward current is necessary for NM neurons to transmit well-timed events reliably for the duration of an acoustic stimulus.