Neurons of the avian nucleus laminaris (NL) provide a neural substrate for azimuthal sound localization. We examined the optimal stimuli for NL neurons to maintain high discharge rates, reliable phase-locking, and sensitivity to time-delayed stimuli. Whole-cell recordings were performed in chick [embryonic days 19–21 (E19-E21)] NL neurons using an in vitro slice preparation. Variation of membrane properties along the tonotopic axis was examined. Computer-controlled intracellular current injection was used to mimic postsynaptic currents or conductances (PSCs) generated in NL neurons by the firing of nucleus magnocellularis (NM) neurons during acoustic stimulation. At various stimulus frequencies, the effects of varying the number of NM cells and PSC amplitudes on firing rate and phase-locking were examined. During high- frequency stimulation, the greatest firing rate and phase-locking occurred when the protocol contained few NM cells that generated large PSCs. Because the stimulus-evoked unitary PSCs are small, we propose that NM cells fire in synchrony to generate large PSCs. To mimic the arrival of PSCs during binaural stimulation, two stimulus trains were summed at different delays before injection. The firing rate of NL neurons was greatest with zero delay. A delay of half the stimulus period evoked firing that was less than that evoked with a single train. Neurons lacking strong outward rectification exhibited neither reliable phase-locking during high-frequency stimulation nor sensitivity to stimulus delays. These findings suggest that the firing responses of NL neurons are determined primarily by their membrane properties.