Bushy cells in the ventral cochlear nucleus convey firing of auditory nerve fibers to neurons in the superior olivary complex that compare the timing and intensity of sounds at the two ears and enable animals to localize sound sources in the horizontal plane. Three voltage-sensitive conductances allow bushy cells to convey acoustic information with submillisecond temporal precision. All bushy cells have a low-voltage-activated, alpha-dendrotoxin (alpha-DTX)-sensitive K(+) conductance (g(KL)) that was activated by depolarization past -70 mV, was half-activated at -39.0 +/- 1.7 (SE) mV, and inactivated approximately 60% over 5 s. Maximal g(KL) varied between 40 and 150 nS (mean: 80.8 +/- 16.7 nS). An alpha-DTX-insensitive, tetraethylammonium (TEA)-sensitive, K(+) conductance (g(KH)) was activated at voltages positive to -40 mV, was half-activated at -18.1 +/- 3.8 mV, and inactivated by 90% over 5 s. Maximal g(KH) varied between 35 and 80 nS (mean: 58.2 +/- 6.5 nS). A ZD7288-sensitive, mixed cation conductance (g(h)) was activated by hyperpolarization greater than -60 mV and half-activated at -83.1 +/- 1.1 mV. Maximum g(h) ranged between 14.5 and 56.6 nS (mean: 30.0 +/- 5.5 nS). 8-Br-cAMP shifted the voltage sensitivity of g(h) positively. Changes in temperature stably altered the steady-state magnitude of I(h). Both g(KL) and g(KH) contribute to repolarizing action potentials and to sharpening synaptic potentials. Those cells with the largest g(h) and the largest g(KL) fired least at the onset of a depolarization, required the fastest depolarizations to fire, and tended to be located nearest the nerve root.