Type I spiral ganglion cells provide the afferent innervation to the inner hair cells of the mammalian organ of Corti and project centrally to the cochlear nucleus. While single-unit studies conducted over the past several decades have provided a wealth of information concerning the response characteristics of these neurons and, to some extent, their receptor targets, little is known about the neuron's intrinsic electrical properties. These properties undeniably will contribute to the firing patterns induced by acoustic stimuli. Type I spiral ganglion cell somata from the guinea pig inner ear were acutely isolated and the voltage-dependent conductances were analyzed with the whole-cell voltage clamp. Under conditions that mimic the normal intra- and extracellular ionic environments, type I spiral ganglion cells demonstrate fast inward TTX-sensitive Na currents (whose current density varied markedly among cells) and somewhat more slowly developing outward K currents. Resting potentials averaged -67.3 mV. Under current clamp, no spontaneous spike activity was noted, but short current injections produced graded action potentials with after hyperpolarizations lasting several milliseconds. The nondecaying outward K current activated at potentials near rest and was characterized by a pronounced rectification. The kinetics of the Na and K currents were rapid. Maximum peak inward Na currents occurred within 400 microseconds, between a voltage range of -10 and 0 mV, and inactivated within 4 msec. Recovery from inactivation was also rapid. At a holding potential of -80 mV, the time constant for recovery from an inactivating voltage step to -10 mV was 2.16 msec. Above -50 mV outward K currents reach half-maximal amplitude within 1.5 msec. In addition to these currents, a slow noninactivating TTX-sensitive inward current was observed that was blockable with Cd2+ or Gd3+. Problems encountered with blocking the tremendous outward K current hampered the characterization of this inward current. Similarities between the kinetics of ganglion cell currents and some of the rapid temporal characteristics of eighth nerve single-unit activity confirm the notion that intrinsic membrane properties help shape auditory neuron responses to sound.