Apart from their primary function as balance sensors, Hermissenda hair cells are presynaptic neurons involved in the Ca2+-dependent neuronal plasticity in postsynaptic B photoreceptors that accompanies classical conditioning. With a view to beginning to understand presynaptic mechanisms of plasticity in the vestibule-visual system, a locus for conditioning-induced neuronal plasticity, outward currents that may govern the excitability of hair cells were recorded by means of a whole-cell patch-clamp technique. Three K+ currents were characterized: a 4-aminopyridine-sensitive transient outward K+ current (I-A), a tetraethyl ammonium-sensitive delayed rectifier K+ current (I-K,I-V), and a Ca2+-activated K+ current (I-K,I-Ca). I-A activates and decays rapidly; the steady-state activation and inactivation curves of the current reveal a window current close to the apparent resting voltage of the hair cells, suggesting that the current is partially activated at rest. By modulating firing frequency and perhaps damping membrane oscillations, I-A may regulate synaptic release at baseline. In contrast, I-KV and I-K,I-Ca have slow onset and exhibit little or no inactivation. These two K+ currents may determine the duration of the repolarization phase of hair-cell action potentials and hence synaptic release via Ca2+ influx through voltage-gated Ca2+ channels. In addition, I-K,I-Ca may be responsible for the afterhyperpolarization of hair cell membrane voltage following prolonged stimulation.