Each eye of the mollusc Hermissenda consists of five photoreceptors, two type A and three type B cells. Type A cells are quiescent, whereas B cells are spontaneously active in the dark. Differences in the intrinsic membrane properties of type A and B photoreceptors were studied using voltage- and current-clamp techniques. The current density of a Ni2+-sensitive, low-voltage activated Ca2+ current was similar in the two cell types. However, type B cells express an inward rectifier current (Ih) that has different permeation and pharmacological properties from the inward rectifier current in type A cells. The current in the B cells was time-dependent and was blocked by Cs+. Na+ and K+ were the charge carriers for Ih. The inward rectifier current in A cells (IK1) was time-independent, was selectively permeable to K+, and was blocked by Ba2+. Ni2+ reduced the spontaneous spike activities of type A and B cells, whereas Cs+ produced membrane hyperpolarization and reduced the spike activities of dark-adapted B cells. The application of both Cs+ and Ni2+ completely blocked dark-adapted spontaneous activities of B cells. Moreover, Ba2+ increased the excitability of type A cells but not B cells. Hence, differential expression of the two distinct inward rectifiers found in type A and B cells contributes to differences in their intrinsic membrane properties. Because changes in the excitability of the two cell types are correlates of conditioning in Hermissenda, modulation of these underlying currents may play a major role during conditioning-induced plasticity.