Axons of the type B photoreceptors form synapses with hair cells and interneurons that are involved in classical conditioning in Hermissenda. We examined the differences in the Ca2+ channels expressed in the soma and axons of the B photoreceptors by direct functional recordings of single-channel currents. Although the soma of the B cells express two Ca2+ current subtypes, a transient BayK 8644-insensitive (approximately 17 pS) current and a sustained BayK 8644-sensitive (approximately 10 pS) current, the axons expressed only the latter. The axonal Ca2+ current activated at potentials positive to -20 mV. Moreover, the Ca2+ channels are distributed heterogeneously along the length of the axon, with the higher channel density (approximately 10-15 channel microm(-2)) occurring at the distal one-third of the isolated axons, with respect to the soma. The regions of Ca2+ channel clusters may represent the presynaptic site of the photoreceptor-interneuron synapses. Furthermore, the high-density clusters of Ca2+ channels may augment postsynaptic responses. The results of the present study represent the first direct recordings of Ca2+ currents at presumed synaptic sites. Expression of different Ca2+ channel subtypes at distinct compartments of the type B photoreceptors may generate diverse Ca2+ domains that may be required for neuronal plasticity in Hermissenda.