A G-protein dependent serotonin (5-HT) receptor on B photoreceptors of Hermissenda crassicornis was investigated. Microapplication of 5-HT to the soma region, but not to the terminal branches, resulted in a rapid, biphasic depolarization with a slow time course of dissipation. The 5-HT-induced depolarization increased at hyperpolarized potentials, and exhibited a strong and complex sensitivity to external K+, but not Na+ or Ca2+. The 5-HT response, but not a cholinergically mediated intraphotoreceptor interaction, was abolished by intracellular injection of the G protein antagonist, GDP[beta S], although the response was unaffected by pretreatment with pertussis toxin. These results are discussed in terms of known 5-HT receptor subtypes, and the potential role of this receptor in activity-dependent forms of plasticity exhibited by these cells.