Olfactory response termination involves Ca2+-ATPase in vertebrate olfactory receptor neuron cilia

Abstract

In vertebrate olfactory receptor neurons (ORNs), odorant-induced activation of the transduction cascade culminates in production of cyclic AMP, which opens cyclic nucleotide–gated channels in the ciliary membrane enabling Ca2+ influx. The ensuing elevation of the intraciliary Ca2+ concentration opens Ca2+-activated Cl− channels, which mediate an excitatory Cl− efflux from the cilia. In order for the response to terminate, the Cl− channel must close, which requires that the intraciliary Ca2+ concentration return to basal levels. Hitherto, the extrusion of Ca2+ from the cilia has been thought to depend principally on a Na+–Ca2+ exchanger.In this study, we show using simultaneous suction pipette recording and Ca2+-sensitive dye fluorescence measurements that in fire salamander ORNs, withdrawal of external Na+ from the solution bathing the cilia, which incapacitates Na+–Ca2+exchange, has only a modest effect on the recovery of the electrical response and the accompanying decay of intraciliary Ca2+ concentration. In contrast, exposure of the cilia to vanadate or carboxyeosin, a manipulation designed to block Ca2+-ATPase, has a substantial effect on response recovery kinetics. Therefore, we conclude that Ca2+-ATPase contributes to Ca2+ extrusion in ORNs, and that Na+–Ca2+exchange makes only a modest contribution to Ca2+ homeostasis in this species.