Electrogenic Na⁺/Ca²⁺ Exchange: A Novel Amplification Step in Squid Olfactory Transduction

Olfactory receptor neurons (ORNs) from the squid, Lolliguncula brevis, respond to the odors l-glutamate or dopamine with increases in internal Ca²⁺ concentrations ([Ca²⁺]_i). To directly asses the effects of increasing [Ca²⁺]_i in perforated-patched squid ORNs, we applied 10 mM caffeine to release Ca²⁺ from internal stores. We observed an inward current response to caffeine. Monovalent cation replacement of Na⁺ from the external bath solution completely and selectively inhibited the caffeine-induced response, and ruled out the possibility of a Ca²⁺-dependent nonselective cation current. The strict dependence on internal Ca²⁺ and external Na⁺ indicated that the inward current was due to an electrogenic Na⁺/Ca²⁺ exchanger. Block of the caffeine-induced current by an inhibitor of Na⁺/Ca²⁺ exchange (50–100 μM 2′,4′-dichlorobenzamil) and reversibility of the exchanger current, further confirmed its presence. We tested whether Na⁺/Ca²⁺ exchange contributed to odor responses by applying the aquatic odor l-glutamate in the presence and absence of 2′,4′-dichlorobenzamil. We found that electrogenic Na⁺/Ca²⁺ exchange was responsible for ∼26% of the total current associated with glutamate-induced odor responses. Although Na⁺/Ca²⁺ exchangers are known to be present in ORNs from numerous species, this is the first work to demonstrate amplifying contributions of the exchanger current to odor transduction.