A Depolarizing Chloride Current Contributes to Chemoelectrical Transduction in Olfactory Sensory Neurons in Situ

Recent biophysical investigations of vertebrate olfactory signal transduction have revealed that Ca2+-gated Cl- channels are activated during odorant detection in the chemosensory membrane of olfactory sensory neurons (OSNs). To understand the role of these channels in chemoelectrical signal transduction, it is necessary to know the Cl--equilibrium potential that determines direction and size of Cl- fluxes across the chemosensory membrane. We have measured Cl-, Na+, and K+ concentrations in ultrathin cryosections of rat olfactory epithelium, as well as relative element contents in isolated microsamples of olfactory mucus, using energy-dispersive x-ray microanalysis. Determination of the Cl- concentrations in dendritic knobs and olfactory mucus yielded an estimate of the Cl--equilibrium potential ECl in situ. With Cl- concentrations of 69 mM in dendritic knobs and 55 mM in olfactory mucus, we obtained an ECl value of +6 +/- 12 mV. This indicates that Ca2+-gated Cl- channels in olfactory cilia conduct inward currents in vivo carried by Cl- efflux into the mucus. Our results show that rat OSNs are among the few known types of neurons that maintain an elevated level of cytosolic Cl-. In these cells, activation of Cl- channels leads to depolarization of the membrane voltage and can induce electrical excitation. The depolarizing Cl- current in mammalian OSNs appears to contribute a major fraction to the receptor current and may sustain olfactory function in sweet-water animals.