Imaging odor-induced calcium transients in single olfactory cilia: specificity of activation and role in transduction.
The possibility that odor stimuli trigger distinct Ca2+ elevations within the cilia of vertebrate olfactory receptor neurons (ORNs) is a widely proposed concept. However, because of the small size of the olfactory cilia, the existence and properties of such Ca2+ elevations and their role in odor transduction are still unknown. We investigate odor-induced Ca2+ changes in individual olfactory cilia from salamander using the Ca2+ indicator dye fluo-3 in combination with laser scanning confocal microscopy. Single brief applications of odor ligand produce highly localized Ca2+ elevations in individual cilia lasting for several seconds. These Ca2+ signals originate in the cilia and depend entirely on Ca2+ entry through ciliary cyclic nucleotide-gated ion channels. The odor specificity of the Ca2+ rises implies a receptor-operated mechanism underlying odor detection. Each of the cilia on a receptor neuron functions as an independent biochemical compartment that can detect odorants and produce a Ca2+ transient with remarkably uniform properties in terms of kinetics and odor specificity. The rate of recovery of the odor-induced Ca2+ transients matches recovery from a short-term form of odor adaptation. Application of the membrane-permeant intracellular Ca2+ chelator BAPTA AM eliminates this odor adaptation. The results indicate that an olfactory cilium serves as a basic functional unit at the input level of the olfactory system, controlling both the specificity and sensitivity of odor detection.
Department of Anatomy and Neurobiology, University of Maryland, Baltimore, Maryland 21201, USA.
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Leinders-Zufall
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Greer
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Shepherd
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Zufall
D000222:Adaptation, Physiological; D000557:Ambystoma; D000818:Animals; D002118:Calcium / Q000378:metabolism*; D002923:Cilia / Q000187:drug effects / Q000378:metabolism; D004791:Enzyme Inhibitors / Q000494:pharmacology; D007091:Image Processing, Computer-Assisted; D018613:Microscopy, Confocal; D009812:Odorants; D018034:Olfactory Receptor Neurons / Q000187:drug effects / Q000378:metabolism* / Q000648:ultrastructure; D015398:Signal Transduction / Q000187:drug effects / Q000502:physiology*
D004791:Enzyme Inhibitors; D002118:Calcium