Amplification of odor-induced Ca(2+) transients by store-operated Ca(2+) release and its role in olfactory signal transduction.
A critical role of Ca(2+) in vertebrate olfactory receptor neurons (ORNs) is to couple odor-induced excitation to intracellular feedback pathways that are responsible for the regulation of the sensitivity of the sense of smell, but the role of intracellular Ca(2+) stores in this process remains unclear. Using confocal Ca(2+) imaging and perforated patch recording, we show that salamander ORNs contain a releasable pool of Ca(2+) that can be discharged at rest by the SERCA inhibitor thapsigargin and the ryanodine receptor agonist caffeine. The Ca(2+) stores are spatially restricted; emptying produces compartmentalized Ca(2+) release and capacitative-like Ca(2+) entry in the dendrite and soma but not in the cilia, the site of odor transduction. We deplete the stores to show that odor stimulation causes store-dependent Ca(2+) mobilization. This odor-induced Ca(2+) release does not seem to be necessary for generation of an immediate electrophysiological response, nor does it contribute significantly to the Ca(2+) transients in the olfactory cilia. Rather, it is important for amplifying the magnitude and duration of Ca(2+) transients in the dendrite and soma and is thus necessary for the spread of an odor-induced Ca(2+) wave from the cilia to the soma. We show that this amplification process depends on Ca(2+)-induced Ca(2+) release. The results indicate that stimulation of ORNs with odorants can produce Ca(2+) mobilization from intracellular stores without an immediate effect on the receptor potential. Odor-induced, store-dependent Ca(2+) mobilization may be part of a feedback pathway by which information is transferred from the distal dendrite of an ORN to its soma.
Zufall
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Department of Anatomy, Program in Neuroscience, University of Maryland, Baltimore, Maryland 21201, USA.
Leinders-Zufall
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Greer
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D000818:Animals; D002110:Caffeine / Q000494:pharmacology; D002118:Calcium / Q000502:physiology*; D002135:Calcium-Binding Proteins / Q000187:drug effects / Q000502:physiology*; D002923:Cilia / Q000187:drug effects / Q000502:physiology*; D003511:Cyclohexanols; D003712:Dendrites / Q000187:drug effects / Q000502:physiology; D004533:Egtazic Acid / Q000494:pharmacology; D000077591:Eucalyptol; D066298:In Vitro Techniques; D008610:Menthol / Q000031:analogs & derivatives / Q000494:pharmacology; D008959:Models, Neurological; D039821:Monoterpenes; D009812:Odorants; D009833:Olfactory Pathways / Q000502:physiology*; D018034:Olfactory Receptor Neurons / Q000187:drug effects / Q000502:physiology*; D018408:Patch-Clamp Techniques; D015398:Signal Transduction / Q000502:physiology; D012997:Solvents; D013729:Terpenes; D019284:Thapsigargin / Q000494:pharmacology; D014562:Caudata
D002135:Calcium-Binding Proteins; D003511:Cyclohexanols; D039821:Monoterpenes; D012997:Solvents; D013729:Terpenes; D008610:Menthol; D002110:Caffeine; D004533:Egtazic Acid; D019284:Thapsigargin; D000077591:Eucalyptol; D002118:Calcium