Calcium concentration changes during sensory transduction in spider mechanoreceptor neurons

ABSTRACT

Most mechanoreceptor neurons encode mechanical signals into action potential trains within the same cell. Evidence suggests that intracellular calcium ion concentration, [Ca²⁺], increases during mechanotransduction, either by direct entry through mechanically activated channels or indirectly through voltage-activated calcium channels. However, little is known about the amounts of calcium involved or its roles in mechanotransduction. We estimated [Ca²⁺] in mechanoreceptor neurons of the spider, Cupiennius salei, during mechanical stimulation using Oregon Green BAPTA-1, and a single-compartment model of [Ca²⁺] as a function of action potential firing rate. Resting [Ca²⁺] was approximately 400 nm and increased to up to 2 µm at 30 action potentials/s. Similar levels of resting and stimulated [Ca²⁺] were obtained in the cell soma, axon and two parts of the sensory dendrite, including the region immediately adjacent to the site of sensory transduction. The time constant of rise and fall of [Ca²⁺] was 1–5 s in the dendrite and axon, but up to 15 s in the soma. Calcium elevation was dependent on action potentials and could not be induced by the receptor potential alone. Blockade of voltage-activated calcium channels by nickel ions prevented calcium increase, but thapsigargin, which empties intracellular calcium stores, had no effect. Estimates of calcium entry per action potential from fluorescence changes agreed approximately with estimates based on action potential voltage–time profile and previous reports of calcium channel properties. This first report of calcium levels during transduction in spiking mechanoreceptors suggests that calcium signaling plays important roles in primary somatosensory neurons.