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Volume 17, Number 5, Issue of March 1, 1997 pp. 1701-1709
Copyright ©1997 Society for Neuroscience

Rapid Coupling of Calcium Release to Depolarization in Limulus polyphemus Ventral Photoreceptors as Revealed by Microphotolysis and Confocal Microscopy

Received Sept. 3, 1996; revised Dec. 20, 1996; accepted Dec. 23, 1996.

Kyrill Ukhanov and Richard Payne

Department of Zoology, University of Maryland, College Park, Maryland 20742

Microphotolysis and confocal microscopy were used to investigate the timing of calcium release and of the electrical response in Limulus polyphemus ventral photoreceptors. The fluorescent dyes Fluo-3 and Calcium Green-5N were used to monitor local Ca²⁺ elevations. Photolysis of caged inositol trisphosphate (InsP₃) close to the plasma membrane of the light-sensitive rhabdomeral (R-) lobe resulted in Ca²⁺ elevation within 10-20 msec, 20-45 msec before the physiological response to light normally would be detected. Inward ionic current flow and depolarization followed InsP₃-induced calcium release within 2.5 ± 3.3 msec. Voltage-clamping the cells and removal of extracellular Ca²⁺ did not affect the timing of the Ca²⁺ elevation that followed the photolysis of caged InsP₃ or its relationship to the electrical response. In contrast to the physiological response to light, which only released calcium within the R-lobe, photolysis of InsP₃ elevated Ca_i in both lobes, although with much greater effect in the R-lobe, as compared with the bulk of the A-lobe, suggesting the presence of InsP₃-sensitive calcium stores in both lobes. Photolysis of caged calcium [o-nitrophenyl EGTA (NPE)] at the edge of the R-lobe activated an inward ionic current within 1.8 ± 0.7 msec. This NPE-induced current reversed at a membrane potential of 10 ± 6 mV in the range typical of that of the light-activated current under physiological conditions. Calcium release, therefore, activates an inward current rapidly enough to contribute to the electrical response to light.

Key words: phototransduction; Limulus polyphemus; photoreceptor; nitrophenyl EGTA (NPE); caged InsP₃; confocal microscopy

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