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Properties of Exocytotic Response in Vertebrate Photoreceptors

M. Kreft^1,2,*, D. Kriaj^3,*, S. Grilc¹ and R. Zorec^1,2

¹Laboratory Neuroendocrinology-Molecular Cell Physiology, Institute of Pathophysiology, Medical Faculty, Zaloka 4, and ²Celica Biomedical Sciences Center, Stegne 21, 1000 Ljubljana, Slovenia; and ³Departments of Ophthalmology and Physiology, University of California School of Medicine, San Francisco, California 94143-0730

Submitted 13 November 2002; accepted in final form 19 March 2003

Synaptic transmission at the photoreceptor synapse is characterized by continuous release of glutamate in darkness. Release is regulated by the intracellular calcium concentration ([Ca²⁺]_i). We here examined the physiological properties of exocytosis in tiger salamander (Ambystoma tigrinum) retinal rods and cones. Patch-clamp capacitance measurements were used to monitor exocytosis elicited by a rapid and uniform increase in [Ca²⁺]_i by photolysis of the caged Ca²⁺ compound NP-EGTA. The amplitude of flash-induced increases in membrane capacitance (C_m) varied monotonically with [Ca²⁺]_i beyond approximately 15 µM. The following two types of kinetic responses in C_m were recorded in both rods and cones: 1) a single exponential rise (39% of cells) or 2) a double-exponential rise (61%). Average rate constants of rapid and slow exocytotic responses were 420 ± 168 and 7.85 ± 5.02 s^–1, respectively. The rate constant for the single exponential exocytotic response was 17.5 ± 12.4 s^–1, not significantly different from that of the slow exocytotic response. Beyond the threshold [Ca²⁺]_i of approximately 15 µM, the average amplitude of rapid, slow, and single C_m response were 0.84 ± 0.35, 0.82 ± 0.20, and 0.70 ± 0.23 pF, respectively. Antibodies against synaptotagmin I, a vesicle protein associated with fast exocytosis, strongly stained the synaptic terminal of isolated photoreceptors, suggesting the presence of fusion-competent vesicles. Our results confirm that photoreceptors possess a large rapidly releasable pool activated by a low-affinity Ca²⁺ sensor whose kinetic and calcium-dependent properties are similar to those reported in retinal bipolar cells and cochlear hair cells.

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