Continuous and transient vesicle cycling at a ribbon synapse

Optical methods were used to study the Ca2+ dependence of vesicle cycling in bipolar cells isolated from goldfish retinas. Uniformly raising the Ca2+ concentration to between 0.8 and 20 microM produced a continuous vesicle cycle of balanced exocytosis and endocytosis with a maximum rate equivalent to the turnover of the entire surface membrane of a terminal every 2 min (or approximately 900 vesicles sec-1). Increasing the Ca2+ concentration above 20 microM inhibited continuous vesicle cycling. In contrast, influx of Ca2+ through voltage-gated channels produced a transient burst of exocytosis that increased the surface area of a terminal by a maximum of 12% (equivalent to the addition of 13,000 vesicles). Endocytosis was delayed until after Ca2+ influx stopped and the average Ca2+ concentration in the terminal declined. Hence, a single terminal has mechanisms for both continuous and transient vesicle cycling.