Evidence That Vesicles on the Synaptic Ribbon of Retinal Bipolar Neurons Can Be Rapidly Released

We relate the ultrastructure of the giant bipolar synapse in goldfish retina to the jump in capacitance that accompanies depolarization-evoked exocytosis. Mean vesicle diameter is 29 +/- 4 nm, giving 26.4 aF/vesicle, so the maximum evoked capacitance (150 fF within 200 ms) represents fusion of about 5700 vesicles. Two terminals contained, respectively, 45 and 65 ribbon-type synaptic outputs, and a fully loaded ribbon tethers about 110 vesicles. Thus, the tethered pool, about 6000 vesicles, corresponds to the rapidly released pool. Further, the difference between small and large terminals in number of tethered vesicles matches their difference in capacitance jump. This suggests, within a "fire and reload" model of exocytosis, that the ribbon translocates synaptic vesicles very rapidly to membrane docking sites, supporting a maximum release rate of 500 vesicles/active zone/s, until the population of tethered vesicles is exhausted.