Two Actions of Calcium Regulate the Supply of Releasable Vesicles at the Ribbon Synapse of Retinal Bipolar Cells

Ribbon synapses of sensory neurons are able to sustain high rates of exocytosis in response to maintained depolarization, but it is not known how this is achieved. Using the capacitance technique, we have found that Ca2+ regulates the supply of releasable vesicles at the ribbon synapse of depolarizing bipolar cells from the retina of goldfish. Ca2+ had two actions that could be differentiated by introduction of the Ca2+chelator EGTA; one action stimulated refilling of the rapidly releasable pool of vesicles from a reserve pool, and a second action stimulated recruitment of vesicles to the reserve pool. The capacity of the reserve pool was ∼3500 vesicles, which is similar to the number that can attach to the ribbons. These results suggest that continuous exocytosis at ribbon synapses is maintained by the Ca2+-dependent translocation of vesicles from the cytoplasm, through the ribbon, to release sites on the plasma membrane.