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The distribution of exocytic sites and ion channels in the synaptic terminal of retinal bipolar cells was investigated by measuring capacitance and conductance changes in cell-attached patches of presynaptic membrane. Patch depolarization evoked capacitance and conductance increases that were inhibited by blocking Ca2+ influx or loading the terminal with EGTA. The increase in capacitance declined as the depolarization approached the reversal potential for Ca2+, indicating that it was a result of Ca2+-dependent exocytosis. The conductance increase was caused by KCa channels that were also activated by Ca2+ influx. Two observations indicated that sites of exocytosis and endocytosis colocalized with clusters of Ca2+ channels and KCachannels; the initial rate of exocytosis was correlated with the activation of KCa channels, and exocytosis did not occur in the 41% of patches lacking this conductance. Electron microscopy demonstrated that there were ∼16 vesicles docked to the plasma membrane at each active zone marked by a ribbon, but vesicles were also attached to the rest of the membrane at a density of 1.5/μm2. The density of ribbons was 0.10 ± 0.02/μm2, predicting that ∼43% of cell-attached patches would lack an active zone. The density of Ca2+ channel clusters assayed by capacitance and conductance responses was therefore similar to the density of ribbons. These results are consistent with the idea that Ca2+channel clusters were colocalized with ribbons but do not exclude the possibility that calcium channels also occurred at other sites. The wide distribution of vesicles docked to the plasma membrane suggests that exocytosis might also be triggered by the spread of Ca2+ from Ca2+ channel clusters.

Exocytosis at the Ribbon Synapse of Retinal Bipolar Cells Studied in Patches of Presynaptic Membrane