Vesicle association and exocytosis at ribbon and extraribbon sites in retinal bipolar cell presynaptic terminals

Synaptic vesicles release neurotransmitter by following a process of vesicle docking and exocytosis. Although these steps are well established, it has been difficult to observe and measure these rates directly in living synapses. Here, by combining the direct imaging of single synaptic vesicles and synaptic ribbons, I measure the properties of vesicle docking and evoked and spontaneous release from ribbon and extraribbon locations in a ribbon-type synaptic terminal, the goldfish retinal bipolar cell. In the absence of a stimulus, captured vesicles near ribbons associate tightly and only rarely undock or undergo spontaneous exocytosis. By contrast, vesicle capture at outlier sites is less stable and spontaneous exocytosis occurs at a higher rate. In response to a stimulus, exocytic events cluster near ribbons, but show no evidence of clustering away from ribbon sites. Together, the results here indicate that, although vesicles can associate and fuse both near and away from synaptic sites, vesicles at synaptic ribbons associate more stably and fusion is more tightly linked to stimuli.