Abstract
Synaptic vesicles can be released at extremely high rates, which places an extraordinary demand on the recycling machinery. Previous ultrastructural studies of vesicle recycling were conducted in dissected preparations using an intense stimulation to maximize the probability of release. Here, a single light stimulus was applied to motor neurons in intact Caenorhabditis elegans nematodes expressing channelrhodopsin, and the animals rapidly frozen. We found that docked vesicles fuse along a broad active zone in response to a single stimulus, and are replenished with a time constant of about 2 s. Endocytosis occurs within 50 ms adjacent to the dense projection and after 1 s adjacent to adherens junctions. These studies suggest that synaptic vesicle endocytosis may occur on a millisecond time scale following a single physiological stimulus in the intact nervous system and is unlikely to conform to current models of endocytosis. DOI:http://dx.doi.org/10.7554/eLife.00723.001.
Highlights
Synaptic transmission is quantal—postsynaptic responses have a uniform minimal size (Fatt and Katz, 1952)
Two major models for synaptic vesicle endocytosis have emerged from studies of ultrastructure: clathrinmediated endocytosis and kiss-and-run endocytosis
Clathrin-mediated endocytosis predicts that vesicles collapse into the membrane and are recovered slowly at a specialized site lateral to the active zone
Summary
Synaptic transmission is quantal—postsynaptic responses have a uniform minimal size (Fatt and Katz, 1952). It was noted that synaptic vesicles were depleted from the terminals, suggesting that vesicles were being consumed during synaptic transmission (Ceccarelli et al, 1972, 1973; Heuser and Reese, 1973). Later it was found by Heuser and Reese that if the synapses were rapidly frozen after single stimulus that vesicles could be observed fusing to the plasma membrane (Heuser and Reese, 1981). Torri-Tarelli et al demonstrated that the timing of vesicle fusion coincided precisely with that of transmitter release (Torri-Tarelli et al, 1985).
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