Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals

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Abstract
Communication among neurons occurs at specialized synaptic junctions, where neurotransmitter is released via calcium-dependent exocytosis from the synaptic terminal of the presynaptic cell onto the postsynaptic target neuron. Here we exploit the unique properties of giant synaptic terminals of bipolar neurons from goldfish retina to establish the kinetics and calcium-dependence of exocytosis, and the characteristics of membrane retrieval following secretion in presynaptic terminals. Simultaneous patch-clamp, calcium-indicator dye and time-resolved capacitance measurements reveal that activation of calcium current drives secretion at a rapid rate of about 10,000 vesicles per s and the calcium level necessary to drive secretion is locally greater than 50 microM. Two components of membrane retrieval were observed following secretory stimulation. After strong stimulation, capacitance returned to rest with a time constant of about 30 s, but after weaker stimuli recovery was much faster, with a time constant of about 2 s. Secretion in a vertebrate central nervous system neuron was thus found to differ substantially from that in other secretory cells in its rapid rate of vesicle fusion, requirement for high levels of intracellular calcium, and the high speed and completeness of membrane retrieval. These distinctive features reflect the specialization of neuronal synaptic terminals for rapid and focally directed release of neurotransmitter.