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The Journal of Neuroscience, August 6, 2003, 23(18):7059-7068

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Presynaptic Capacitance Measurements and Ca²⁺ Uncaging Reveal Submillisecond Exocytosis Kinetics and Characterize the Ca²⁺ Sensitivity of Vesicle Pool Depletion at a Fast CNS Synapse

Markus Wölfel and Ralf Schneggenburger

Arbeitsgruppe Synaptische Dynamik und Modulation and Abteilung Membranbiophysik, Max-Planck-Institut für Biophysikalische Chemie, D-37077 Göttingen, Germany

The intracellular Ca²⁺ sensitivity of synaptic vesicle fusion is an important determinant of transmitter release probability, but it is unknown for most CNS synapses. We combined whole-cell membrane capacitance measurements and Ca²⁺ uncaging at the large calyx of Held nerve terminals to determine the Ca²⁺ sensitivity of synaptic vesicle fusion at a glutamatergic CNS synapse, independent of recording EPSCs. Capacitance increases measured 30-50 msec after elevating the intracellular Ca²⁺ concentration ([Ca²⁺]_i) by Ca²⁺ uncaging were half-maximal at 5 µM [Ca²⁺]_i. At 10 µM [Ca²⁺]_i, capacitance increases reached maximal values (256 ± 125 fF; mean ± SD), indicating the depletion of an average pool of 4000 readily releasable vesicles. Vesicle pool depletion was confirmed in cross-depletion experiments, in which capacitance responses were measured after Ca²⁺ uncaging, or after combined stimuli of prolonged presynaptic depolarizations and Ca²⁺ uncaging. To analyze the Ca²⁺-dependent rates of vesicle pool depletion, the capacitance rise after Ca²⁺ uncaging was fitted with single- or double-exponential functions. The fast time constants of double-exponential fits, and the time constants of single-exponential fits were 2-3 msec at 10-15 µM [Ca²⁺]_i and reached submillisecond values at 30 µM [Ca²⁺]_i. These results suggest that three to five readily releasable vesicles can fuse within <1 msec at each active zone of a calyx of Held, given that [Ca²⁺]_i rises sufficiently high. Submillisecond kinetics of exocytosis are reached at significantly lower [Ca²⁺]_i than at ribbon-type sensory synapses previously investigated by capacitance measurements.

Key words: synaptic transmission; vesicle fusion; readily releasable pool; release probability; calcium sensitivity; Synaptotagmin

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Received Apr. 11, 2003; revised Jun. 6, 2003; accepted Jun. 11, 2003.

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