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The Journal of Neuroscience, August 1, 2002, 22(15):6336-6346

Multimodal Quantal Release at Individual Hippocampal Synapses: Evidence for No Lateral Inhibition

Alessandra Abenavoli¹, Lia Forti¹, Mario Bossi², Andrea Bergamaschi¹, Antonello Villa², and Antonio Malgaroli¹

¹ Unit of Neurobiology, Università Vita-Salute San Raffaele, Milan, Italy 20132, and ² Microscopy and Image Analysis Center, Medical School University Bicocca, Milan, Italy 20052

Most CNS synapses investigated thus far contain a large number of vesicles docked at the active zone, possibly forming individual release sites. At the present time, it is unclear whether these vesicles can be discharged independently of one another. To investigate this problem, we recorded miniature excitatory currents by whole-cell and single-synapse recordings from CA3-CA1 hippocampal neurons and analyzed their stochastic properties. In addition, spontaneous release was investigated by ultrastructural analysis of quickly frozen synapses, revealing vesicle intermediates in docking and spontaneous fusion states. In these experiments, no signs of inhibitory interactions between quanta could be detected up to 1 msec from the previous discharge. This suggests that exocytosis at one site does not per se inhibit vesicular fusion at neighboring sites. At longer intervals, the output of quanta diverged from a random memoryless Poisson process because of the presence of a bursting component. The latter, which could not be accounted for by random coincidences, was independent of Ca²⁺ elevations in the cytosol, whether from Ca²⁺ flux through the plasma membrane or release from internal stores. Results of these experiments, together with the observation of spontaneous pairs of omega profiles at the active zone, suggest that multimodal release is produced by an enduring activation of an integrated cluster of release sites.

Key words: central synapses; exocytosis; miniature excitatory currents; stochastic properties; multivesicular release; hippocampus

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Copyright © 2002 Society for Neuroscience  0270-6474/02/22156336-11$05.00/0

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