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The Journal of Neuroscience, July 2, 2003, 23(13):5936-5944

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Long-Term Depression of Presynaptic Release from the Readily Releasable Vesicle Pool Induced by NMDA Receptor-Dependent Retrograde Nitric Oxide

Patric K. Stanton,¹ Jochen Winterer,² Christopher P. Bailey,¹ Andreas Kyrozis,¹ Ivan Raginov,² Gregor Laube,³ Rüdiger W. Veh,³ Can Q. Nguyen,¹ and Wolfgang Müller²

¹Departments of Neuroscience and Neurology, Albert Einstein College of Medicine, Bronx, New York 10461, and ²Neuroscience Research Institute and ³Institute for Anatomy, Charité, Humboldt University, Berlin, D-10117, Germany

Postsynaptic alterations are currently believed to be able to fully account for NMDA-receptor-dependent long-term depression (LTD) and long-term potentiation of synaptic strength, although there is also evidence supporting changes in presynaptic release. Using dualphoton laser scan microscopy of N-(3-triethylammoniumpropyl)-4-(4-(dibutylamino)styryl) pyridinium dibromide (FM1-43) to directly visualize presynaptic vesicular release at Schaffer collateral–CA1 excitatory synapses in hippocampal slices, we demonstrate reduced vesicular release associated with LTD. Selective loading, by hypertonic shock, of the readily releasable vesicle pool (RRP) showed that LTD of release is a selective modification of release from the RRP. Presynaptic LTD of RRP release required activation of NMDA receptors, production and extracellular diffusion of the intercellular messenger NO, and activation of cGMP-dependent protein kinase.

Key words: CA1; cGMP; hippocampus; long-term depression; nitric oxide; presynaptic; readily releasable vesicle pool; Schaffer collateral; PKG; transmitter release

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Received Mar. 11, 2003; revised Mar. 11, 2003; accepted Apr. 18, 2003.

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