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The Journal of Neuroscience, February 20, 2008, 28(8):1894-1903; doi:10.1523/JNEUROSCI.4518-07.2008

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Cellular/Molecular
Release of the Styryl Dyes from Single Synaptic Vesicles in Hippocampal Neurons

Xi Chen,¹ Sebastian Barg,² and Wolfhard Almers¹

¹Vollum Institute, Oregon Health & Sciences University, Portland, Oregon 97239, and ²Department of Cell Biology, Division of Medicine, Sir Alexander Fleming Building, Imperial College London, London SW7 2AZ, United Kingdom

Correspondence should be addressed to Wolfhard Almers, Vollum Institute, Oregon Health & Sciences University, 3181 Southwest Sam Jackson Park Road, Portland, OR 97239. Email: almersw{at}ohsu.edu

In small presynaptic boutons in brain, synaptic vesicles are thought not to merge with the plasma membrane when they release transmitter, but instead to close their fusion pores and survive intact for future use (kiss-and-run exocytosis). The strongest evidence for this idea is the slow and incomplete release of the fluorescent membrane marker, FM1-43 [N-(3-triethylammoniumpropyl)-4-(4-(dibutylamino)styryl) pyridinium dibromide], from single vesicles. We investigated the release of FM1-43 from sparse cultures of hippocampal neurons grown on coverslips with no glia. This allowed presynaptic boutons to be imaged at favorable signal-to-noise ratio. Sparingly stained boutons were imaged at high time resolution, while high-frequency electrical stimulation caused exocytosis. The release of FM1-43 was quantal and occurred in abrupt steps, each representing a single fusion event. The fluorescence of vesicle clusters traveling along axons had a distribution with the same quantal size, indicating that a vesicle releases all the dye it contains. In most fusion events, the time constant of dye release was <100 ms, and slower release was rarely observed. After exocytosis, no FM1-43 could be detected in the axon to either side of a bouton, indicating that dye was released before it could spread. Our results are consistent with synaptic vesicles fusing fully with the plasma membrane during high-frequency stimulation.

Key words: presynaptic terminal; quantal release; fluorescence microscopy; vesicle transport; kiss-and-run; hippocampus

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Received Oct. 3, 2007; revised Dec. 13, 2007; accepted Jan. 5, 2008.

Correspondence should be addressed to Wolfhard Almers, Vollum Institute, Oregon Health & Sciences University, 3181 Southwest Sam Jackson Park Road, Portland, OR 97239. Email: almersw{at}ohsu.edu

This article has been cited by other articles:

				J. A. Daniel, S. Galbraith, L. Iacovitti, A. Abdipranoto, and B. Vissel Functional Heterogeneity at Dopamine Release Sites J. Neurosci., November 18, 2009; 29(46): 14670 - 14680. [Abstract] [Full Text] [PDF]

				Q. Zhang, Y. Li, and R. W. Tsien The Dynamic Control of Kiss-And-Run and Vesicular Reuse Probed with Single Nanoparticles Science, March 13, 2009; 323(5920): 1448 - 1453. [Abstract] [Full Text] [PDF]

				B. Granseth and L. Lagnado The role of endocytosis in regulating the strength of hippocampal synapses J. Physiol., December 15, 2008; 586(24): 5969 - 5982. [Abstract] [Full Text] [PDF]

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