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The Journal of Neuroscience, March 19, 2008, 28(12):3150-3158; doi:10.1523/JNEUROSCI.5753-07.2008

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Cellular/Molecular
Mobility and Turnover of Vesicles at the Synaptic Ribbon

Lisamarie LoGiudice,^1,2 Peter Sterling,³ and Gary Matthews¹

¹Department of Neurobiology and Behavior and ²Graduate Program in Neuroscience, State University of New York, Stony Brook, Stony Brook, New York 11794-5230, and ³Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104

Correspondence should be addressed to Gary Matthews, Department of Neurobiology and Behavior, Life Sciences 550, State University of New York, Stony Brook, Stony Brook, NY 11794-5230. Email: gary.g.matthews{at}sunysb.edu

Ribbon synapses release neurotransmitter continuously at high rates, and the ribbons tether a large pool of synaptic vesicles. To determine whether the tethered vesicles are actually released, we tracked vesicles labeled with styryl dye in mouse retinal bipolar cell terminals whose ribbons had been labeled with a fluorescent peptide. We photobleached vesicles in regions with ribbons and without them and then followed recovery of fluorescence as bleached regions were repopulated by labeled vesicles. In the resting terminal, fluorescence recovered by 50% in non-ribbon regions but by only 20% at ribbons. Thus, at rest, vesicles associated with ribbons cannot exchange freely with cytoplasmic vesicles. Depolarization stimulated vesicle turnover at ribbons as bleached, immobile vesicles were released by exocytosis and were then replaced by fluorescent vesicles from the cytoplasm, producing an additional increase in fluorescence specifically at the ribbon location. We conclude that vesicles immobilized at synaptic ribbons participate in the readily releasable pool that is tapped rapidly during depolarization.

Key words: retina; ribbon synapse; retinal bipolar cell; synaptic transmission; exocytosis; neurotransmitter release

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Received Aug. 26, 2007; revised Jan. 29, 2008; accepted Feb. 2, 2008.

Correspondence should be addressed to Gary Matthews, Department of Neurobiology and Behavior, Life Sciences 550, State University of New York, Stony Brook, Stony Brook, NY 11794-5230. Email: gary.g.matthews{at}sunysb.edu

This article has been cited by other articles:

				L. LoGiudice and G. Matthews The Role of Ribbons at Sensory Synapses Neuroscientist, August 1, 2009; 15(4): 380 - 391. [Abstract] [PDF]

				K. Reim, H. Regus-Leidig, J. Ammermuller, A. El-Kordi, K. Radyushkin, H. Ehrenreich, J. H. Brandstatter, and N. Brose Aberrant function and structure of retinal ribbon synapses in the absence of complexin 3 and complexin 4 J. Cell Sci., May 1, 2009; 122(9): 1352 - 1361. [Abstract] [Full Text] [PDF]

				M. Coggins and D. Zenisek Evidence that Exocytosis Is Driven by Calcium Entry Through Multiple Calcium Channels in Goldfish Retinal Bipolar Cells J Neurophysiol, May 1, 2009; 101(5): 2601 - 2619. [Abstract] [Full Text] [PDF]

				G. Matthews and P. Sterling Evidence That Vesicles Undergo Compound Fusion on the Synaptic Ribbon J. Neurosci., May 21, 2008; 28(21): 5403 - 5411. [Abstract] [Full Text] [PDF]

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