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The Journal of Neuroscience, January 25, 2006, 26(4):1239-1246; doi:10.1523/JNEUROSCI.3553-05.2006

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Cellular/Molecular
Rab3 Superprimes Synaptic Vesicles for Release: Implications for Short-Term Synaptic Plasticity

Oliver M. Schlüter,^2,3 Jayeeta Basu,^1,2 Thomas C. Südhof,⁴ and Christian Rosenmund^1,2

¹Departments of Neuroscience and Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas 77030, Max-Planck-Institute for ²Biophysical Chemistry and ³Experimental Medicine, 37075 Göttingen, Germany, and ⁴Center for Basic Neuroscience, Department of Molecular Genetics, and Howard Hughes Medical Institute, The University of Texas Southwestern Medical Center, Dallas, Texas 75390-9111

Correspondence should be addressed to either of the following: Christian Rosenmund, Departments of Neuroscience and Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Room 833E, Houston, TX 77030, Email: rosenmun{at}bcm.tmc.edu; or Oliver M. Schlüter, Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA 94305, oschlue{at}stanford.edu

Presynaptic vesicle trafficking and priming are important steps in regulating synaptic transmission and plasticity. The four closely related small GTP-binding proteins Rab3A, Rab3B, Rab3C, and Rab3D are believed to be important for these steps. In mice, the complete absence of all Rab3s leads to perinatal lethality accompanied by a 30% reduction of probability of Ca²⁺-triggered synaptic release. This study examines the role of Rab3 during Ca²⁺-triggered release in more detail and identifies its impact on short-term plasticity. Using patch-clamp electrophysiology of autaptic neuronal cultures from Rab3-deficient mouse hippocampus, we show that excitatory Rab3-deficient neurons display unique time- and frequency-dependent short-term plasticity characteristics in response to spike trains. Analysis of vesicle release and repriming kinetics as well as Ca²⁺ sensitivity of release indicate that Rab3 acts on a subset of primed, fusion competent vesicles. They lower the amount of Ca²⁺ required for action potential-triggered release, which leads to a boosting of release probability, but their action also introduces a significant delay in the supply of these modified vesicles. As a result, Rab3-induced modifications to primed vesicles causes a transient increase in the transduction efficacy of synaptic action potential trains and optimizes the encoding of synaptic information at an intermediate spike frequency range.

Key words: synaptic transmission; hippocampus; exocytosis; vesicle trafficking; release probability; GTP binding proteins

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Received Aug. 22, 2005; revised Dec. 3, 2005; accepted Dec. 5, 2005.

Correspondence should be addressed to either of the following: Christian Rosenmund, Departments of Neuroscience and Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Room 833E, Houston, TX 77030, Email: rosenmun{at}bcm.tmc.edu; or Oliver M. Schlüter, Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA 94305, oschlue{at}stanford.edu

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