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Science 320 (5873): 201-205

Copyright © 2008 by the American Association for the Advancement of Science

Surface Mobility of Postsynaptic AMPARs Tunes Synaptic Transmission

Martin Heine,1* Laurent Groc,1 Renato Frischknecht,4 Jean-Claude Béïque,3 Brahim Lounis,2 Gavin Rumbaugh,3 Richard L. Huganir,3 Laurent Cognet,2 Daniel Choquet1{dagger}

Abstract: AMPA glutamate receptors (AMPARs) mediate fast excitatory synaptic transmission. Upon fast consecutive synaptic stimulation, transmission can be depressed. Recuperation from fast synaptic depression has been attributed solely to recovery of transmitter release and/or AMPAR desensitization. We show that AMPAR lateral diffusion, observed in both intact hippocampi and cultured neurons, allows fast exchange of desensitized receptors with naïve functional ones within or near the postsynaptic density. Recovery from depression in the tens of millisecond time range can be explained in part by this fast receptor exchange. Preventing AMPAR surface movements through cross-linking, endogenous clustering, or calcium rise all slow recovery from depression. Physiological regulation of postsynaptic receptor mobility affects the fidelity of synaptic transmission by shaping the frequency dependence of synaptic responses.

1 CNRS, UMR 5091, Université Bordeaux, Bordeaux, France.
2 Centre de Physique Moleculaire Optique et Hertzienne, CNRS, UMR 5798, Université Bordeaux, Talence, France.
3 Department of Neuroscience, Johns Hopkins University, Baltimore, MD, USA.
4 Leibniz Institut für Neurobiologie, Magdeburg, Germany.

* Present address: Leibniz Institut für Neurobiologie, Magdeburg, Germany.

{dagger} To whom correspondence should be addressed: dchoquet{at}u-bordeaux2.fr


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   Abstract »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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S. Tomita (2010)
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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E. Tarusawa, K. Matsui, T. Budisantoso, E. Molnar, M. Watanabe, M. Matsui, Y. Fukazawa, and R. Shigemoto (2009)
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Full Text »    PDF »
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   Abstract »    Full Text »    PDF »

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