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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}

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J. P. Dupuis, L. Ladepeche, H. Seth, L. Bard, J. Varela, L. Mikasova, D. Bouchet, V. Rogemond, J. Honnorat, E. Hanse, et al. (2014)
EMBO J. 33, 842-861
   Abstract »    Full Text »    PDF »
Developmental switch in the kinase dependency of long-term potentiation depends on expression of GluA4 subunit-containing AMPA receptors.
N. V. Luchkina, J. Huupponen, V. R. J. Clarke, S. K. Coleman, K. Keinanen, T. Taira, and S. E. Lauri (2014)
PNAS 111, 4321-4326
   Abstract »    Full Text »    PDF »
A Novel Mechanism for Nicotinic Potentiation of Glutamatergic Synapses.
A. W. Halff, D. Gomez-Varela, D. John, and D. K. Berg (2014)
J. Neurosci. 34, 2051-2064
   Abstract »    Full Text »    PDF »
Dendritic Spines: The Locus of Structural and Functional Plasticity.
C. Sala and M. Segal (2014)
Physiol Rev 94, 141-188
   Abstract »    Full Text »    PDF »
The expression of long-term potentiation: reconciling the preists and the postivists.
M. J. MacDougall and A. Fine (2013)
Phil Trans R Soc B 369, 20130135
   Abstract »    Full Text »    PDF »
Moderate AMPA receptor clustering on the nanoscale can efficiently potentiate synaptic current.
L. P. Savtchenko and D. A. Rusakov (2013)
Phil Trans R Soc B 369, 20130167
   Abstract »    Full Text »    PDF »
Cell biology in neuroscience: The interplay between Hebbian and homeostatic synaptic plasticity.
N. Vitureira and Y. Goda (2013)
J. Cell Biol. 203, 175-186
   Abstract »    Full Text »    PDF »
Lateral Mobility of Presynaptic {alpha}7-Containing Nicotinic Receptors and Its Relevance for Glutamate Release.
D. Gomez-Varela and D. K. Berg (2013)
J. Neurosci. 33, 17062-17071
   Abstract »    Full Text »    PDF »
Exposure to cocaine regulates inhibitory synaptic transmission from the ventral tegmental area to the nucleus accumbens.
M. Ishikawa, M. Otaka, P. A. Neumann, Z. Wang, J. M. Cook, O. M. Schluter, Y. Dong, and Y. H. Huang (2013)
J. Physiol. 591, 4827-4841
   Abstract »    Full Text »    PDF »
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H. Nishimura, K. Ritchie, R. S. Kasai, M. Goto, N. Morone, H. Sugimura, K. Tanaka, I. Sase, A. Yoshimura, Y. Nakano, et al. (2013)
J. Cell Biol. 202, 967-983
   Abstract »    Full Text »    PDF »
Differential Subcellular Targeting of Glutamate Receptor Subtypes during Homeostatic Synaptic Plasticity.
C. Soares, K. F. H. Lee, W. Nassrallah, and J.-C. Beique (2013)
J. Neurosci. 33, 13547-13559
   Abstract »    Full Text »    PDF »
Super-Resolution Imaging Reveals That AMPA Receptors Inside Synapses Are Dynamically Organized in Nanodomains Regulated by PSD95.
D. Nair, E. Hosy, J. D. Petersen, A. Constals, G. Giannone, D. Choquet, and J.-B. Sibarita (2013)
J. Neurosci. 33, 13204-13224
   Abstract »    Full Text »    PDF »
Kainate Receptor Post-translational Modifications Differentially Regulate Association with 4.1N to Control Activity-dependent Receptor Endocytosis.
B. A. Copits and G. T. Swanson (2013)
J. Biol. Chem. 288, 8952-8965
   Abstract »    Full Text »    PDF »
Simultaneous Monitoring of Presynaptic Transmitter Release and Postsynaptic Receptor Trafficking Reveals an Enhancement of Presynaptic Activity in Metabotropic Glutamate Receptor-Mediated Long-Term Depression.
W. Xu, Y. C. Tse, F. A. Dobie, M. Baudry, A. M. Craig, T. P. Wong, and Y. T. Wang (2013)
J. Neurosci. 33, 5867-5877
   Abstract »    Full Text »    PDF »
A Noncanonical Postsynaptic Transport Route for a GPCR Belonging to the Serotonin Receptor Family.
T. Liebmann, M. Kruusmagi, N. Sourial-Bassillious, A. Bondar, P. Svenningsson, M. Flajolet, P. Greengard, L. Scott, H. Brismar, and A. Aperia (2012)
J. Neurosci. 32, 17998-18008
   Abstract »    Full Text »    PDF »
Glutamate Receptor 1 Phosphorylation at Serine 831 and 845 Modulates Seizure Susceptibility and Hippocampal Hyperexcitability after Early Life Seizures.
S. N. Rakhade, E. F. Fitzgerald, P. M. Klein, C. Zhou, H. Sun, R. L. Huganir, and F. E. Jensen (2012)
J. Neurosci. 32, 17800-17812
   Abstract »    Full Text »    PDF »
Heterogeneity of AMPA receptor trafficking and molecular interactions revealed by superresolution analysis of live cell imaging.
N. Hoze, D. Nair, E. Hosy, C. Sieben, S. Manley, A. Herrmann, J.-B. Sibarita, D. Choquet, and D. Holcman (2012)
PNAS 109, 17052-17057
   Abstract »    Full Text »    PDF »
Dendritic spines: from structure to in vivo function.
N. L. Rochefort and A. Konnerth (2012)
EMBO Rep. 13, 699-708
   Abstract »    Full Text »    PDF »
Regulation of presynaptic strength by controlling Ca2+ channel mobility: effects of cholesterol depletion on release at the cone ribbon synapse.
A. J. Mercer, R. J. Szalewski, S. L. Jackman, M. J. Van Hook, and W. B. Thoreson (2012)
J Neurophysiol 107, 3468-3478
   Abstract »    Full Text »    PDF »
Photochemical Inactivation Analysis of Temporal Dynamics of Postsynaptic Native AMPA Receptors in Hippocampal Slices.
H. Kamiya (2012)
J. Neurosci. 32, 6517-6524
   Abstract »    Full Text »    PDF »
Disrupted surface cross-talk between NMDA and Ephrin-B2 receptors in anti-NMDA encephalitis.
L. Mikasova, P. De Rossi, D. Bouchet, F. Georges, V. Rogemond, A. Didelot, C. Meissirel, J. Honnorat, and L. Groc (2012)
Brain 135, 1606-1621
   Abstract »    Full Text »    PDF »
CaMKII binding to GluN2B is critical during memory consolidation.
A. R. Halt, R. F. Dallapiazza, Y. Zhou, I. S. Stein, H. Qian, S. Juntti, S. Wojcik, N. Brose, A. J. Silva, and J. W. Hell (2012)
EMBO J. 31, 1203-1216
   Abstract »    Full Text »    PDF »
Selective and Sustained {alpha}-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid Receptor Activation in Cerebellum Induces Dystonia in Mice.
X. Fan, K. E. Hughes, H. A. Jinnah, and E. J. Hess (2012)
J. Pharmacol. Exp. Ther. 340, 733-741
   Abstract »    Full Text »    PDF »
Unified quantitative model of AMPA receptor trafficking at synapses.
K. Czondor, M. Mondin, M. Garcia, M. Heine, R. Frischknecht, D. Choquet, J.-B. Sibarita, and O. R. Thoumine (2012)
PNAS 109, 3522-3527
   Abstract »    Full Text »    PDF »
Mechanisms Underlying Signal Filtering at a Multisynapse Contact.
T. Budisantoso, K. Matsui, N. Kamasawa, Y. Fukazawa, and R. Shigemoto (2012)
J. Neurosci. 32, 2357-2376
   Abstract »    Full Text »    PDF »
Parasynaptic NMDA Receptor Signaling Couples Neuronal Glutamate Transporter Function to AMPA Receptor Synaptic Distribution and Stability.
L. A. Jarzylo and H.-Y. Man (2012)
J. Neurosci. 32, 2552-2563
   Abstract »    Full Text »    PDF »
New Insights Into Molecular Players Involved in Neurotransmitter Release.
P. Ariel and T. A. Ryan (2012)
Physiology 27, 15-24
   Abstract »    Full Text »    PDF »
Subsynaptic AMPA Receptor Distribution Is Acutely Regulated by Actin-Driven Reorganization of the Postsynaptic Density.
J. M. Kerr and T. A. Blanpied (2012)
J. Neurosci. 32, 658-673
   Abstract »    Full Text »    PDF »
Prestin in HEK cells is an obligate tetramer.
R. Hallworth and M. G. Nichols (2012)
J Neurophysiol 107, 5-11
   Abstract »    Full Text »    PDF »
Searching for Presynaptic NMDA Receptors in the Nucleus Accumbens.
Y. H. Huang, M. Ishikawa, B. R. Lee, N. Nakanishi, O. M. Schluter, and Y. Dong (2011)
J. Neurosci. 31, 18453-18463
   Abstract »    Full Text »    PDF »
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C. Ribrault, J. Reingruber, M. Petkovic, T. Galli, N. E. Ziv, D. Holcman, and A. Triller (2011)
J. Neurosci. 31, 17590-17602
   Abstract »    Full Text »    PDF »
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P. Michaluk, M. Wawrzyniak, P. Alot, M. Szczot, P. Wyrembek, K. Mercik, N. Medvedev, E. Wilczek, M. De Roo, W. Zuschratter, et al. (2011)
J. Cell Sci. 124, 3369-3380
   Abstract »    Full Text »    PDF »
Neurexin-Neuroligin Adhesions Capture Surface-Diffusing AMPA Receptors through PSD-95 Scaffolds.
M. Mondin, V. Labrousse, E. Hosy, M. Heine, B. Tessier, F. Levet, C. Poujol, C. Blanchet, D. Choquet, and O. Thoumine (2011)
J. Neurosci. 31, 13500-13515
   Abstract »    Full Text »    PDF »
Surface Traffic of Dendritic CaV1.2 Calcium Channels in Hippocampal Neurons.
V. Di Biase, P. Tuluc, M. Campiglio, G. J. Obermair, M. Heine, and B. E. Flucher (2011)
J. Neurosci. 31, 13682-13694
   Abstract »    Full Text »    PDF »
The neuronal K-Cl cotransporter KCC2 influences postsynaptic AMPA receptor content and lateral diffusion in dendritic spines.
G. Gauvain, I. Chamma, Q. Chevy, C. Cabezas, T. Irinopoulou, N. Bodrug, M. Carnaud, S. Levi, and J. C. Poncer (2011)
PNAS 108, 15474-15479
   Abstract »    Full Text »    PDF »
Rapid Active Zone Remodeling during Synaptic Plasticity.
A. Weyhersmuller, S. Hallermann, N. Wagner, and J. Eilers (2011)
J. Neurosci. 31, 6041-6052
   Abstract »    Full Text »    PDF »
CB1 modulation of temporally distinct synaptic facilitation among local circuit interneurons mediated by N-type calcium channels in CA1.
A. B. Ali (2011)
J Neurophysiol 105, 1051-1062
   Abstract »    Full Text »    PDF »
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S. Levi, M. Dahan, and A. Triller (2011)
Cold Spring Harb Protoc 2011, prot5580
   Abstract »    Full Text »    PDF »
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R. L. Stornetta and J. J. Zhu (2011)
Neuroscientist 17, 54-78
   Abstract »    PDF »
Synaptic targeting of AMPA receptors is regulated by a CaMKII site in the first intracellular loop of GluA1.
W. Lu, K. Isozaki, K. W. Roche, and R. A. Nicoll (2010)
PNAS 107, 22266-22271
   Abstract »    Full Text »    PDF »
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M. V. Schmidt, D. Trumbach, P. Weber, K. Wagner, S. H. Scharf, C. Liebl, N. Datson, C. Namendorf, T. Gerlach, C. Kuhne, et al. (2010)
J. Neurosci. 30, 16949-16958
   Abstract »    Full Text »    PDF »
A Novel Form of Presynaptic Plasticity Based on the Fast Reactivation of Release Sites Switched Off during Low-Frequency Depression.
F. Doussau, Y. Humeau, F. Benfenati, and B. Poulain (2010)
J. Neurosci. 30, 16679-16691
   Abstract »    Full Text »    PDF »
Auditory Nerve Fibers Excite Targets Through Synapses That Vary in Convergence, Strength, and Short-Term Plasticity.
X.-J. Cao and D. Oertel (2010)
J Neurophysiol 104, 2308-2320
   Abstract »    Full Text »    PDF »
AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK-dependent manner during long-term potentiation.
M. A. Patterson, E. M. Szatmari, and R. Yasuda (2010)
PNAS 107, 15951-15956
   Abstract »    Full Text »    PDF »
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C. C. Fernandes, D. K. Berg, and D. Gomez-Varela (2010)
J. Neurosci. 30, 8841-8851
   Abstract »    Full Text »    PDF »
Learning, AMPA receptor mobility and synaptic plasticity depend on n-cofilin-mediated actin dynamics.
M. B. Rust, C. B. Gurniak, M. Renner, H. Vara, L. Morando, A. Gorlich, M. Sassoe-Pognetto, M. A. Banchaabouchi, M. Giustetto, A. Triller, et al. (2010)
EMBO J. 29, 1889-1902
   Abstract »    Full Text »    PDF »
AMPA receptor desensitization mutation results in severe developmental phenotypes and early postnatal lethality.
L. A. Christie, T. A. Russell, J. Xu, L. Wood, G. M. G. Shepherd, and A. Contractor (2010)
PNAS 107, 9412-9417
   Abstract »    Full Text »    PDF »
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M. Sun, J. C. Gewirtz, L. Bofenkamp, R. J. Wickham, H. Ge, and M. B. O'Connor (2010)
J. Neurosci. 30, 6025-6035
   Abstract »    Full Text »    PDF »
A Low-Affinity Antagonist Reveals Saturation and Desensitization in Mature Synapses in the Auditory Brain Stem.
S. Chanda and M. A. Xu-Friedman (2010)
J Neurophysiol 103, 1915-1926
   Abstract »    Full Text »    PDF »
Regulation of Ionotropic Glutamate Receptors by Their Auxiliary Subunits.
S. Tomita (2010)
Physiology 25, 41-49
   Abstract »    Full Text »    PDF »
Synchronous and Asynchronous Transmitter Release at Nicotinic Synapses Are Differentially Regulated by Postsynaptic PSD-95 Proteins.
R. A. Neff III, W. G. Conroy, J. D. Schoellerman, and D. K. Berg (2009)
J. Neurosci. 29, 15770-15779
   Abstract »    Full Text »    PDF »
Input-Specific Intrasynaptic Arrangements of Ionotropic Glutamate Receptors and Their Impact on Postsynaptic Responses.
E. Tarusawa, K. Matsui, T. Budisantoso, E. Molnar, M. Watanabe, M. Matsui, Y. Fukazawa, and R. Shigemoto (2009)
J. Neurosci. 29, 12896-12908
   Abstract »    Full Text »    PDF »
Matrix Metalloproteinase-9 Controls NMDA Receptor Surface Diffusion through Integrin {beta}1 Signaling.
P. Michaluk, L. Mikasova, L. Groc, R. Frischknecht, D. Choquet, and L. Kaczmarek (2009)
J. Neurosci. 29, 6007-6012
   Abstract »    Full Text »    PDF »
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Q. Zhang, Y. Li, and R. W. Tsien (2009)
Science 323, 1448-1453
   Abstract »    Full Text »    PDF »
Control of the Postsynaptic Membrane Viscosity.
M. Renner, D. Choquet, and A. Triller (2009)
J. Neurosci. 29, 2926-2937
   Abstract »    Full Text »    PDF »
Receptor-associated proteins and synaptic plasticity.
E. G. Bruneau, J. A. Esteban, and M. Akaaboune (2009)
FASEB J 23, 679-688
   Abstract »    Full Text »    PDF »
2008: Signaling Breakthroughs of the Year.
E. M. Adler (2009)
Science Signaling 2, eg1
   Abstract »    Full Text »    PDF »
Principles of Long-Term Dynamics of Dendritic Spines.
N. Yasumatsu, M. Matsuzaki, T. Miyazaki, J. Noguchi, and H. Kasai (2008)
J. Neurosci. 28, 13592-13608
   Abstract »    Full Text »    PDF »
Altered surface trafficking of presynaptic cannabinoid type 1 receptor in and out synaptic terminals parallels receptor desensitization.
L. Mikasova, L. Groc, D. Choquet, and O. J. Manzoni (2008)
PNAS 105, 18596-18601
   Abstract »    Full Text »    PDF »
Shuffling of neuronal receptors.
N. LeBrasseur (2008)
J. Cell Biol. 181, 400
   Full Text »    PDF »
NEUROSCIENCE: Refreshing Connections.
R. A. Silver and R. T. Kanichay (2008)
Science 320, 183-184
   Abstract »    Full Text »    PDF »

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