Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology
Open accessAbstract
Synapse specificity is a basic feature of synaptic plasticity, but it remains unclear how synapse-specific signaling is achieved if postsynaptic membrane proteins can diffuse laterally between synapses. We monitored movements of AMPA receptors (AMPARs) on the surface of mature neurons to investigate the role of lateral diffusion in constitutive AMPAR trafficking and to assess the influence of membrane architecture on the surface distribution of synaptic proteins. Our data show that lateral diffusion is responsible for the continual exchange of a substantial pool of AMPARs at the spine surface. Furthermore, we found that a general characteristic of membrane proteins is that their movement into and out of spines is slow compared with that in nonspiny membrane. This shows that lateral diffusion is dependent on spine morphology and is restricted at the spine neck. These results demonstrate the importance of lateral diffusion in trafficking of AMPAR protein population and provide new insight into how spine structure can maintain synapse specificity by compartmentalizing lateral diffusion and therefore increasing the residence time of membrane proteins near individual synapses.
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Receptor turnover in spines is slower compared to non-spinal plasma membrane, and recovery in the spine neck and base is particularly slow.
“Studying the FRAP dynamics of a fusion of SEP with the AMPA receptor subunit GluA2 (SEP-GluA2) revealed that receptor turnover in spines is slower compared to non-spinal plasma membrane and that recovery in the spine neck and base is particularly slow (Ashby et al., 2006).”
From Barriers in the brain: resolving dendritic spine morphology and compartmentalization (2014) · cites this paper as Ashby et al., 2006
In “Lateral diffusion is compartmentalized at spines” and “Diffusion of AMPARs in and out of spines is limited by the neck” (pages unavailable), the paper reports slower AMPA-receptor exchange in spine heads than in nonspiny membrane and slower diffusion in the neck. It does not support particularly slow recovery at the neck base: the latter section reports that the base and dendritic shaft had indistinguishable fluorescence-loss rates, indicating relatively rapid equilibration outside the spine. The regional neck/base comparison used FLIP, not FRAP recovery. (LLM, conf=0.88)
Experimental — accuracy not yet measuredFluorescently-tagged plasma membrane probes in spines showed a faster recovery rate in stubby than in mushroom-shaped spines.
“Furthermore, fluorescently-tagged plasma membrane probes in spines of different morphologies showed a faster recovery rate in stubby than in mushroom-shaped spines (Richards et al., 2004; Ashby et al., 2006), indicating that mushroom-shaped spines form a membrane compartment in which diffusion is slowed.”
From Barriers in the brain: resolving dendritic spine morphology and compartmentalization (2014) · cites this paper as Ashby et al., 2006
Mushroom-shaped spines form a membrane compartment in which diffusion is slowed.
“indicating that mushroom-shaped spines form a membrane compartment in which diffusion is slowed.”
From Barriers in the brain: resolving dendritic spine morphology and compartmentalization (2014) · cites this paper as Ashby et al., 2006
Mushroom shaped spines retain AMPA receptors in the vicinity of the synapse for an increased period of time.
“Mushroom shaped spines were found to retain AMPA receptors in the vicinity of the synapse for an increased period of time (Ashby et al., 2006; Ehlers et al., 2007; Opazo and Choquet, 2011, see Figure 3A).”
From Barriers in the brain: resolving dendritic spine morphology and compartmentalization (2014) · cites this paper as Ashby et al., 2006
Two-dimensional diffusion of membrane markers and AMPA-type glutamate receptors is sensitive to the morphology of the dendritic spine.
“Several experiments have shown that two-dimensional diffusion of membrane markers and AMPA-type glutamate receptors is sensitive to the morphology of the dendritic spine (Ashby et al., 2006; Shim et al., 2012).”
From Barriers in the brain: resolving dendritic spine morphology and compartmentalization (2014) · cites this paper as Ashby et al., 2006
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Mobility measurement by analysis of fluorescence photobleaching recovery kinetics
Axelrod, D., Koppel, D. E., Schlessinger, J., Elson, E. L., & Webb, W. W. (1976) · Biophysical Journal · doi:10.1016/s0006-3495(76)85755-4 · Cited by 2,717 · see citing works
AMPA Receptor Trafficking and Synaptic Plasticity
Malinow, R., & Malenka, R. C. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142758 · Cited by 2,588 · see citing works
Structural basis of long-term potentiation in single dendritic spines
Matsuzaki, M., Honkura, N., Ellis-Davies, G. C. R., & Kasai, H. (2004) · Nature · doi:10.1038/nature02617 · Cited by 2,500 · see citing works
Structure and function of dendritic spines
Nimchinsky, E. A., Sabatini, B. L., & Svoboda, K. (2002) · Annual Review of Physiology · doi:10.1146/annurev.physiol.64.081501.160008 · Cited by 1,208 · see citing works
Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity
Lee, H.-K., Barbarosie, M., Kameyama, K., Bear, M. F., & Huganir, R. L. (2000) · Nature · doi:10.1038/35016089 · Cited by 1,116 · see citing works
Reinsertion or Degradation of AMPA Receptors Determined by Activity-Dependent Endocytic Sorting
Ehlers, M. D. (2000) · Neuron · doi:10.1016/s0896-6273(00)00129-x · Cited by 1,096 · see citing works
Shi, S.-H., Hayashi, Y., Esteban, J. A., & Malinow, R. (2001) · Cell · doi:10.1016/s0092-8674(01)00321-x · Cited by 1,094 · see citing works
Receptor trafficking and synaptic plasticity
Collingridge, G. L., Isaac, J. T. R., & Wang, Y. T. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1556 · Cited by 1,046 · see citing works
Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses
Zhou, Q., Homma, K. J., & Poo, M.-M. (2004) · Neuron · doi:10.1016/j.neuron.2004.11.011 · Cited by 1,025 · see citing works
Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons
Wenthold, R., Petralia, R., Blahos J, II, & Niedzielski, A. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-06-01982.1996 · Cited by 850 · see citing works
Recycling Endosomes Supply AMPA Receptors for LTP
Park, M., Penick, E. C., Edwards, J. G., Kauer, J. A., & Ehlers, M. D. (2004) · Science · doi:10.1126/science.1102026 · Cited by 730 · see citing works
Role of AMPA Receptor Cycling in Synaptic Transmission and Plasticity
Lüscher, C., Xia, H., Beattie, E. C., Carroll, R. C., von Zastrow, M., Malenka, R. C., & Nicoll, R. A. (1999) · Neuron · doi:10.1016/s0896-6273(00)81119-8 · Cited by 692 · see citing works
From fixed to FRAP: measuring protein mobility and activity in living cells
Reits, E. A., & Neefjes, J. (2001) · Nature Cell Biology · doi:10.1038/35078615 · Cited by 681 · see citing works
Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons
Passafaro, M., Piëch, V., & Sheng, M. (2001) · Nature Neuroscience · doi:10.1038/nn0901-917 · Cited by 655 · see citing works
Lipid Rafts in the Maintenance of Synapses, Dendritic Spines, and Surface AMPA Receptor Stability
Hering, H., Lin, C.-C., & Sheng, M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03262.2003 · Cited by 602 · see citing works
Bidirectional Activity-Dependent Morphological Plasticity in Hippocampal Neurons
Nägerl, U. V., Eberhorn, N., Cambridge, S. B., & Bonhoeffer, T. (2004) · Neuron · doi:10.1016/j.neuron.2004.11.016 · Cited by 602 · see citing works
The Use of pHluorins for Optical Measurements of Presynaptic Activity
Sankaranarayanan, S., Angelis, D. A. D., Rothman, J. E., & Ryan, T. A. (2000) · Biophysical Journal · doi:10.1016/s0006-3495(00)76468-x · Cited by 586 · see citing works
NSF Binding to GluR2 Regulates Synaptic Transmission
Nishimune, A., Isaac, J. T. R., Molnár, E., Noël, J., Nash, S. R., Tagaya, M., Collingridge, G. L., Nakanishi, S., & Henley, J. M. (1998) · Neuron · doi:10.1016/s0896-6273(00)80517-6 · Cited by 544 · see citing works
Self-citationRegulation of AMPA receptor lateral movements
Borgdorff, A. J., & Choquet, D. (2002) · Nature · doi:10.1038/nature00780 · Cited by 542 · see citing works
Glutamate Receptor Exocytosis and Spine Enlargement during Chemically Induced Long-Term Potentiation
Kopec, C. D., Li, B., Wei, W., Boehm, J., & Malinow, R. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3918-05.2006 · Cited by 486 · see citing works
Constrained diffusion or immobile fraction on cell surfaces: a new interpretation
Feder, T., Brust‐Mascher, I., Slattery, J. P., Baird, B. A., & Webb, W. W. (1996) · Biophysical Journal · doi:10.1016/s0006-3495(96)79846-6 · Cited by 476 · see citing works
Direct measurement of coupling between dendritic spines and shafts
Svoboda, K., Tank, D. W., & Denk, W. (1996) · Science · doi:10.1126/science.272.5262.716 · Cited by 472 · see citing works
Electron Microscopy of Synaptic Contacts on Dendrite Spines of the Cerebral Cortex
Gray, E. G. (1959) · Nature · doi:10.1038/1831592a0 · Cited by 443 · see citing works
Lee, S. H., Liu, L., Wang, Y. T., & Sheng, M. (2002) · Neuron · doi:10.1016/s0896-6273(02)01024-3 · Cited by 441 · see citing works
Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors
Groc, L., Heine, M., Cognet, L., Brickley, K., Stephenson, F. A., Lounis, B., & Choquet, D. (2004) · Nature Neuroscience · doi:10.1038/nn1270 · Cited by 429 · see citing works
Postsynaptic Membrane Fusion and Long-Term Potentiation
Lledo, P.-M., Zhang, X., Südhof, T. C., Malenka, R. C., & Nicoll, R. A. (1998) · Science · doi:10.1126/science.279.5349.399 · Cited by 413 · see citing works
The role of receptor diffusion in the organization of the postsynaptic membrane
Choquet, D., & Triller, A. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1077 · Cited by 410 · see citing works
Direct imaging of lateral movements of AMPA receptors inside synapses
Tardin, C., Cognet, L., Bats, C., Lounis, B., & Choquet, D. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg463 · Cited by 384 · see citing works
From form to function: calcium compartmentalization in dendritic spines
Yuste, R., Majewska, A. K., & Holthoff, K. (2000) · Nature Neuroscience · doi:10.1038/76609 · Cited by 370 · see citing works
Dynamics and Regulation of Clathrin Coats at Specialized Endocytic Zones of Dendrites and Spines
Blanpied, T. A., Scott, D. B., & Ehlers, M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00979-0 · Cited by 366 · see citing works
Neuronal activity regulates diffusion across the neck of dendritic spines
Bloodgood, B. L., & Sabatini, B. L. (2005) · Science · doi:10.1126/science.1114816 · Cited by 344 · see citing works
Molecular organization of the postsynaptic specialization
Sheng, M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.111146298 · Cited by 336 · see citing works
Noël, J., Ralph, G. S., Pickard, L., Williams, J., Molnár, E., Uney, J. B., Collingridge, G. L., & Henley, J. M. (1999) · Neuron · doi:10.1016/s0896-6273(00)80786-2 · Cited by 299 · see citing works
Self-citationSurface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move!
Triller, A., & Choquet, D. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.01.001 · Cited by 285 · see citing works
Rapid recruitment of NMDA receptor transport packets to nascent synapses
Washbourne, P., Bennett, J. E., & McAllister, A. K. (2002) · Nature Neuroscience · doi:10.1038/nn883 · Cited by 284 · see citing works
Labeling Neural Cells Using Adenoviral Gene Transfer of Membrane-Targeted GFP
Moriyoshi, K., Richards, L. J., Akazawa, C., O’Leary, D. D. M., & Nakanishi, S. (1996) · Neuron · doi:10.1016/s0896-6273(00)80044-6 · Cited by 280 · see citing works
Gardner, S. M., Takamiya, K., Xia, J., Suh, J., Johnson, R. C., Yu, S., & Huganir, R. L. (2005) · Neuron · doi:10.1016/j.neuron.2005.02.026 · Cited by 245 · see citing works
Ashby, M. C., De La Rue, S. A., Ralph, G. S., Uney, J., Collingridge, G. L., & Henley, J. M. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1042-04.2004 · Cited by 244 · see citing works
Self-citationPhotoinactivation of native AMPA receptors reveals their real-time trafficking
Adesnik, H., Nicoll, R. A., & England, P. M. (2005) · Neuron · doi:10.1016/j.neuron.2005.11.030 · Cited by 234 · see citing works
Lateral organization of endocytic machinery in dendritic spines
Rácz, B., Blanpied, T. A., Ehlers, M., & Weinberg, R. J. (2004) · Nature Neuroscience · doi:10.1038/nn1303 · Cited by 227 · see citing works
Redistribution and Stabilization of Cell Surface Glutamate Receptors during Synapse Formation
Mammen, A. L., Huganir, R. L., & O’Brien, R. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-19-07351.1997 · Cited by 211 · see citing works
It's green outside: tracking cell surface proteins with pH-sensitive GFP
Ashby, M. C., Ibaraki, K., & Henley, J. M. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.03.010 · Cited by 128 · see citing works
Self-citationInternalization at glutamatergic synapses during development
Petralia, R. S., Wang, Y., & Wenthold, R. J. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03074.x · Cited by 120 · see citing works
Activity‐dependent endocytic sorting of kainate receptors to recycling or degradation pathways
Martin, S., & Henley, J. M. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600483 · Cited by 112 · see citing works
Self-citationPickard, L., Noël, J., Duckworth, J. K., Fitzjohn, S. M., Henley, J. M., Collingridge, G. L., & Molnár, E. (2001) · Neuropharmacology · doi:10.1016/s0028-3908(01)00127-7 · Cited by 107 · see citing works
Self-citationStructure and molecular organization of dendritic spines.
Tashiro, A., & Yuste, R. (2003) · PubMed · doi:10.14670/hh-18.617 · Cited by 60 · see citing works
Syntaxin-1A Is Excluded from Recycling Synaptic Vesicles at Nerve Terminals
Mitchell, S. J., & Ryan, T. A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0174-04.2004 · Cited by 57 · see citing works
Richards, D. A., De Paola, V., Caroni, P., Gähwiler, B. H., & McKinney, R. A. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.062091 · Cited by 49 · see citing works
Flagged first, then by citations
1 of the 49 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
The Postsynaptic Architecture of Excitatory Synapses: A More Quantitative View
Sheng, M., & Hoogenraad, C. C. (2007) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.060805.160029 · Cited by 1,003 · see citing works
Balancing Structure and Function at Hippocampal Dendritic Spines
Bourne, J. N., & Harris, K. M. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125646 · Cited by 916 · see citing works
Do thin spines learn to be mushroom spines that remember?
Bourne, J., & Harris, K. M. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.04.009 · Cited by 843 · see citing works
Dendritic Excitability and Synaptic Plasticity
Sjöström, P. J., Rancz, E. A., Roth, A., & Häusser, M. (2008) · Physiological Reviews · doi:10.1152/physrev.00016.2007 · Cited by 721 · see citing works
Structure, Function, and Pharmacology of Glutamate Receptor Ion Channels
Hansen, K. B., Wollmuth, L. P., Bowie, D., Furukawa, H., Menniti, F. S., Sobolevsky, A. I., Swanson, G. T., Swanger, S. A., Greger, I. H., Nakagawa, T., et al. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000131 · Cited by 686 · see citing works
Stochastic models of intracellular transport
Bressloff, P. C., & Newby, J. (2013) · Reviews of Modern Physics · doi:10.1103/revmodphys.85.135 · Cited by 631 · see citing works
The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking
Bats, C., Groc, L., & Choquet, D. (2007) · Neuron · doi:10.1016/j.neuron.2007.01.030 · Cited by 590 · see citing works
Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity
Frischknecht, R., Heine, M., Perrais, D., Seidenbecher, C. I., Choquet, D., & Gundelfinger, E. D. (2009) · Nature Neuroscience · doi:10.1038/nn.2338 · Cited by 554 · see citing works
Surface Mobility of Postsynaptic AMPARs Tunes Synaptic Transmission
Heine, M., Groc, L., Frischknecht, R., Béïque, J.-C., Lounis, B., Rumbaugh, G., Huganir, R. L., Cognet, L., & Choquet, D. (2008) · Science · doi:10.1126/science.1152089 · Cited by 518 · see citing works
Shim, S.-H., Xia, C., Zhong, G., Babcock, H. P., Vaughan, J. C., Huang, B., Wang, X., Xu, C., Bi, G.-Q., & Zhuang, X. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201882109 · Cited by 514 · see citing works
AMPA Receptor Incorporation into Synapses during LTP: The Role of Lateral Movement and Exocytosis
Makino, H., & Malinow, R. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.035 · Cited by 501 · see citing works
Pathophysiology of L-dopa-induced motor and non-motor complications in Parkinson's disease
Bastide, M. F., Meissner, W. G., Picconi, B., Fasano, S., Fernagut, P., Feyder, M. T., Francardo, V., Alcacer, C., Ding, Y., Brambilla, R., et al. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.07.002 · Cited by 470 · see citing works
Dendritic Spines: The Locus of Structural and Functional Plasticity
Sala, C., & Segal, M. (2014) · Physiological Reviews · doi:10.1152/physrev.00012.2013 · Cited by 465 · see citing works
Glutamate receptor dynamics in dendritic microdomains.
Newpher, T. M., & Ehlers, M. D. (2008) · Neuron · doi:10.1016/j.neuron.2008.04.030 · Cited by 356 · see citing works
Regulation of AMPA receptor extrasynaptic insertion by 4.1N, phosphorylation and palmitoylation
Lin, D.-T., Makino, Y., Sharma, K., Hayashi, T., Neve, R., Takamiya, K., & Huganir, R. L. (2009) · Nature Neuroscience · doi:10.1038/nn.2351 · Cited by 347 · see citing works
ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity
Gu, J., Lee, C. W., Fan, Y., Komlos, D., Tang, X., Sun, C., Yu, K., Hartzell, H. C., Chen, G., Bamburg, J. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2634 · Cited by 325 · see citing works
Nanoconnectomic upper bound on the variability of synaptic plasticity
Bartol, T. M., Bromer, C., Kinney, J. P., Chirillo, M. A., Bourne, J. N., Harris, K. M., & B, T. J. S. A. (2015) · eLife · doi:10.7554/elife.10778 · Cited by 319 · see citing works
Septins and the Lateral Compartmentalization of Eukaryotic Membranes
Caudron, F., & Barral, Y. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.04.003 · Cited by 296 · see citing works
Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity
Ehlers, M. D., Heine, M., Groc, L., Lee, M.-C., & Choquet, D. (2007) · Neuron · doi:10.1016/j.neuron.2007.04.010 · Cited by 300 · see citing works
Syntaxin-4 defines a domain for activity-dependent exocytosis in dendritic spines
Kennedy, M. J., Davison, I. G., Robinson, C. G., & Ehlers, M. D. (2010) · Cell · doi:10.1016/j.cell.2010.02.042 · Cited by 294 · see citing works
Role of Septin Cytoskeleton in Spine Morphogenesis and Dendrite Development in Neurons
Tada, T., Simonetta, A., Batterton, M. N., Kinoshita, M., Edbauer, D., & Sheng, M. (2007) · Current Biology · doi:10.1016/j.cub.2007.09.039 · Cited by 284 · see citing works
Lateral transport of Smoothened from the plasma membrane to the membrane of the cilium
Milenkovic, L., Scott, M. P., & Rohatgi, R. (2009) · Journal of Cell Biology · doi:10.1083/jcb.200907126 · Cited by 263 · see citing works
Lu, J., Helton, T. D., Blanpied, T. A., Rácz, B., Newpher, T. M., Weinberg, R. J., & Ehlers, M. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.06.041 · Cited by 273 · see citing works
New Concepts in Synaptic Biology Derived from Single-Molecule Imaging
Triller, A., & Choquet, D. (2008) · Neuron · doi:10.1016/j.neuron.2008.06.022 · Cited by 262 · see citing works
Patterson, M. A., Szatmari, E. M., & Yasuda, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913875107 · Cited by 259 · see citing works
AMPA receptor trafficking and the mechanisms underlying synaptic plasticity and cognitive aging
Henley, J. M., & Wilkinson, K. A. (2013) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2013.15.1/jhenley · Cited by 236 · see citing works
Self-citationMembrane Shape Modulates Transmembrane Protein Distribution
Aimon, S., Callan-Jones, A., Berthaud, A., Pinot, M., Toombes, G. E. S., & Bassereau, P. M. (2014) · Developmental Cell · doi:10.1016/j.devcel.2013.12.012 · Cited by 232 · see citing works
Spine Expansion and Stabilization Associated with Long-Term Potentiation
Yang, Y., Wang, X.-B., Frerking, M., & Zhou, Q. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3998-07.2008 · Cited by 222 · see citing works
Linking glutamate receptor movements and synapse function
Groc, L., & Choquet, D. (2020) · Science · doi:10.1126/science.aay4631 · Cited by 207 · see citing works
From the stochasticity of molecular processes to the variability of synaptic transmission
Ribrault, C., Sekimoto, K., & Triller, A. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3025 · Cited by 198 · see citing works
Real-Time Imaging of Discrete Exocytic Events Mediating Surface Delivery of AMPA Receptors
Yudowski, G. A., Puthenveedu, M. A., Leonoudakis, D., Panicker, S., Thorn, K. S., Beattie, E. C., & von Zastrow, M. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2465-07.2007 · Cited by 197 · see citing works
Groc, L., Lafourcade, M., Heine, M., Renner, M. L., Racine, V., Sibarita, J., Lounis, B., Choquet, D., & Cognet, L. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3349-07.2007 · Cited by 194 · see citing works
A three-step model for the synaptic recruitment of AMPA receptors
Opazo, P., & Choquet, D. (2011) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2010.08.014 · Cited by 190 · see citing works
Smith, K. R., Kopeikina, K. J., Fawcett‐Patel, J. M., Leaderbrand, K., Gao, R., Schürmann, B., Myczek, K., Radulović, J., Swanson, G. T., & Penzes, P. (2014) · Neuron · doi:10.1016/j.neuron.2014.10.010 · Cited by 177 · see citing works
Synaptic stability and plasticity in a floating world
Gerrow, K., & Triller, A. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.06.010 · Cited by 171 · see citing works
Holcman, D., & Schuss, Z. (2014) · SIAM Review · doi:10.1137/120898395 · Cited by 159 · see citing works
Constals, A., Penn, A. C., Compans, B., Toulmé, E., Philippat, A., Marais, S., Retailleau, N., Hafner, A., Coussen, F., Hosy, E., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.01.012 · Cited by 157 · see citing works
Bian, W.-J., Miao, W., He, S., Qiu, Z., & Yu, X. (2015) · Cell · doi:10.1016/j.cell.2015.07.018 · Cited by 159 · see citing works
Segal, M. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07270.x · Cited by 152 · see citing works
A Vesicle Superpool Spans Multiple Presynaptic Terminals in Hippocampal Neurons
Staras, K., Branco, T., Burden, J. J., Pozo, K., Darcy, K., Marra, V., Ratnayaka, J. A., & Goda, Y. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.020 · Cited by 153 · see citing works
Neurexin-Neuroligin Adhesions Capture Surface-Diffusing AMPA Receptors through PSD-95 Scaffolds
Mondin, M., Labrousse, V. F., Hosy, E., Heine, M., Tessier, B., Levet, F., Poujol, C., Blanchet, C., Choquet, D., & Thoumine, O. R. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6439-10.2011 · Cited by 150 · see citing works
Membrane Potential Changes in Dendritic Spines during Action Potentials and Synaptic Input
Palmer, L. M., & Stuart, G. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5847-08.2009 · Cited by 149 · see citing works
AMPA receptor biogenesis and trafficking
Greger, I. H., & Esteban, J. A. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.04.007 · Cited by 145 · see citing works
Control of the postsynaptic membrane viscosity
Renner, M., Choquet, D., & Triller, A. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4445-08.2009 · Cited by 145 · see citing works
Hozé, N., Nair, D. K., Hosy, E., Sieben, C., Manley, S., Herrmann, A., Sibarita, J., Choquet, D., & Holcman, D. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1204589109 · Cited by 142 · see citing works
Gauvain, G., Chamma, I., Chevy, Q., Cabezas, C., Irinopoulou, T., Bodrug, N., Carnaud, M., Lévi, S., & Poncer, J. C. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1107893108 · Cited by 141 · see citing works
Choquet, D. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.2119-18.2018 · Cited by 141 · see citing works
Regulation of AMPA receptors and synaptic plasticity
Santos, S. D., Carvalho, A. L., Caldeira, M. V., & Duarte, C. B. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.037 · Cited by 139 · see citing works
Spine microdomains for postsynaptic signaling and plasticity
Newpher, T. M., & Ehlers, M. D. (2009) · Trends in Cell Biology · doi:10.1016/j.tcb.2009.02.004 · Cited by 140 · see citing works
Surface dynamics of GluN2B‐NMDA receptors controls plasticity of maturing glutamate synapses
Dupuis, J. P., Ladépêche, L., Seth, H., Bard, L., Varela, J. A., Mikasová, L., Bouchet, D., Rogemond, V., Honnorat, J., Hanse, E., et al. (2014) · The EMBO Journal · doi:10.1002/embj.201386356 · Cited by 132 · see citing works
Corticosterone Alters AMPAR Mobility and Facilitates Bidirectional Synaptic Plasticity
Martin, S., Henley, J. M., Holman, D., Zhou, M., Wiegert, O., van Spronsen, M., Joëls, M., Hoogenraad, C. C., & Krugers, H. J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004714 · Cited by 130 · see citing works
Self-citationWidespread Changes in Dendritic Spines in a Model of Alzheimer's Disease
Knafo, S., Alonso-Nanclares, L., Gonzalez-Soriano, J., Merino-Serrais, P., Fernaud-Espinosa, I., Ferrer, I., & DeFelipe, J. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn111 · Cited by 132 · see citing works
Proteostasis in complex dendrites
Hanus, C., & Schuman, E. M. (2013) · Nature reviews. Neuroscience · doi:10.1038/nrn3546 · Cited by 130 · see citing works
Pontrello, C. G., Sun, M., Lin, A. Y., Fiacco, T. A., DeFea, K., & Ethell, I. M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1118803109 · Cited by 130 · see citing works
The emerging functions of septins in metazoans
Saarikangas, J., & Barral, Y. (2011) · EMBO Reports · doi:10.1038/embor.2011.193 · Cited by 129 · see citing works
PSD-95 expression controls l-DOPA dyskinesia through dopamine D1 receptor trafficking
Porras, G., Berthet, A., Dehay, B., Li, Q., Ladépêche, L., Normand, E., Doveró, S., Martínez, A., Doudnikoff, É., Martin‐Négrier, M., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci59426 · Cited by 126 · see citing works
Doublecortin-like kinase enhances dendritic remodelling and negatively regulates synapse maturation
Shin, E., Kashiwagi, Y., Kuriu, T., Iwasaki, H., Tanaka, T., Koizumi, H., Gleeson, J. G., & Okabe, S. (2013) · Nature Communications · doi:10.1038/ncomms2443 · Cited by 134 · see citing works
Chemical labelling for visualizing native AMPA receptors in live neurons
Wakayama, S., Kiyonaka, S., Arai, I., Kakegawa, W., Matsuda, S., Ibata, K., Nemoto, Y. L., Kusumi, A., Yuzaki, M., & Hamachi, I. (2017) · Nature Communications · doi:10.1038/ncomms14850 · Cited by 124 · see citing works
Multiple Association States between Glycine Receptors and Gephyrin Identified by SPT Analysis
Ehrensperger, M.-V., Hanus, C., Vannier, C., Triller, A., & Dahan, M. (2007) · Biophysical Journal · doi:10.1529/biophysj.106.095596 · Cited by 122 · see citing works
Cell and Molecular Biology of Septins
Fung, K., Dai, L., & Trimble, W. S. (2014) · International review of cytology · doi:10.1016/b978-0-12-800180-6.00007-4 · Cited by 118 · see citing works
Clathrin‐Mediated Endocytosis at Synapses
Jung, N., & Haucke, V. (2007) · Traffic · doi:10.1111/j.1600-0854.2007.00595.x · Cited by 118 · see citing works
Synaptic transmission and plasticity require AMPA receptor anchoring via its N-terminal domain
Watson, J. F., Ho, H., & Greger, I. H. (2017) · eLife · doi:10.7554/elife.23024 · Cited by 117 · see citing works
Agonist binding to the NMDA receptor drives movement of its cytoplasmic domain without ion flow
Doré, K., Aow, J., & Malinow, R. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1520023112 · Cited by 109 · see citing works
Burrone, J., Li, Z., & Murthy, V. N. (2006) · Nature Protocols · doi:10.1038/nprot.2006.449 · Cited by 113 · see citing works
Electrodiffusion phenomena in neuroscience: a neglected companion
Savtchenko, L. P., Poo, M. M., & Rusakov, D. A. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2017.101 · Cited by 110 · see citing works
Synaptic SAP97 Isoforms Regulate AMPA Receptor Dynamics and Access to Presynaptic Glutamate
Waites, C. L., Specht, C. G., Härtel, K., Leal-Ortiz, S., Genoux, D., Li, D., Drisdel, R. C., Jeyifous, O., Cheyne, J. E., Green, W. N., et al. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4431-08.2009 · Cited by 97 · see citing works
Unified quantitative model of AMPA receptor trafficking at synapses
Czöndör, K., Mondin, M., Garcia, M., Heine, M., Frischknecht, R., Choquet, D., Sibarita, J., & Thoumine, O. R. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109818109 · Cited by 105 · see citing works
A Septin-Dependent Diffusion Barrier at Dendritic Spine Necks
Ewers, H., Tada, T., Petersen, J. D., Rácz, B., Sheng, M., & Choquet, D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113916 · Cited by 104 · see citing works
Shaping the synaptic signal: molecular mobility inside and outside the cleft
Rusakov, D. A., Savtchenko, L. P., Zheng, K., & Henley, J. M. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.03.002 · Cited by 105 · see citing works
Self-citationMobility in geometrically confined membranes
Domanov, Y. A., Aimon, S., Toombes, G. E. S., Renner, M., Quemeneur, F., Triller, A., Turner, M. S., & Bassereau, P. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102646108 · Cited by 105 · see citing works
AMPA Receptors as Therapeutic Targets for Neurological Disorders
Lee, K., Goodman, L., Fourie, C., Schenk, S., Leitch, B., & Montgomery, J. M. (2015) · Advances in protein chemistry and structural biology · doi:10.1016/bs.apcsb.2015.10.004 · Cited by 102 · see citing works
Fast AMPAR trafficking for a high‐frequency synaptic transmission
Choquet, D. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07350.x · Cited by 93 · see citing works
Zhang, H., Etherington, L.-A., Hafner, A., Belelli, D., Coussen, F., Delagrange, P., Chaouloff, F., Spedding, M., Lambert, J. J., Choquet, D., et al. (2012) · Molecular Psychiatry · doi:10.1038/mp.2012.80 · Cited by 92 · see citing works
Subsynaptic positioning of AMPARs by LRRTM2 controls synaptic strength
Ramsey, A. M., Tang, A., LeGates, T. A., Gou, X., Carbone, B. E., Thompson, S. M., Biederer, T., & Blanpied, T. A. (2021) · Science Advances · doi:10.1126/sciadv.abf3126 · Cited by 90 · see citing works
Kerr, J. M., & Blanpied, T. A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2927-11.2012 · Cited by 91 · see citing works
Synapse Geometry and Receptor Dynamics Modulate Synaptic Strength
Freche, D., Pannasch, U., Rouach, N., & Holcman, D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025122 · Cited by 86 · see citing works
Earnshaw, B. A., & Bressloff, P. C. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3601-06.2006 · Cited by 85 · see citing works
Bell, M. K., Bartol, T., B, T. J. S. A., & Rangamani, P. (2019) · The Journal of General Physiology · doi:10.1085/jgp.201812261 · Cited by 80 · see citing works
Visualizing synaptic plasticity in vivo by large-scale imaging of endogenous AMPA receptors
Graves, A. R., Roth, R. H., Tan, H. L., Zhu, Q., Bygrave, A. M., Lopez-Ortega, E., Hong, I., Spiegel, A. C., Johnson, R. C., Vogelstein, J. T., et al. (2021) · eLife · doi:10.7554/elife.66809 · Cited by 84 · see citing works
Examining Form and Function of Dendritic Spines
Lee, K. F. H., Soares, C., & Béïque, J.-C. (2012) · Neural Plasticity · doi:10.1155/2012/704103 · Cited by 82 · see citing works
KCC2 Gates Activity-Driven AMPA Receptor Traffic through Cofilin Phosphorylation
Chevy, Q., Heubl, M., Goutierre, M., Backer, S., Moutkine, I., Eugène, E., Bloch‐Gallego, E., Lévi, S., & Poncer, J. C. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1735-15.2015 · Cited by 82 · see citing works
Szepesi, Z., Hosy, E., Ruszczycki, B., Bijata, M., Pyskaty, M., Bikbaev, A., Heine, M., Choquet, D., Kaczmarek, L., & Wlodarczyk, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098274 · Cited by 83 · see citing works
An optimized CRISPR/Cas9 approach for precise genome editing in neurons
Fang, H., Bygrave, A. M., Roth, R. H., Johnson, R. C., & Huganir, R. L. (2021) · eLife · doi:10.7554/elife.65202 · Cited by 78 · see citing works
Swanger, S. A., Yao, X., Groß, C., & Bassell, G. J. (2011) · Molecular Brain · doi:10.1186/1756-6606-4-38 · Cited by 81 · see citing works
Trafficking of AMPA Receptors at Plasma Membranes of Hippocampal Neurons
Tao-Cheng, J.-H., Crocker, V. T., Winters, C. A., Azzam, R., Chludzinski, J., & Reese, T. S. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4745-10.2011 · Cited by 82 · see citing works
Molecular genetics and imaging technologies for circuit-based neuroanatomy
Arenkiel, B. R., & Ehlers, M. D. (2009) · Nature · doi:10.1038/nature08536 · Cited by 78 · see citing works
The discovery of dendritic spines by Cajal in 1888 and its relevance in the present neuroscience
García-López, P., García‐Marín, V., & Freire, M. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.06.002 · Cited by 77 · see citing works
Lee, S. H., Jin, C., Cai, E., Ge, P., Ishitsuka, Y., Teng, K. W., de Thomaz, A. A., Nall, D., Baday, M., Jeyifous, O., et al. (2017) · eLife · doi:10.7554/elife.27744 · Cited by 76 · see citing works
The structure and function of actin cytoskeleton in mature glutamatergic dendritic spines
Bellot, A., Guivernau, B., Tajes, M., Bosch-Morató, M., Valls-Comamala, V., & Muñoz, F. J. (2014) · Brain Research · doi:10.1016/j.brainres.2014.05.024 · Cited by 74 · see citing works
Tyrosine dephosphorylation regulates AMPAR internalisation in mGluR-LTD
Gladding, C. M., Collett, V. J., Jia, Z., Bashir, Z. I., Collingridge, G. L., & Molnár, E. (2009) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.10.014 · Cited by 74 · see citing works
Changes in Hippocampal Plasticity in Depression and Therapeutic Approaches Influencing These Changes
Xu, W., Yao, X., Zhao, F., Zhao, H., Cheng, Z., Yang, W., Cui, R., Xu, S., & Li, B. (2020) · Neural Plasticity · doi:10.1155/2020/8861903 · Cited by 73 · see citing works
Knafo, S., Venero, C., Merino‐Serrais, P., Fernaud-Espinosa, I., González‐Soriano, J., Ferrer, I., Santpere, G., & DeFelipe, J. (2009) · The Journal of Pathology · doi:10.1002/path.2565 · Cited by 73 · see citing works
Bell, M. E., Bourne, J. N., Chirillo, M. A., Mendenhall, J. M., Kuwajima, M., & Harris, K. M. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23646 · Cited by 72 · see citing works
Control of flux by narrow passages and hidden targets in cellular biology
Holcman, D., & Schuss, Z. (2013) · Reports on Progress in Physics · doi:10.1088/0034-4885/76/7/074601 · Cited by 68 · see citing works
Campos, V., Prado-Alcalá, R. A., León-Jacinto, U., Aguilar-Vázquez, A. R., Quirarte, G. L., Ramı́rez-Amaya, V., & Díaz-Cintra, S. Y. (2010) · Brain Research · doi:10.1016/j.brainres.2010.10.105 · Cited by 70 · see citing works
Diffusion of Protein Receptors on a Cylindrical Dendritic Membrane with Partially Absorbing Traps
Bressloff, P. C., Earnshaw, B. A., & Ward, M. J. (2008) · SIAM Journal on Applied Mathematics · doi:10.1137/070698373 · Cited by 70 · see citing works
Patriarchi, T., Buonarati, O. R., & Hell, J. W. (2018) · The EMBO Journal · doi:10.15252/embj.201899771 · Cited by 65 · see citing works
Robertson, H. R., Gibson, E. S., Benke, T. A., & Dell’Acqua, M. L. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.6093-08.2009 · Cited by 68 · see citing works
Dynamin-dependent Membrane Drift Recruits AMPA Receptors to Dendritic Spines
Jaskolski, F., Mayo-Martin, M. B., Jane, D. E., & Henley, J. M. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m808401200 · Cited by 65 · see citing works
Self-citationCasting a net on dendritic spines: The extracellular matrix and its receptors
Dansie, L. E., & Ethell, I. M. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20963 · Cited by 66 · see citing works
- Authors
- Ashby, M. C., Maier, S. R., Nishimune, A., & Henley, J. M.
- Affiliations
- University of Bristol (GB)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-06-28
- Volume
- 26
- Issue
- 26
- Pages
- 7046-7055
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6673929
- OpenAlex
- W1982726026
- Cited by
- 302
- References
- 49
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 11 · 2023: 8 · 2022: 12 · 2021: 16 · 2020: 8 · 2019: 6 · 2018: 13 · 2017: 14 · 2016: 8 · 2015: 15 · 2014: 26 · 2013: 19 · 2012: 20
- FWCI
- 8.98
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Bristol Research (University of Bristol) (submittedVersion)
- Funders
- Wellcome Trust
- European Commission
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
- Keywords
- lateral diffusion, AMPA receptors, dendritic spines, dendritic spine morphology, receptor trafficking, synapse specificity, membrane protein diffusion, synaptic plasticity, postsynaptic membrane
- MeSH terms
- Animals, Biological Transport, Cell Membrane, Cells, Cultured, Diffusion, Neurons, Tissue Distribution, Receptors, AMPA, Protein Transport, Photobleaching, Dendritic Spines, Green Fluorescent Proteins, Rats
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