AMPA Receptor Incorporation into Synapses during LTP: The Role of Lateral Movement and Exocytosis
Open accessAbstract
The regulated trafficking of AMPA receptors (AMPARs) to synapses is thought to underlie the enhanced transmission in long-term potentiation (LTP), a cellular model of memory. However, there is controversy regarding the nonsynaptic site, either on the surface or intracellularly, from which AMPARs move into synapses during LTP. Using recombinant surface-fluorescent receptors in organotypic rat hippocampal slices, we show that the majority of AMPARs incorporated into synapses during LTP is from lateral diffusion of spine surface receptors containing GluR1, an AMPAR subunit. Following synaptic potentiation, AMPARs in intracellular pools containing GluR1 are driven to the surface primarily on dendrites. These exocytosed receptors likely serve to replenish the local extrasynaptic pool available for subsequent bouts of plasticity. These results clarify the role of intracellular and surface AMPARs during synaptic plasticity.
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Blocking postsynaptic exocytosis by a variety of means blocks LTP/sLTP.
“Numerous studies have shown that blocking postsynaptic exocytosis by a variety of means blocks LTP/sLTP (195, 249, 250, 332–338).”
From Synaptic memory and CaMKII (2023) · cites this paper as [249]
The Discussion (page not available in our copy) says several studies found that agents targeted to block exocytosis can inhibit LTP, supporting the LTP portion of the claim. It does not establish that blocking exocytosis blocks structural LTP (sLTP), and it cautions that some agents may inhibit LTP through effects other than exocytosis. (LLM, conf=0.84)
Experimental — accuracy not yet measuredSurface localized AMPARs are supplied by exocytosis from pools of intracellular receptors contained within endosomes.
“Surface localized AMPARs are supplied by exocytosis from pools of intracellular receptors contained within endosomes (Lin et al., 2009, Makino and Malinow, 2009).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Makino and Malinow, 2009
The Results section (‘Compartmentalized GluR1 exocytosis replenishing a local extrasynaptic AMPAR pool’; page unavailable) says intracellular GluR1 is exocytosed onto the dendritic surface and replenishes an extrasynaptic receptor pool. Our copy does not identify those intracellular pools as endosomes, so that specific part of the claim is unsupported. (LLM, conf=0.86)
Experimental — accuracy not yet measuredLarge packets of GluA1 are inserted into the dendritic shaft from intracellular recycling endosomes, containing an estimated fifty GluA1-containing receptors, in an activity-dependent manner.
“Large packets of GluA1 are inserted into the dendritic shaft from intracellular recycling endosomes, containing an estimated fifty GluA1-containing receptors, in an activity-dependent manner (Lin et al., 2009, Makino and Malinow, 2009).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Makino and Malinow, 2009
The Results section, “Small contribution of AMPAR exocytosis to synaptic potentiation during LTP” (page unavailable), reports GluR1-containing compartments undergoing exocytosis onto dendrites after LTP induction. The cited paper does not identify those compartments as recycling endosomes or estimate that each contains fifty receptors; its reported fluorescent spots do not establish the claimed packet size. (LLM, conf=0.87)
Experimental — accuracy not yet measuredSynaptic potentiation of AMPA receptors is achieved by restricting their diffusion out of the synaptic membrane.
“Combining SEP-GluA1 photobleaching experiments with glutamate uncaging in organotypic slices revealed that synaptic potentiation of AMPA receptors is achieved by restricting their diffusion out of the synaptic membrane (Makino and Malinow, 2009).”
From Barriers in the brain: resolving dendritic spine morphology and compartmentalization (2014) · cites this paper as Makino and Malinow, 2009
LTP-inducing stimuli cause rapid addition of AMPARs to classical dendritic spines.
“These synapses contain AMPARs, but LTP-inducing stimuli cause a rapid addition of AMPARs to the synapse (246–250).”
From Synaptic memory and CaMKII (2023) · cites this paper as [249]
Many synaptic proteins are remarkably dynamic, including AMPARs, NMDARs, CaMKII, and scaffolding proteins such as PSD-95.
“These studies show that many synaptic proteins are remarkably dynamic, including AMPARs (237, 249, 327, 328), NMDARs (329), CaMKII (330), and scaffolding proteins, such as PSD-95 (331).”
From Synaptic memory and CaMKII (2023) · cites this paper as [249]
By tagging AMPARs with a pH-sensitive tag (SEP-GluA1), insertion of AMPARs into the surface membrane can be directly visualized during LTP-inducing protocols.
“By tagging AMPARs with a pH-sensitive tag (SEP-GluA1), the insertion of AMPARs into the surface membrane can be directly visualized during LTP-inducing protocols (249, 250, 335, 337, 338, 340).”
From Synaptic memory and CaMKII (2023) · cites this paper as [249]
In most cases AMPARs are inserted via exocytosis into the dendritic shaft, some distance from the synapse.
“Fourth, in most cases the AMPARs are inserted via exocytosis into the dendritic shaft, some distance from the synapse (220, 249, 250, 337).”
From Synaptic memory and CaMKII (2023) · cites this paper as [249]
This form of plasticity shares many properties with Schaffer collateral LTP, including dependence on NMDARs, Rho GTPase signaling, CaMKII phosphorylation, F-actin polymerization and synaptic AMPAR insertion.
“This form of plasticity shares many properties with Schaffer collateral LTP, including dependence on N-methyl-d-aspartate receptors (NMDARs), Rho GTPase signaling, Ca2+/calmodulin-dependent protein kinase II (CaMKII) phosphorylation, F-actin polymerization and synaptic AMPAR insertion (20–24).”
From Synaptic evidence for the efficacy of spaced learning (2012) · cites this paper as [23]
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Cites
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
Self-citationStructural 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
Hayashi, Y., Shi, S.-H., Esteban, J. A., Piccini, A., Poncer, J.-C., & Malinow, R. (2000) · Science · doi:10.1126/science.287.5461.2262 · Cited by 1,524 · see citing works
Self-citationRapid Spine Delivery and Redistribution of AMPA Receptors After Synaptic NMDA Receptor Activation
Shi, S.-H., Hayashi, Y., Petralia, R. S., Zaman, S. H., Wenthold, R. J., Svoboda, K., & Malinow, R. (1999) · Science · doi:10.1126/science.284.5421.1811 · Cited by 1,276 · see citing works
Self-citationAMPA receptor trafficking at excitatory synapses
Bredt, D. S., & Nicoll, R. A. (2003) · Neuron · doi:10.1016/s0896-6273(03)00640-8 · Cited by 1,150 · see citing works
Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms
Chen, L., Chetkovich, D. M., Petralia, R. S., Sweeney, N. T., Kawasaki, Y., Wenthold, R. J., Bredt, D. S., & Nicoll, R. A. (2000) · Nature · doi:10.1038/35050030 · Cited by 1,111 · 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
Self-citationReceptor 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
Petralia, R. S., & Wenthold, R. J. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903180309 · Cited by 999 · see citing works
The cell biology of synaptic plasticity: AMPA receptor trafficking
Shepherd, J. D., & Huganir, R. L. (2007) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.23.090506.123516 · Cited by 978 · see citing works
Importance of AMPA Receptors for Hippocampal Synaptic Plasticity But Not for Spatial Learning
Zamanillo, D., Sprengel, R., Hvalby, Ø., Jensen, V., Burnashev, N., Rozov, A., Kaiser, K. M. M., Köster, H. J., Borchardt, T., Worley, P., et al. (1999) · Science · doi:10.1126/science.284.5421.1805 · Cited by 791 · see citing works
Postsynaptic signaling and plasticity mechanisms
Sheng, M., & Kim, M. J. (2002) · Science · doi:10.1126/science.1075333 · Cited by 731 · 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
Unusual spectral energy distribution of a galaxy previously reported to be at redshift 6.68
Chen, H., Lanzetta, K. M., Pascarelle, S. M., & Yahata, N. (2000) · RePEc: Research Papers in Economics · Cited by 680 · see citing works
Subunit Composition of Synaptic AMPA Receptors Revealed by a Single-Cell Genetic Approach
Lu, W., Shi, Y., Jackson, A. C., Bjorgan, K., During, M. J., Sprengel, R., Seeburg, P. H., & Nicoll, R. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.027 · Cited by 660 · 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
Locally dynamic synaptic learning rules in pyramidal neuron dendrites
Harvey, C. D., & Svoboda, K. (2007) · Nature · doi:10.1038/nature06416 · Cited by 625 · see citing works
Regulation of AMPA receptor lateral movements
Borgdorff, A. J., & Choquet, D. (2002) · Nature · doi:10.1038/nature00780 · Cited by 542 · 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
Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes
Park, M., Salgado, J. M., Ostroff, L., Helton, T. D., Robinson, C. G., Harris, K. M., & Ehlers, M. D. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.040 · Cited by 493 · see citing works
Specific long-lasting potentiation of synaptic transmission in hippocampal slices
Andersen, P. N., Sundberg, S. H., Sveen, O., & Wigström, H. (1977) · Nature · doi:10.1038/266736a0 · Cited by 489 · 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
Self-citationMyosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity
Wang, Z., Edwards, J. G., Riley, N., Provance, D. W., Karcher, R., Li, X.-D., Davison, I. G., Ikebe, M., Mercer, J. A., Kauer, J. A., et al. (2008) · Cell · doi:10.1016/j.cell.2008.09.057 · Cited by 470 · see citing works
Oh, M. C., Derkach, V. A., Guire, E. S., & Soderling, T. R. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m509677200 · Cited by 456 · 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
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
Ashby, M. C., Maier, S. R., Nishimune, A., & Henley, J. M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1235-06.2006 · Cited by 302 · 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
Surface 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
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
Photoinactivation 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
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
GluR1 Links Structural and Functional Plasticity at Excitatory Synapses
Kopec, C. D., Réal, É., Kessels, H. W. H. G., & Malinow, R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3503-07.2007 · Cited by 220 · see citing works
Self-citationSynaptotagmin-IV modulates synaptic function and long-term potentiation by regulating BDNF release
Dean, C., Liu, H., Dunning, F. M., Chang, P. Y., Jackson, M. B., & Chapman, E. R. (2009) · Nature Neuroscience · doi:10.1038/nn.2315 · Cited by 212 · 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
A GluR1-cGKII Interaction Regulates AMPA Receptor Trafficking
Serulle, Y., Zhang, S., Ninan, I., Puzzo, D., McCarthy, M., Khatri, L., Arancio, O., & Ziff, E. B. (2007) · Neuron · doi:10.1016/j.neuron.2007.09.016 · Cited by 174 · see citing works
Sharma, K., Fong, D. K., & Craig, A. M. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2006.01.010 · Cited by 150 · see citing works
Yang, Y., Wang, X.-B., Frerking, M. E., & Zhou, Q. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802978105 · Cited by 149 · see citing works
Dual role of the exocyst in AMPA receptor targeting and insertion into the postsynaptic membrane
Gerges, N. Z., Backos, D. S., Rupasinghe, C. N., Spaller, M. R., & Esteban, J. A. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601065 · Cited by 147 · see citing works
Fernández-Alfonso, T., & Ryan, T. A. (2008) · Journal of Neurocytology · doi:10.1007/s11068-008-9030-y · Cited by 95 · see citing works
Changes in AMPA receptor currents following LTP induction on rat CA1 pyramidal neurones
Andrásfalvy, B. K., & Magee, J. C. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.065219 · Cited by 70 · see citing works
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Mechanisms of CaMKII action in long-term potentiation
Lisman, J., Yasuda, R., & Raghavachari, S. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3192 · Cited by 1,134 · see citing works
AMPARs and Synaptic Plasticity: The Last 25 Years
Huganir, R. L., & Nicoll, R. A. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.025 · Cited by 968 · see citing works
The AMPA Receptor Code of Synaptic Plasticity
Diering, G. H., & Huganir, R. L. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.018 · Cited by 844 · see citing works
A Brief History of Long-Term Potentiation
Nicoll, R. A. (2017) · Neuron · doi:10.1016/j.neuron.2016.12.015 · Cited by 841 · see citing works
Structural dynamics of dendritic spines in memory and cognition
Kasai, H., Fukuda, M., Watanabe, S., Hayashi-Takagi, A., & Noguchi, J. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.01.001 · Cited by 804 · 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
Structural and Molecular Remodeling of Dendritic Spine Substructures during Long-Term Potentiation
Bosch, M., Castro, J., Saneyoshi, T., Matsuno, H., Sur, M., & Hayashi, Y. (2014) · Neuron · doi:10.1016/j.neuron.2014.03.021 · Cited by 637 · see citing works
Nair, D., Hosy, E., Petersen, J. D., Constals, A., Giannone, G., Choquet, D., & Sibarita, J.-B. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2381-12.2013 · Cited by 617 · see citing works
Regulation of AMPA receptor trafficking and synaptic plasticity
Anggono, V., & Huganir, R. L. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.12.006 · Cited by 588 · see citing works
Unraveling mechanisms of homeostatic synaptic plasticity
Pozo, K., & Goda, Y. (2010) · Neuron · doi:10.1016/j.neuron.2010.04.028 · Cited by 565 · see citing works
Choquet, D., & Triller, A. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.013 · Cited by 514 · see citing works
Synaptic AMPA receptor composition in development, plasticity and disease
Henley, J. M., & Wilkinson, K. A. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.37 · Cited by 506 · see citing works
Izquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453 · see citing works
Lesch, K.-P., & Waider, J. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.013 · Cited by 435 · see citing works
Neural and cellular mechanisms of fear and extinction memory formation
Orsini, C. A., & Maren, S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.12.014 · Cited by 429 · see citing works
Long-Term Potentiation: From CaMKII to AMPA Receptor Trafficking
Herring, B. E., & Nicoll, R. A. (2016) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021014-071753 · Cited by 425 · see citing works
Linking neurodevelopmental and synaptic theories of mental illness through DISC1
Brandon, N. J., & Sawa, A. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn3120 · Cited by 422 · see citing works
CaMKII Triggers the Diffusional Trapping of Surface AMPARs through Phosphorylation of Stargazin
Opazo, P., Labrecque, S., Tigaret, C. M., Frouin, A., Wiseman, P. W., Koninck, P. D., & Choquet, D. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.007 · Cited by 403 · see citing works
The role of AMPA receptors in postsynaptic mechanisms of synaptic plasticity
Chater, T. E., & Goda, Y. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00401 · Cited by 330 · 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
Hippocampal LTP and contextual learning require surface diffusion of AMPA receptors
Penn, A. C., Zhang, C. L., Georges, F., Royer, L., Breillat, C., Hosy, E., Petersen, J. D., Humeau, Y., & Choquet, D. (2017) · Nature · doi:10.1038/nature23658 · Cited by 324 · see citing works
Expression of NMDA receptor-dependent LTP in the hippocampus: bridging the divide
Bliss, T. V., & Collingridge, G. L. (2013) · Molecular Brain · doi:10.1186/1756-6606-6-5 · Cited by 305 · see citing works
Dendritic spines: from structure to in vivo function
Rochefort, N. L., & Konnerth, A. (2012) · The EMBO Reports · doi:10.1038/embor.2012.102 · Cited by 299 · 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
Metabotropic NMDA receptor function is required for NMDA receptor-dependent long-term depression
Nabavi, S., Kessels, H. W. H. G., Alfonso, S., Aow, J., Fox, R., & Malinow, R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219454110 · Cited by 280 · see citing works
Self-citationHDAC4 Governs a Transcriptional Program Essential for Synaptic Plasticity and Memory
Sando, R., Gounko, N., Pieraut, S., Liao, L., Yates, J., & Maximov, A. (2012) · Cell · doi:10.1016/j.cell.2012.09.037 · Cited by 274 · see citing works
Phase separation at the synapse
Chen, X., Wu, X., Wu, H., & Zhang, M. (2020) · Nature Neuroscience · doi:10.1038/s41593-019-0579-9 · Cited by 261 · see citing works
Synaptic Signaling in Learning and Memory
Kennedy, M. B. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016824 · Cited by 270 · see citing works
Homeostatic Scaling Requires Group I mGluR Activation Mediated by Homer1a
Hu, J.-H., Park, J. M., Park, S. J., Xiao, B., Dehoff, M. H., Kim, S., Hayashi, T., Schwarz, M. K., Huganir, R. L., Seeburg, P. H., et al. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.008 · Cited by 263 · 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
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Jurado, S., Goswami, D., Zhang, Y., Molina, A. J. M., Südhof, T. C., & Malenka, R. C. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.029 · Cited by 232 · see citing works
Compartmentalized versus Global Synaptic Plasticity on Dendrites Controlled by Experience
Makino, H., & Malinow, R. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.036 · Cited by 219 · see citing works
Self-citationDoc2 Is a Ca2+ Sensor Required for Asynchronous Neurotransmitter Release
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Plasticity of Spine Structure: Local Signaling, Translation and Cytoskeletal Reorganization
Nakahata, Y., & Yasuda, R. (2018) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2018.00029 · Cited by 209 · see citing works
Stress hormones and AMPA receptor trafficking in synaptic plasticity and memory
Krugers, H. J., Hoogenraad, C. C., & Groc, L. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2913 · Cited by 197 · see citing works
Postsynaptic synaptotagmins mediate AMPA receptor exocytosis during LTP
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Synaptic evidence for the efficacy of spaced learning
Kramár, E. A., Babayan, A. H., Gavin, C. F., Cox, C. D., Jafari, M., Gall, C. M., Rumbaugh, G., & Lynch, G. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1120700109 · Cited by 192 · 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
Fortin, D. A., Davare, M. A., Srivastava, T., Brady, J. D., Nygaard, S. C., Derkach, V. A., & Soderling, T. R. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1746-10.2010 · Cited by 188 · 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
The developmental stages of synaptic plasticity
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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
Lisman, J. E. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0260 · Cited by 165 · see citing works
Twenty Years of SynGAP Research: From Synapses to Cognition
Gamache, T. R., Araki, Y., & Huganir, R. L. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.0420-19.2020 · Cited by 161 · see citing works
Ras and Rap Signaling in Synaptic Plasticity and Mental Disorders
Stornetta, R. L., & Zhu, J. (2010) · The Neuroscientist · doi:10.1177/1073858410365562 · Cited by 159 · see citing works
The interplay between Hebbian and homeostatic synaptic plasticity
Vitureira, N., & Goda, Y. (2013) · Journal of Cell Biology · doi:10.1083/jcb.201306030 · Cited by 152 · see citing works
Routes, destinations and delays: recent advances in AMPA receptor trafficking
Henley, J. M., Barker, E. A., & Glebov, O. O. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.02.004 · Cited by 158 · see citing works
AMPA receptors as drug targets in neurological disease—advantages, caveats, and future outlook
Chang, P. K. ‐., Verbich, D., & McKinney, R. A. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08165.x · Cited by 155 · see citing works
Postsynaptic signaling during plasticity of dendritic spines
Murakoshi, H., & Yasuda, R. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2011.12.002 · Cited by 158 · see citing works
Molecular Mechanisms of Early and Late LTP
Baltaci, S. B., Mogulkoc, R., & Baltaci, A. K. (2019) · Neurochemical Research · doi:10.1007/s11064-018-2695-4 · Cited by 152 · see citing works
Functional organization of postsynaptic glutamate receptors
Scheefhals, N., & MacGillavry, H. D. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.05.002 · Cited by 151 · see citing works
Distinct Initial SNARE Configurations Underlying the Diversity of Exocytosis
Kasai, H., Takahashi, N., & Tokumaru, H. (2012) · Physiological Reviews · doi:10.1152/physrev.00007.2012 · Cited by 150 · see citing works
Kalashnikova, E., Lorca, R. A., Kaur, I., Barisone, G. A., Li, B., Ishimaru, T., Trimmer, J. S., Mohapatra, D. P., & Dı́az, E. (2010) · Neuron · doi:10.1016/j.neuron.2009.12.021 · Cited by 149 · see citing works
Long-term potentiation: Peeling the onion
Nicoll, R. A., & Roche, K. W. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.02.010 · Cited by 146 · see citing works
Serotonin Mediates Cross-Modal Reorganization of Cortical Circuits
Jitsuki, S., Takemoto, K., Kawasaki, T., Tada, H., Takahashi, A., Bécamel, C., Sano, A., Yuzaki, M., Zukin, R. S., Ziff, E. B., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.016 · Cited by 145 · see citing works
Munsie, L. N., Milnerwood, A. J., Seibler, P., Beccano-Kelly, D. A., Tatarnikov, I., Khinda, J., Volta, M., Kadgien, C., Cao, L. P., Tapia, L., et al. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu582 · Cited by 143 · see citing works
Choquet, D. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.2119-18.2018 · Cited by 141 · see citing works
Loweth, J. A., Tseng, K. Y., & Wolf, M. E. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.061 · Cited by 139 · see citing works
Sanderson, J. L., Gorski, J. A., Gibson, E. S., Lam, P., Freund, R. K., Chick, W. S., & Dell'Acqua, M. L. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3326-12.2012 · Cited by 137 · see citing works
“Extrasynaptic AMPARs can move into the PSD in response to PKC and CaMK activation during LTP (Oh et al., 2006; Guire et al., 2008; Makino and Malinow, 2009; Petrini et al., 2009; Opazo et al., 2010; Yang et al., 2010), while protein phosphatases PP1, PP2A, and calcineurin (CaN) (also known as PP2B)…”
BackgroundRetromer Mediates a Discrete Route of Local Membrane Delivery to Dendrites
Choy, R., Park, M., Temkin, P. A., Herring, B. E., Marley, A., Nicoll, R. A., & von Zastrow, M. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.018 · Cited by 137 · see citing works
Converting juvenile into adult plasticity: a role for the brain's extracellular matrix
Gundelfinger, E. D., Frischknecht, R., Choquet, D., & Heine, M. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07253.x · Cited by 136 · see citing works
Compans, B., Camus, C., Kallergi, E., Sposini, S., Martineau, M., Butler, C., Kechkar, A., Klaassen, R. V., Retailleau, N., B, T. J. S. A., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23133-9 · Cited by 136 · see citing works
Mechanisms and Function of Dendritic Exocytosis
Kennedy, M. J., & Ehlers, M. D. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.032 · Cited by 132 · see citing works
Nicoll, R. A., & Schulman, H. (2023) · Physiological Reviews · doi:10.1152/physrev.00034.2022 · Cited by 126 · see citing works
“By tagging AMPARs with a pH-sensitive tag (SEP-GluA1), the insertion of AMPARs into the surface membrane can be directly visualized during LTP-inducing protocols (249, 250, 335, 337, 338, 340).”
BackgroundInfluentialPlasticity of dendritic spines: subcompartmentalization of signaling
Colgan, L. A., & Yasuda, R. (2014) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021113-170400 · Cited by 124 · see citing works
Stress and excitatory synapses: From health to disease
Timmermans, W., Xiong, H., Hoogenraad, C. C., & Krugers, H. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.05.043 · 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
Hu, Z., Yu, D., Gu, Q.-H., Yang, Y., Tu, K., Zhu, J., & Li, Z. (2014) · Nature Communications · doi:10.1038/ncomms4263 · Cited by 117 · see citing works
Chen, Y., Kramár, E. A., Chen, L. Y., Babayan, A. H., Andres, A. L., Gall, C. M., Lynch, G., & Baram, T. Z. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.17 · Cited by 115 · see citing works
Klaassen, R. V., Stroeder, J., Coussen, F., Hafner, A., Petersen, J. D., Renancio, C., Schmitz, L. J. M., Normand, E., Lodder, J. C., Rotaru, D. C., et al. (2016) · Nature Communications · doi:10.1038/ncomms10682 · Cited by 112 · see citing works
Gutierrez-Castellanos, N., Da Silva-Matos, C. M., Zhou, K., Canto, C. B., Renner, M. C., Koene, L. M. C., Ozyildirim, O., Sprengel, R., Kessels, H. W., & De Zeeuw, C. I. (2017) · Neuron · doi:10.1016/j.neuron.2016.11.046 · Cited by 111 · see citing works
Ferrario, C. R., Loweth, J. A., Milovanovic, M., Ford, K. A., Galiñanes, G. L., Heng, L., Tseng, K. Y., & Wolf, M. E. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.021 · Cited by 109 · see citing works
Imaging ERK and PKA Activation in Single Dendritic Spines during Structural Plasticity
Tang, S., & Yasuda, R. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.032 · Cited by 108 · see citing works
Genetic dissection of GABAergic neural circuits in mouse neocortex
Taniguchi, H. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00008 · Cited by 106 · see citing works
Role of nucleus accumbens glutamatergic plasticity in drug addiction
Garzola, G. C. Q. (2013) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s45963 · Cited by 106 · 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
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
Cortical Synaptic AMPA Receptor Plasticity during Motor Learning
Roth, R. H., Cudmore, R. H., Tan, H. L., Hong, I., Zhang, Y., & Huganir, R. L. (2019) · Neuron · doi:10.1016/j.neuron.2019.12.005 · Cited by 103 · 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
AMPA Receptor Trafficking for Postsynaptic Potentiation
Park, M. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00361 · Cited by 102 · see citing works
Park, P., Kang, H., Sanderson, T. M., Bortolotto, Z. A., Georgiou, J., Zhuo, M., Kaang, B., & Collingridge, G. L. (2018) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2018.00042 · Cited by 99 · see citing works
Sumi, T., & Harada, K. (2020) · Scientific Reports · doi:10.1038/s41598-020-71528-3 · Cited by 95 · see citing works
Neurodevelopmental Disorders Associated with PSD-95 and Its Interaction Partners
Levy, A. M., Gómez‐Puertas, P., & Tümer, Z. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23084390 · Cited by 97 · see citing works
Activity Shapes Neural Circuit Form and Function: A Historical Perspective
Pan, Y., & Monje, M. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0740-19.2019 · Cited by 95 · 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
Lü, W., Isozaki, K., Roche, K. W., & Nicoll, R. A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016289107 · Cited by 92 · 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
Assembly of AMPA receptors: mechanisms and regulation
Gan, Q., Salussolia, C. L., & Wollmuth, L. P. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.273755 · Cited by 90 · see citing works
Subunit-specific role for the amino-terminal domain of AMPA receptors in synaptic targeting
Díaz-Alonso, J., Sun, Y. J., Granger, A. J., Levy, J. M., Blankenship, S. M., & Nicoll, R. A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1707472114 · Cited by 89 · see citing works
Learning binds new inputs into functional synaptic clusters via spinogenesis
Hedrick, N. G., Lu, Z., Bushong, E. A., Singhi, S., Nguyen, P., Magaña, Y., Jilani, S., Lim, B. K., Ellisman, M. H., & Komiyama, T. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01086-6 · Cited by 88 · see citing works
Retinoic Acid and LTP Recruit Postsynaptic AMPA Receptors Using Distinct SNARE-Dependent Mechanisms
Arendt, K. L., Zhang, Y., Jurado, S., Malenka, R. C., Südhof, T. C., & Chen, L. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.009 · Cited by 87 · see citing works
Biophysics of Biochemical Signaling in Dendritic Spines: Implications in Synaptic Plasticity
Yasuda, R. (2017) · Biophysical Journal · doi:10.1016/j.bpj.2017.07.029 · Cited by 85 · see citing works
Long-term potentiation in cultured hippocampal neurons
Molnár, E. (2011) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2011.07.017 · Cited by 85 · see citing works
Volk, L., Kim, C.-H., Takamiya, K., Yu, Y., & Huganir, R. L. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016103107 · Cited by 85 · 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
Yang, Y., Wang, X.-B., & Zhou, Q. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913004107 · Cited by 84 · see citing works
- Authors
- Makino, H., & Malinow, R.
- Affiliations
- Cold Spring Harbor Laboratory (US)
- Corresponding author
- Malinow, Roberto
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2009-11
- Volume
- 64
- Issue
- 3
- Pages
- 381-390
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC2999463
- OpenAlex
- W2058113433
- Cited by
- 501
- References
- 41
- Citations by year
- 2026: 16 · 2025: 18 · 2024: 20 · 2023: 12 · 2022: 22 · 2021: 38 · 2020: 39 · 2019: 27 · 2018: 34 · 2017: 35 · 2016: 26 · 2015: 22 · 2014: 41 · 2013: 52 · 2012: 38
- FWCI
- 13.72
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1354 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- Funders
- National Institute on Aging (R01AG032132)
- National Institute of Mental Health (R01MH049159, R37MH049159)
- 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 › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- AMPA receptors, long-term potentiation, receptor trafficking, synaptic plasticity, GluR1, lateral diffusion, exocytosis, hippocampus, memory
- MeSH terms
- Animals, Cell Membrane, Dendrites, Diffusion, Exocytosis, Fluorescence, Hippocampus, Neurons, Synapses, Video Recording, Long-Term Potentiation, Pyramidal Cells, Receptors, AMPA, Intracellular Space, Dendritic Spines, Rats, CA1 Region, Hippocampal, In Vitro Techniques
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