The DOI matches its Crossref record; 41 of the 41 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“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
The cited source says what the claim attributes to it.
In the citing paper
“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]
The cited source says what the claim attributes to it.
In the citing paper
“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]
The cited source says what the claim attributes to it.
In the citing paper
“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]
The cited source says what the claim attributes to it.
In the citing paper
“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]
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
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
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 2,483
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
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
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
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
Shi, S.-H., Hayashi, Y., Esteban, J. A., & Malinow, R. (2001) · Cell · doi:10.1016/s0092-8674(01)00321-x · Cited by 1,094
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
Petralia, R. S., & Wenthold, R. J. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903180309 · Cited by 1,003
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
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
Postsynaptic signaling and plasticity mechanisms
Sheng, M., & Kim, M. J. (2002) · Science · doi:10.1126/science.1075333 · Cited by 731
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
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
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
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
Locally dynamic synaptic learning rules in pyramidal neuron dendrites
Harvey, C. D., & Svoboda, K. (2007) · Nature · doi:10.1038/nature06416 · Cited by 625
Regulation of AMPA receptor lateral movements
Borgdorff, A. J., & Choquet, D. (2002) · Nature · doi:10.1038/nature00780 · Cited by 542
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
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
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
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
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
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
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
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
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
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
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
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
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
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 226
Self-citationSpine 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
Synaptotagmin-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 214
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
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
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 156
Sharma, K., Fong, D. K., & Craig, A. M. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2006.01.010 · Cited by 150
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
Fernández-Alfonso, T., & Ryan, T. A. (2008) · Journal of Neurocytology · doi:10.1007/s11068-008-9030-y · Cited by 95
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 71
Flagged first, then by citations
Cited by
Sorted by citations
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
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
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
A Brief History of Long-Term Potentiation
Nicoll, R. A. (2017) · Neuron · doi:10.1016/j.neuron.2016.12.015 · Cited by 841
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
Metadata
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
