Role of AMPA Receptor Cycling in Synaptic Transmission and Plasticity
Open accessAbstract
Compounds known to disrupt exocytosis or endocytosis were introduced into CA1 pyramidal cells while monitoring excitatory postsynaptic currents (EPSCs). Disrupting exocytosis or the interaction of GluR2 with NSF caused a gradual reduction in the AMPAR EPSC, while inhibition of endocytosis caused a gradual increase in the AMPAR EPSC. These manipulations had no effect on the NMDAR EPSC but prevented the subsequent induction of LTD. These results suggest that AMPARs, but not NMDARs, cycle into and out of the synaptic membrane at a rapid rate and that certain forms of synaptic plasticity may utilize this dynamic process.
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
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.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Glutamate receptors put in their place
Sheng, M. (1997) · Nature · doi:10.1038/386221a0 · Cited by 81 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- [1]1. Allison, D.W ∙ Gelfand, V.I ∙ Spector, I ... Role of actin in anchoring postsynaptic receptors in cultured hippocampal neuronsdifferential attachment of NMDA versus AMPA receptors J. Neurosci. 1998; 18:2423-2436 Crossref PubMed Google Scholar
- [2]2. Barria, A ∙ Muller, D ∙ Derkach, V ... Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation Science. 1997; 276:2042-2045 Crossref Scopus (910) PubMed Google Scholar
- [3]3. Baude, A ∙ Nusser, Z ∙ Molnár, E ... High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus Neuroscience. 1995; 69:1031-1055
Cited by
Sorted by citations
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-citationMatsuzaki, M., Ellis-Davies, G. C. R., Nemoto, T., Miyashita, Y., Iino, M., & Kasai, H. (2001) · Nature Neuroscience · doi:10.1038/nn736 · Cited by 1,563 · see citing works
Control of Synaptic Strength by Glial TNFα
Beattie, E. C., Stellwagen, D., Morishita, W., Bresnahan, J. C., Ha, B. K., Von Zastrow, M., Beattie, M. S., & Malenka, R. C. (2002) · Science · doi:10.1126/science.1067859 · Cited by 1,344 · see citing works
Self-citationNMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD).
Luscher, C., & Malenka, R. C. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005710 · Cited by 1,110 · see citing works
Self-citationShi, 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
AMPAR Removal Underlies Aβ-Induced Synaptic Depression and Dendritic Spine Loss
Hsieh, H., Boehm, J., Sato, C., Iwatsubo, T., Tomita, T., Sisodia, S., & Malinow, R. (2006) · Neuron · doi:10.1016/j.neuron.2006.10.035 · Cited by 1,042 · 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
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
Self-citationDifferential Regulation of AMPA Receptor and GABA Receptor Trafficking by Tumor Necrosis Factor-α
Stellwagen, D., Beattie, E. C., Seo, J. Y., & Malenka, R. C. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4486-04.2005 · Cited by 985 · see citing works
“Transverse hippocampal slices (400 m) were prepared from 2- to 4-week-old Sprague Dawley rats as described previously (Luscher et al., 1999).”
MethodSelf-citationActivity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system
Ehlers, M. D. (2003) · Nature Neuroscience · doi:10.1038/nn1013 · Cited by 977 · see citing works
The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity
Isaac, J. T. R., Ashby, M. C., & McBain, C. J. (2007) · Neuron · doi:10.1016/j.neuron.2007.06.001 · Cited by 802 · see citing works
Arc/Arg3.1 Mediates Homeostatic Synaptic Scaling of AMPA Receptors
Shepherd, J. D., Rumbaugh, G., Wu, J., Chowdhury, S., Plath, N., Kuhl, D., Huganir, R. L., & Worley, P. F. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.034 · Cited by 779 · 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
Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD
Beattie, E. C., Carroll, R. C., Yu, X., Morishita, W., Yasuda, H., von Zastrow, M., & Malenka, R. C. (2000) · Nature Neuroscience · doi:10.1038/81823 · Cited by 745 · see citing works
Self-citationSubunit-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
Ubiquitination Regulates PSD-95 Degradation and AMPA Receptor Surface Expression
Colledge, M., Snyder, E. M., Crozier, R. A., Soderling, J. A., Jin, Y., Langeberg, L. K., Lu, H., Bear, M. F., & Scott, J. D. (2003) · Neuron · doi:10.1016/s0896-6273(03)00687-1 · Cited by 567 · see citing works
Molecular determinants of NMDA receptor internalization
Roche, K. W., Standley, S., McCallum, J., Dune Ly, C., Ehlers, M. D., & Wenthold, R. J. (2001) · Nature Neuroscience · doi:10.1038/90498 · Cited by 550 · 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
Izquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453 · see citing works
Postnatal synaptic potentiation: delivery of GluR4-containing AMPA receptors by spontaneous activity
Zhu, J. J., Esteban, J. A., Hayashi, Y., & Malinow, R. (2000) · Nature Neuroscience · doi:10.1038/80614 · Cited by 437 · see citing works
How does PKMζ maintain long-term memory?
Sacktor, T. C. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn2949 · Cited by 431 · see citing works
Bhatt, D. H., Zhang, S., & Gan, W.-B. (2009) · Annual Review of Physiology · doi:10.1146/annurev.physiol.010908.163140 · Cited by 380 · see citing works
Long-term synaptic plasticity in hippocampal interneurons
Kullmann, D. M., & Lamsa, K. P. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2207 · Cited by 340 · see citing works
Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse
Hooks, B. M., & Chen, C. (2006) · Neuron · doi:10.1016/j.neuron.2006.07.007 · Cited by 311 · see citing works
Visualization of changes in presynaptic function during long-term synaptic plasticity
Zakharenko, S. S., Zablow, L., & Siegelbaum, S. A. (2001) · Nature Neuroscience · doi:10.1038/89498 · Cited by 305 · see citing works
NMDA Receptor Content of Synapses in Stratum Radiatum of the Hippocampal CA1 Area
Racca, C., Stephenson, F. A., Streit, P., Roberts, J. D. B., & Somogyi, P. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-07-02512.2000 · Cited by 304 · 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
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
Krapivinsky, G., Medina, I., Krapivinsky, L., Gapon, S., & Clapham, D. E. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.003 · Cited by 287 · see citing works
Ahmadian, G., Ju, W., Liu, L., Wyszynski, M., Lee, S. H., Dunah, A. W., Taghibiglou, C., Wang, Y., Lu, J., Wong, T. P., et al. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600126 · Cited by 296 · 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
Synaptic transmission and plasticity in the absence of AMPA glutamate receptor GluR2 and GluR3
Meng, Y., Zhang, Y., & Jia, Z. (2003) · Neuron · doi:10.1016/s0896-6273(03)00368-4 · Cited by 251 · 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
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 · see citing works
Regulation of Synaptic Strength by Protein Phosphatase 1
Morishita, W., Connor, J. H., Xia, H., Quinlan, E. M., Shenolikar, S., & Malenka, R. C. (2001) · Neuron · doi:10.1016/s0896-6273(01)00554-2 · Cited by 227 · see citing works
Self-citationSeidenman, K. J., Steinberg, J. P., Huganir, R., & Malinow, R. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-27-09220.2003 · Cited by 225 · see citing works
Activity-Dependent Regulation of Synaptic AMPA Receptor Composition and Abundance by β3 Integrins
Cingolani, L. A., Thalhammer, A., Yu, L. M. Y., Catalano, M., Ramos, T., Colicos, M. A., & Goda, Y. (2008) · Neuron · doi:10.1016/j.neuron.2008.04.011 · Cited by 223 · see citing works
Hippocampal long-term depression mediates spatial reversal learning in the Morris water maze
Dong, Z., Bai, Y., Wu, X., Li, H., Gong, B., Howland, J. G., Huang, Y., He, W., Li, T., & Wang, Y. T. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.06.027 · Cited by 219 · see citing works
Chapter 2 PKMζ, LTP maintenance, and the dynamic molecular biology of memory storage
Sacktor, T. C. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(07)00002-7 · Cited by 208 · 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
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
Mechanisms of synaptic depression triggered by metabotropic glutamate receptors
Bellone, C., Lüscher, C., & Mameli, M. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8263-3 · Cited by 150 · see citing works
Self-citationPlasticity 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
Hashimotodani, Y., Nasrallah, K., Jensen, K. R., Chávez, A. E., Carrera, D., & Castillo, P. E. (2017) · Neuron · doi:10.1016/j.neuron.2017.07.028 · Cited by 104 · see citing works
<i>Sapap3</i> Deletion Causes mGluR5-Dependent Silencing of AMPAR Synapses
Wan, Y., Feng, G., & Calakos, N. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.2533-11.2011 · Cited by 101 · see citing works
Kastning, K., Kukhtina, V., Kittler, J. T., Chen, G., Pechstein, A., Enders, S., Lee, S. H., Sheng, M., Yan, Z., & Haucke, V. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611170104 · Cited by 88 · see citing works
Two Loci of Expression for Long-Term Depression at Hippocampal Mossy Fiber-Interneuron Synapses
Lei, S., & McBain, C. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4645-03.2004 · Cited by 85 · see citing works
Bell, R. L., Hauser, S. R., McClintick, J., Rahman, S., Edenberg, H. J., Szumlinski, K. K., & McBride, W. J. (2016) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2015.10.018 · Cited by 65 · see citing works
How to scale down postsynaptic strength
Tatavarty, V., Sun, Q., & Turrigiano, G. G. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1676-13.2013 · Cited by 50 · see citing works
Targeting metaplasticity mechanisms to promote sustained antidepressant actions
Brown, K. A., & Gould, T. D. (2024) · Molecular Psychiatry · doi:10.1038/s41380-023-02397-1 · Cited by 49 · see citing works
Migues, P. V., Hardt, O., Finnie, P., Wang, Y. W., & Nader, K. (2014) · Hippocampus · doi:10.1002/hipo.22295 · Cited by 33 · see citing works
- Authors
- Lüscher, C., Xia, H., Beattie, E. C., Carroll, R. C., von Zastrow, M., Malenka, R. C., & Nicoll, R. A.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Nicoll, Roger A
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 1999-11
- Volume
- 24
- Issue
- 3
- Pages
- 649-658
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2039959072
- Cited by
- 692
- References
- 1
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 5 · 2023: 6 · 2022: 6 · 2021: 19 · 2020: 12 · 2019: 15 · 2018: 18 · 2017: 12 · 2016: 18 · 2015: 15 · 2014: 25 · 2013: 21 · 2012: 24
- FWCI
- 17.93
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Human Frontier Science Program
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- National Institutes of Health
- Bristol-Myers Squibb
- 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 › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- synaptic transmission, synaptic plasticity, long-term depression, exocytosis, endocytosis, GluR2, NSF, excitatory postsynaptic currents, NMDA receptor, CA1 pyramidal neurons, hippocampus
- MeSH terms
- Animals, Carrier Proteins, Endocytosis, Exocytosis, Synaptic Transmission, Neuronal Plasticity, Synapses, Rats, Sprague-Dawley, Long-Term Potentiation, Receptors, AMPA, Vesicular Transport Proteins, Rats, N-Ethylmaleimide-Sensitive Proteins, 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
