Receptor trafficking and synaptic plasticity
Abstract
Long-term potentiation and long-term depression are processes that have been widely studied to understand the molecular basis of information storage in the brain. Glutamate receptors are required for the induction and expression of these forms of plasticity, and GABA (gamma-aminobutyric acid) receptors are involved in their modulation. Recent insights into how these receptors are rapidly moved into and out of synaptic membranes has profound implications for our understanding of the mechanisms of long-term potentiation and long-term depression.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Long-term potentiation (LTP) is brief repetitive synaptic stimulation that results in long-lasting increases in synaptic strength.
“long-term potentiation (LTP), in which brief repetitive synaptic stimulation results in long-lasting increases in synaptic strength, was gaining popularity as a cellular model for learning and memory (16–22).”
From Synaptic memory and CaMKII (2023) · cites this paper as [16]
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
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
PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity
Esteban, J. A., Shi, S.-H., Wilson, C., Nuriya, M., Huganir, R. L., & Malinow, R. (2003) · Nature Neuroscience · doi:10.1038/nn997 · Cited by 894 · 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
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
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
Regulation of AMPA receptor lateral movements
Borgdorff, A. J., & Choquet, D. (2002) · Nature · doi:10.1038/nature00780 · Cited by 542 · see citing works
Subunit-Specific NMDA Receptor Trafficking to Synapses
Barria, A., & Malinow, R. (2002) · Neuron · doi:10.1016/s0896-6273(02)00776-6 · Cited by 515 · see citing works
Stein, V., House, D. R. C., Bredt, D. S., & Nicoll, R. A. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05503.2003 · Cited by 341 · see citing works
Kittler, J. T., & Moss, S. J. (2003) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(03)00064-3 · Cited by 301 · cited 1× · see citing works
“There is also growing evidence that GABA A Rs are rapidly inserted and removed at synapses and that this process is important in the regulation of synaptic inhibitio”
BackgroundAhmadian, 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
Self-citationJovanovic, J. N., Thomas, P., Kittler, J. T., Smart, T. G., & Moss, S. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.3606-03.2004 · Cited by 273 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Glutamate Receptor Ion Channels: Structure, Regulation, and Function
Traynelis, S. F., Wollmuth, L. P., McBain, C. J., Menniti, F. S., Vance, K. M., Ogden, K. K., Hansen, K. B., Yuan, H., Myers, S. J., & Dingledine, R. (2010) · Pharmacological Reviews · doi:10.1124/pr.109.002451 · Cited by 3,568 · see citing works
Neurosteroids: endogenous regulators of the GABAA receptor
Belelli, D., & Lambert, J. J. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1703 · Cited by 1,159 · see citing works
NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders
Lau, C. G., & Zukin, R. S. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2153 · Cited by 1,159 · see citing works
NMDA 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
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
Long-term depression in the CNS
Collingridge, G. L., Peineau, S., Howland, J. G., & Wang, Y. T. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2867 · Cited by 926 · see citing works
Self-citationVyazovskiy, V. V., Cirelli, C., Pfister-Genskow, M., Faraguna, U., & Tononi, G. (2008) · Nature Neuroscience · doi:10.1038/nn2035 · Cited by 837 · 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
Self-citationPostsynaptic receptor trafficking underlying a form of associative learning
Rumpel, S., LeDoux, J., Zador, A., & Malinow, R. (2005) · Science · doi:10.1126/science.1103944 · Cited by 775 · see citing works
Regulatory mechanisms of AMPA receptors in synaptic plasticity
Derkach, V. A., Oh, M. C., Guire, E. S., & Soderling, T. R. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2055 · Cited by 708 · see citing works
Amyloid beta oligomers induce impairment of neuronal insulin receptors
Zhao, W., De Felice, F. G., Fernandez, S., Chen, H., Lambert, M. P., Quon, M. J., Krafft, G. A., & Klein, W. L. (2008) · The FASEB Journal · doi:10.1096/fj.06-7703com · Cited by 587 · 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
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
Synthetic amyloid-β oligomers impair long-term memory independently of cellular prion protein
Balducci, C., Beeg, M., Stravalaci, M., Bastone, A., Sclip, A., Biasini, E., Tapella, L., Colombo, L., Manzoni, C., Borsello, T., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911829107 · Cited by 466 · 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
Tartt, A. N., Mariani, M. B., Hen, R., Mann, J. J., & Boldrini, M. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01520-y · Cited by 408 · see citing works
“Intracellular calcium activates protein kinases responsible for enhancing synaptic communication efficiency through increasing sodium conductance [136, 137] (Fig.”
BackgroundLTP requires a reserve pool of glutamate receptors independent of subunit type
Granger, A. J., Shi, Y., Lu, W., Cerpas, M., & Nicoll, R. A. (2013) · Nature · doi:10.1038/nature11775 · Cited by 313 · see citing works
Man, H.-Y., Sekine-Aizawa, Y., & Huganir, R. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611698104 · Cited by 311 · 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
CaMKII: a biochemical bridge linking accumbens dopamine and glutamate systems in cocaine seeking
Anderson, S. M., Famous, K. R., Sadri-Vakili, G., Kumaresan, V., Schmidt, H. D., Bass, C. E., Terwilliger, E. F., Cha, J.-H. J., & Pierce, R. C. (2008) · Nature Neuroscience · doi:10.1038/nn2054 · Cited by 295 · see citing works
Shehata, M., Matsumura, H., Okubo-Suzuki, R., Ohkawa, N., & Inokuchi, K. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.4533-11.2012 · Cited by 285 · see citing works
The Jak/STAT pathway is involved in synaptic plasticity
Nicolas, C. S., Peineau, S., Amici, M., Csaba, Z., Fafouri, A., Javalet, C., Collett, V. J., Hildebrandt, L., Seaton, G., Choi, S.-L., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.024 · Cited by 246 · 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
Regulation of AMPA receptor surface diffusion by PSD-95 slots
Opazo, P., Sainlos, M., & Choquet, D. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.10.010 · Cited by 234 · see citing works
Serotonin 5-HT1A Receptors Regulate NMDA Receptor Channels through a Microtubule-Dependent Mechanism
Yuen, E. Y. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1187-05.2005 · Cited by 225 · see citing works
Groc, L., Choquet, D., Stephenson, F. A., Verrier, D., Manzoni, O. J., & Chavis, P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1772-07.2007 · Cited by 225 · 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
Self-citationDendritic Spine Pathology in Neurodegenerative Diseases
Herms, J., & Dorostkar, M. M. (2016) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-012615-044216 · Cited by 201 · see citing works
A critical role for PSD-95/AKAP interactions in endocytosis of synaptic AMPA receptors
Bhattacharyya, S., Biou, V., Xu, W., Schlüter, O., & Malenka, R. C. (2009) · Nature Neuroscience · doi:10.1038/nn.2249 · Cited by 185 · see citing works
Deregulation of excitatory neurotransmission underlying synapse failure in Alzheimer's disease
Paula‐Lima, A. C., Brito‐Moreira, J., & Ferreira, S. T. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12304 · Cited by 170 · see citing works
Regulation of NMDA receptor Ca2+ signalling and synaptic plasticity
Lau, C. G., Takeuchi, K., Rodenas-Ruano, A., Takayasu, Y., Murphy, J., Bennett, M. V. L., & Zukin, R. S. (2009) · Biochemical Society Transactions · doi:10.1042/bst0371369 · Cited by 138 · see citing works
Postsynaptic Complexin Controls AMPA Receptor Exocytosis during LTP
Ahmad, M., Polepalli, J. S., Goswami, D., Yang, X., Kaeser-Woo, Y. J., Südhof, T. C., & Malenka, R. C. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.020 · Cited by 133 · see citing works
GKAP orchestrates activity-dependent postsynaptic protein remodeling and homeostatic scaling
Shin, S. M., Zhang, N., Hansen, J., Gerges, N. Z., Pak, D. T. S., Sheng, M., & Lee, S. H. (2012) · Nature Neuroscience · doi:10.1038/nn.3259 · Cited by 126 · see citing works
Nicoll, R. A., & Schulman, H. (2023) · Physiological Reviews · doi:10.1152/physrev.00034.2022 · Cited by 126 · see citing works
Ketamine amplifies induced gamma frequency oscillations in the human cerebral cortex
Shaw, A. D., Saxena, N., E. Jackson, L., Hall, J. E., Singh, K. D., & Muthukumaraswamy, S. D. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.04.012 · Cited by 122 · see citing works
SNAP-25 is a target of protein kinase C phosphorylation critical to NMDA receptor trafficking
Lau, C. G., Takayasu, Y., Rodenas-Ruano, A., Paternain, A. V., Lerma, J., Bennett, M. V. L., & Zukin, R. S. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4933-08.2010 · Cited by 120 · see citing works
Aleksandrova, L. R., Wang, Y. T., & Phillips, A. G. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.07.007 · Cited by 114 · see citing works
Self-citationHeise, C., Gardoni, F., Culotta, L., di Luca, M., Verpelli, C., & Sala, C. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00035 · Cited by 99 · see citing works
Ho, M. T.-W., Pelkey, K. A., Topolnik, L., Petralia, R. S., Takamiya, K., Xia, J., Huganir, R. L., Lacaille, J.-C., & McBain, C. J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2671-07.2007 · Cited by 98 · see citing works
Araki, Y., Lin, D.-T., & Huganir, R. L. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1006584107 · Cited by 92 · see citing works
Mills, F., Bartlett, T. E., Dissing-Olesen, L., Wisniewska, M. B., Kuznicki, J., Macvicar, B. A., Wang, Y. T., & Bamji, S. X. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1404670111 · Cited by 82 · see citing works
Self-citationBell, 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
Sheng, N., Bemben, M. A., Díaz-Alonso, J., Tao, W., Shi, Y. S., & Nicoll, R. A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800719115 · Cited by 65 · see citing works
Barriers in the brain: resolving dendritic spine morphology and compartmentalization
Adrian, M., Kusters, R., Wierenga, C. J., Storm, C., Hoogenraad, C. C., & Kapitein, L. C. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00142 · Cited by 62 · see citing works
“Controlled addition and removal of AMPA-type glutamate receptors from the postsynaptic density is believed to underlie the changes in synaptic strength during learning and memory formation (Malinow and Malenka, 2002; Sheng and Kim, 2002; Bredt and Nicoll, 2003; Collingridge et al., 2004).”
Delgado, J. Y., Coba, M., Anderson, C. N. G., Thompson, K. R., Gray, E. E., Heusner, C. L., Martin, K. C., Grant, S. G. N., & O'Dell, T. J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3056-07.2007 · Cited by 62 · see citing works
Potier, M., Georges, F., Brayda-Bruno, L., Ladépêche, L., Lamothe, V., Al Abed, A. S., Groc, L., & Marighetto, A. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.07.017 · Cited by 61 · see citing works
Mechanisms underlying nontoxic indoor air health problems: A review
Nordin, S. (2020) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2020.113489 · Cited by 58 · see citing works
Han, M., Ban, J.-J., Bae, J.-S., Shin, C.-Y., Lee, D. H., & Chung, J. H. (2017) · Scientific Reports · doi:10.1038/s41598-017-15773-z · Cited by 54 · see citing works
Insulin, Synaptic Function, and Opportunities for Neuroprotection
Mielke, J. G., & Wang, Y.-T. (2011) · Progress in Molecular Biology and Translational Science · doi:10.1016/b978-0-12-385506-0.00004-1 · Cited by 55 · see citing works
Self-citationHu, P., Liu, J., Yasrebi, A., Gotthardt, J. D., Bello, N. T., Pang, Z. P., & Roepke, T. A. (2016) · Endocrinology · doi:10.1210/en.2016-1191 · Cited by 40 · see citing works
Schmidt, H. D., Kimmey, B. A., Arreola, A. C., & Pierce, R. C. (2015) · Addiction Biology · doi:10.1111/adb.12122 · Cited by 38 · see citing works
The Neuronal Actions of Leptin and the Implications for Treating Alzheimer’s Disease
Hamilton, K., & Harvey, J. (2021) · Pharmaceuticals · doi:10.3390/ph14010052 · Cited by 36 · see citing works
Regulation of glutamate receptors by striatal‐enriched tyrosine phosphatase 61 (STEP<sub>61</sub>)
Won, S., & Roche, K. W. (2021) · The Journal of Physiology · doi:10.1113/jp278703 · Cited by 34 · see citing works
Synaptic refinement during development and its effect on slow-wave activity: a computational study
Hoel, E. P., Albantakis, L., Cirelli, C., & Tononi, G. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00812.2015 · Cited by 30 · see citing works
Liu, H.-P., Lin, W.-Y., Liu, S.-H., Wang, W.-F., Tsai, C.-H., Wu, B.-T., Wang, C.-K., & Tsai, F.-J. (2009) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000254757 · Cited by 29 · see citing works
Munk, A., Reme, S. E., & Jacobsen, H. B. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.630422 · Cited by 16 · see citing works
Molecular organization and assembly of the postsynaptic density of excitatory brain synapses.
Kim, E., & Ko, J. (2006) · Results and Problems in Cell Differentiation · doi:10.1007/400_011 · Cited by 11 · see citing works
- Authors
- Collingridge, G. L., Isaac, J. T. R., & Wang, Y. T.
- Affiliations
- University of British Columbia Hospital (CA)
- National Institutes of Health (US)
- Corresponding author
- Collingridge, Graham L.
- Venue
- Nature Reviews Neuroscience
- Published
- 2004-12
- Volume
- 5
- Issue
- 12
- Pages
- 952-962
- ISSN
- 1471-003X (ISSN-L)
- 1471-0048
- OpenAlex
- W2079302576
- Cited by
- 1,046
- References
- 12
- Citations by year
- 2026: 14 · 2025: 31 · 2024: 26 · 2023: 24 · 2022: 31 · 2021: 42 · 2020: 46 · 2019: 29 · 2018: 47 · 2017: 48 · 2016: 37 · 2015: 43 · 2014: 50 · 2013: 72 · 2012: 66
- FWCI
- 5.03
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature reviews. Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- Royal Society
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
- Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
- Keywords
- receptor trafficking, synaptic plasticity, long-term potentiation, long-term depression, glutamate receptors, GABA receptors, synaptic membranes, information storage, synaptic modulation
- MeSH terms
- Animals, Humans, Neuronal Plasticity, Synapses, Receptors, Glutamate, Receptors, GABA, Protein Transport
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
