Postsynaptic Complexin Controls AMPA Receptor Exocytosis during LTP
Open accessAbstract
Long-term potentiation (LTP) is a compelling synaptic correlate of learning and memory. LTP induction requires NMDA receptor (NMDAR) activation, which triggers SNARE-dependent exocytosis of AMPA receptors (AMPARs). However, the molecular mechanisms mediating AMPAR exocytosis induced by NMDAR activation remain largely unknown. Here, we show that complexin, a protein that regulates neurotransmitter release via binding to SNARE complexes, is essential for AMPAR exocytosis during LTP but not for the constitutive AMPAR exocytosis that maintains basal synaptic strength. The regulated postsynaptic AMPAR exocytosis during LTP requires binding of complexin to SNARE complexes. In hippocampal neurons, presynaptic complexin acts together with synaptotagmin-1 to mediate neurotransmitter release. However, postsynaptic synaptotagmin-1 is not required for complexin-dependent AMPAR exocytosis during LTP. These results suggest a complexin-dependent molecular mechanism for regulating AMPAR delivery to synapses, a mechanism that is surprisingly similar to presynaptic exocytosis but controlled by regulators other than synaptotagmin-1.
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.
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?
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 [333]
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
Long-Term Potentiation--A Decade of Progress?
Malenka, R. C., & Nicoll, A. R. A. (1999) · Science · doi:10.1126/science.285.5435.1870 · Cited by 2,729 · see citing works
Self-citationAMPA 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-citationSüdhof, T. C. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131412 · Cited by 2,491 · see citing works
Self-citationSNAREpins: Minimal Machinery for Membrane Fusion
Weber, T., Zemelman, B. V., McNew, J. A., Westermann, B., Gmachl, M., Parlati, F., Söllner, T. H., & Rothman, J. E. (1998) · Cell · doi:10.1016/s0092-8674(00)81404-x · Cited by 2,481 · see citing works
Membrane Fusion: Grappling with SNARE and SM Proteins
Südhof, T. C., & Rothman, J. E. (2009) · Science · doi:10.1126/science.1161748 · Cited by 2,027 · see citing works
Self-citationGermline Transmission and Tissue-Specific Expression of Transgenes Delivered by Lentiviral Vectors
Lois, C., Hong, E. J., Pease, S., Brown, E. J., & Baltimore, D. (2002) · Science · doi:10.1126/science.1067081 · Cited by 1,974 · see citing works
Synaptotagmin I: A major Ca2+ sensor for transmitter release at a central synapse
Geppert, M., Goda, Y., Hammer, R. E., Li, C., Rosahl, T. W., Stevens, C. F., & Südhof, T. C. (1994) · Cell · doi:10.1016/0092-8674(94)90556-8 · Cited by 1,483 · see citing works
Self-citationSynaptic plasticity and addiction
Kauer, J. A., & Malenka, R. C. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2234 · Cited by 1,397 · see citing works
Self-citationPDZ Domains and the Organization of Supramolecular Complexes
Sheng, M., & Sala, C. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1 · Cited by 1,191 · see citing works
AMPA 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
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
Lu, W.-Y., Man, H.-Y., Ju, W., Trimble, W., Macdonald, J., & Wang, Y.-T. (2001) · Neuron · doi:10.1016/s0896-6273(01)00194-5 · Cited by 978 · 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
Synaptotagmin I functions as a calcium regulator of release probability
Fernández-Chacón, R., Königstorfer, A., Gerber, S. H., García, J., Matos, M. F., Stevens, C. F., Brose, N., Rizo, J., Rosenmund, C., & Südhof, T. C. (2001) · Nature · doi:10.1038/35065004 · Cited by 961 · see citing works
Self-citationRecycling 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
SNARE Function Analyzed in Synaptobrevin/VAMP Knockout Mice
Schoch, S., Deák, F., Königstorfer, A., Mozhayeva, M. G., Sara, Y., Südhof, T. C., & Kavalali, E. T. (2001) · Science · doi:10.1126/science.1064335 · Cited by 664 · 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
Rizo, J., & Rosenmund, C. (2008) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1450 · Cited by 538 · see citing works
Complexins Regulate a Late Step in Ca2+-Dependent Neurotransmitter Release
Reim, K., Mansour, M., Varoqueaux, F., McMahon, H. T., Südhof, T. C., Brose, N., & Rosenmund, C. (2001) · Cell · doi:10.1016/s0092-8674(01)00192-1 · Cited by 500 · see citing works
Self-citationComplexins: cytosolic proteins that regulate SNAP receptor function.
McMahon, H., Missler, M., Li, C., & Südhof, T. (1995) · Cell · doi:10.1016/0092-8674(95)90239-2 · Cited by 497 · see citing works
Self-citationA complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis.
Tang, J., Maximov, A., Shin, O., Dai, H., Rizo, J., & Südhof, T. (2006) · Cell · doi:10.1016/j.cell.2006.08.030 · Cited by 467 · see citing works
Self-citationPostsynaptic organisation and regulation of excitatory synapses
Scannevin, R. H., & Huganir, R. L. (2000) · Nature reviews. Neuroscience · doi:10.1038/35039075 · Cited by 460 · 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
Self-citationA Clamping Mechanism Involved in SNARE-Dependent Exocytosis
Giraudo, C. G., Eng, W. S., Melia, T. J., & Rothman, J. E. (2006) · Science · doi:10.1126/science.1129450 · Cited by 368 · see citing works
ORGANELLES AND TRAFFICKING MACHINERY FOR POSTSYNAPTIC PLASTICITY
Kennedy, M. J., & Ehlers, M. D. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112808 · Cited by 346 · see citing works
Complexin Controls the Force Transfer from SNARE Complexes to Membranes in Fusion
Maximov, A., Tang, J., Yang, X., Pang, Z. P., & Südhof, T. C. (2009) · Science · doi:10.1126/science.1166505 · Cited by 339 · see citing works
Self-citationXu, J., Mashimo, T., & Südhof, T. C. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.004 · Cited by 336 · see citing works
Self-citationPetrini, E. M., Lü, J., Cognet, L., Lounis, B., Ehlers, M., & Choquet, D. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.025 · Cited by 296 · 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
A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth
Huntwork, S., & Littleton, J. T. (2007) · Nature Neuroscience · doi:10.1038/nn1980 · Cited by 292 · see citing works
Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins
Elias, G. M., & Nicoll, R. A. (2007) · Trends in Cell Biology · doi:10.1016/j.tcb.2007.07.005 · Cited by 288 · 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
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
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
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
Schonn, J., Maximov, A., Lao, Y., Südhof, T. C., & Sørensen, J. B. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712373105 · Cited by 186 · see citing works
Self-citationA 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
Self-citationSelective Interaction of Complexin with the Neuronal SNARE Complex
Pabst, S., Hazzard, J. W., Antonin, W., Südhof, T. C., Jahn, R., Rizo, J., & Fasshauer, D. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m002571200 · Cited by 172 · see citing works
Self-citationRoutes, 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
A neuronal role for SNAP-23 in postsynaptic glutamate receptor trafficking
Suh, Y. H., Terashima, A., Petralia, R. S., Wenthold, R. J., Isaac, J. T. R., Roche, K. W., & Roche, P. A. (2010) · Nature Neuroscience · doi:10.1038/nn.2488 · Cited by 153 · see citing works
Yang, X., Kaeser-Woo, Y. J., Pang, Z., Xu, W., & Südhof, T. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.001 · Cited by 152 · see citing works
Self-citationYang, 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
Xue, M., Qi, L. Y., Pan, H., Reim, K., Deng, H., Bellen, H. J., & Rosenmund, C. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.043 · Cited by 138 · see citing works
Xue, M., Stradomska, A., Chen, H., Brose, N., Zhang, W., Rosenmund, C., & Reim, K. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803012105 · Cited by 137 · 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
Calmodulin Controls Synaptic Strength via Presynaptic Activation of Calmodulin Kinase II
Pang, Z. P., Cao, P., Xu, W., & Südhof, T. C. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3129-09.2010 · Cited by 106 · see citing works
Self-citationComplexin II plays a positive role in Ca 2+ -triggered exocytosis by facilitating vesicle priming
Cai, H., Reim, K., Varoqueaux, F., Tapechum, S., Hill, K., Sørensen, J. B., Brose, N., & Chow, R. H.-P. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810232105 · Cited by 82 · see citing works
Reduced hippocampal LTP in mice lacking a presynaptic protein: complexin II
Takahashi, S., Ujihara, H., Huang, G., Yagyu, K., Sanbo, M., Kaba, H., & Yagi, T. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00652.x · Cited by 78 · see citing works
Yamada, M., Saisu, H., Ishizuka, T., Takahashi, H., & Abe, T. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00104-9 · Cited by 62 · see citing works
Huang, G.-Z., Ujihara, H., Takahashi, S., Kaba, H., Yagi, T., & Inoue, S. (2000) · The Japanese Journal of Pharmacology · doi:10.1254/jjp.84.179 · Cited by 21 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Insular Cortex is Critical for the Perception, Modulation, and Chronification of Pain
Lu, C., Yang, T., Zhao, H., Zhang, M., Meng, F., Fu, H., Xie, Y., & Xu, H. (2016) · Neuroscience Bulletin · doi:10.1007/s12264-016-0016-y · Cited by 270 · see citing works
LTP Requires a Unique Postsynaptic SNARE Fusion Machinery
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
Self-citationSpinelli, M., Fusco, S., Mainardi, M., Scala, F., Natale, F., Lapenta, R., Mattera, A., Rinaudo, M., Puma, D. D. L., Ripoli, C., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-02221-9 · Cited by 208 · see citing works
Postsynaptic synaptotagmins mediate AMPA receptor exocytosis during LTP
Wu, D., Bacaj, T., Morishita, W., Goswami, D., Arendt, K. L., Xu, W., Chen, L., Malenka, R. C., & Südhof, T. C. (2017) · Nature · doi:10.1038/nature21720 · Cited by 195 · see citing works
Self-citationThe molecular machinery of neurotransmitter release (Nobel lecture).
Südhof, T. (2014) · Angewandte Chemie · doi:10.1002/anie.201406359 · Cited by 173 · see citing works
Self-citationNassi, J. J., Cepko, C. L., Born, R. T., & Beier, K. T. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00080 · Cited by 156 · 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
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
Aging, Synaptic Dysfunction, and Insulin-Like Growth Factor (IGF)-1
Deák, F., & Sonntag, W. E. (2012) · The Journals of Gerontology Series A · doi:10.1093/gerona/gls118 · Cited by 147 · see citing works
An Increase in Synaptic NMDA Receptors in the Insular Cortex Contributes to Neuropathic Pain
Qiu, S., Chen, T., Koga, K., Guo, Y., Xu, H., Song, Q., Wang, J., Descalzi, G., Kaang, B., Luo, J., et al. (2013) · Science Signaling · doi:10.1126/scisignal.2003778 · Cited by 147 · 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
Choquet, D. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.2119-18.2018 · Cited by 141 · see citing works
Input- and Output-Specific Regulation of Serial Order Performance by Corticostriatal Circuits
Rothwell, P. E., Hayton, S. J., Sun, G. L., Fuccillo, M. V., Lim, B. K., & Malenka, R. C. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.035 · Cited by 129 · see citing works
Self-citationNicoll, R. A., & Schulman, H. (2023) · Physiological Reviews · doi:10.1152/physrev.00034.2022 · Cited by 126 · see citing works
Plasticity 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
CaMKII Phosphorylation of TARPγ-8 Is a Mediator of LTP and Learning and Memory
Park, J., Chávez, A. E., Mineur, Y. S., Morimoto-Tomita, M., Lutzu, S., Kim, K. S., Picciotto, M. R., Castillo, P. E., & Tomita, S. (2016) · Neuron · doi:10.1016/j.neuron.2016.09.002 · Cited by 121 · 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
Purkey, A., & Dell’Acqua, M. L. (2020) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2020.00008 · Cited by 113 · see citing works
Lü, Y., Bu, F., Wang, F., Liu, L., Zhang, S., Wang, G., & Hu, X. (2023) · Translational Neurodegeneration · doi:10.1186/s40035-023-00341-5 · Cited by 117 · see citing works
NGF steers microglia toward a neuroprotective phenotype
Rizzi, C., Tiberi, A., Giustizieri, M., Marrone, M. C., Gobbo, F., Carucci, N. M., Meli, G., Arisi, I., D’Onofrio, M., Marinelli, S., et al. (2018) · Glia · doi:10.1002/glia.23312 · Cited by 103 · see citing works
Ghrelin triggers the synaptic incorporation of AMPA receptors in the hippocampus
Ribeiro, L. F., Catarino, T., Santos, S. D., Benoist, M., van Leeuwen, J. F., Esteban, J. A., & Carvalho, A. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1313798111 · Cited by 101 · 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
The Retromer Supports AMPA Receptor Trafficking During LTP
Temkin, P. A., Morishita, W., Goswami, D., Arendt, K. L., Chen, L., & Malenka, R. C. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.020 · Cited by 96 · see citing works
Self-citationSumi, T., & Harada, K. (2020) · Scientific Reports · doi:10.1038/s41598-020-71528-3 · Cited by 95 · see citing works
Therapeutic use of botulinum toxin in migraine: mechanisms of action
Ramachandran, R., & Yaksh, T. L. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12763 · Cited by 97 · see citing works
Cho, R. W., Buhl, L. K., Volfson, D., Tran, A., Li, F., Akbergenova, Y., & Littleton, J. T. (2015) · Neuron · doi:10.1016/j.neuron.2015.10.011 · Cited by 92 · see citing works
Yang, X., Cao, P., & Südhof, T. C. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1321367110 · Cited by 92 · see citing works
Self-citationRetinoic 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
Self-citationJiang, M., Polepalli, J. S., Chen, L. Y., Zhang, B., Südhof, T. C., & Malenka, R. C. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.80 · Cited by 88 · see citing works
Self-citationHomeostatic synaptic plasticity as a metaplasticity mechanism — a molecular and cellular perspective
Li, J., Park, E., Zhong, L. R., & Chen, L. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.08.010 · Cited by 81 · see citing works
Nagahama, K., Sakoori, K., Watanabe, T., Kishi, Y., Kawaji, K., Koebis, M., Nakao, K., Gotoh, Y., Aiba, A., Uesaka, N., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108126 · Cited by 94 · see citing works
Activity-dependent BDNF release via endocytic pathways is regulated by synaptotagmin-6 and complexin
Wong, Y., Lee, C.-M. J., 谢文俊, Cui, B., & Poo, M.-M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1511830112 · Cited by 82 · see citing works
AMPAR trafficking in synapse maturation and plasticity
Bassani, S., Folci, A., Zapata, J., & Passafaro, M. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1309-1 · Cited by 81 · see citing works
Anggono, V., Koç-Schmitz, Y., Widagdo, J., Kormann, J., Quan, A., Chen, C.-M., Robinson, P., Choi, S.-Y., Linden, D. J., Plomann, M., et al. (2013) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1312467110 · Cited by 81 · see citing works
Leucine-Rich Repeat Transmembrane Proteins Are Essential for Maintenance of Long-Term Potentiation
Soler-Llavina, G. J., Arstikaitis, P., Morishita, W., Ahmad, M., Südhof, T. C., & Malenka, R. C. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.007 · Cited by 77 · see citing works
Self-citationChang, S., Reim, K., Pedersen, M., Neher, E., Brose, N., & Taschenberger, H. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4841-14.2015 · Cited by 66 · see citing works
Purkey, A., Woolfrey, K. M., Crosby, K. C., Stich, D., Chick, W. S. H., Aoto, J. N., & Dell’Acqua, M. L. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.09.085 · Cited by 65 · see citing works
Synaptic activity regulates AMPA receptor trafficking through different recycling pathways
Zheng, N., Jeyifous, O., Munro, C., Montgomery, J. M., & Green, W. N. (2015) · eLife · doi:10.7554/elife.06878 · Cited by 59 · see citing works
Bhouri, M., Morishita, W., Temkin, P. A., Goswami, D., Kawabe, H., Brose, N., Südhof, T. C., Craig, A. M., Siddiqui, T. J., & Malenka, R. C. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1803280115 · Cited by 63 · see citing works
Self-citationComplexin Activates Exocytosis of Distinct Secretory Vesicles Controlled by Different Synaptotagmins
Cao, P., Yang, X., & Südhof, T. C. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4087-12.2013 · Cited by 61 · see citing works
Self-citationRecycling Endosomes Undergo Rapid Closure of a Fusion Pore on Exocytosis in Neuronal Dendrites
Jullié, D., Choquet, D., & Perrais, D. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0799-14.2014 · Cited by 50 · see citing works
Subcellular and regional localization of mRNA translation in midbrain dopamine neurons
Hobson, B. D., Kong, L., Angelo, M. F., Lieberman, O. J., Mosharov, E. V., Herzog, É., Sulzer, D. L., & Sims, P. A. (2022) · Cell Reports · doi:10.1016/j.celrep.2021.110208 · Cited by 49 · see citing works
The intersections of NMDAR-dependent synaptic plasticity and cell survival
Bartlett, T. E., & Wang, Y. T. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.01.012 · Cited by 49 · see citing works
miR-135a Regulates Synaptic Transmission and Anxiety-Like Behavior in Amygdala
Mannironi, C., Biundo, A., Rajendran, S., Vito, F. D., Saba, L., Caioli, S., Zona, C., Ciotti, T., Caristi, S., Perlas, E., et al. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0564-9 · Cited by 49 · see citing works
The rise and fall of insulin signaling in Alzheimer’s disease
Chami, B., Steel, A. J., de la Monte, S. M., & Sutherland, G. T. (2016) · Metabolic Brain Disease · doi:10.1007/s11011-016-9806-1 · Cited by 48 · see citing works
Bodrikov, V., Pauschert, A., Kochlamazashvili, G., & Stuermer, C. A. O. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.12.007 · Cited by 48 · see citing works
Mainardi, M., Spinelli, M., Scala, F., Mattera, A., Fusco, S., D’Ascenzo, M., & Grassi, C. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00225 · Cited by 46 · see citing works
Popova, D., Ċastrén, E., & Taira, T. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.09.003 · Cited by 45 · see citing works
Mechanisms and Role of Dendritic Membrane Trafficking for Long-Term Potentiation
Hiester, B. G., Becker, M. I., Bowen, A. B., Schwartz, S. L., & Kennedy, M. J. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00391 · Cited by 37 · see citing works
Yu, J. J., Luo, X., Xu, H., Ma, Q., Yuan, J., Li, X., Chang, R. C., Qu, Z., Huang, X., Zhuang, Z., et al. (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-141776 · Cited by 40 · see citing works
Self-citationWang, J., Lv, X., Wu, Y., Xu, T., Jiao, M., Yang, R., Li, X., Chen, M., Yan, Y.-G., Chen, C., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04672-0 · Cited by 38 · see citing works
Hiester, B. G., Bourke, A. M., Sinnen, B. L., Cook, S. G., Gibson, E. S., Smith, K. R., & Kennedy, M. J. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.105 · Cited by 37 · see citing works
Postsynaptic SNARE Proteins: Role in Synaptic Transmission and Plasticity
Madrigal, M. P., Portalés, A., SanJuan, M. P., & Jurado, S. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.11.012 · Cited by 37 · see citing works
The glutamatergic synapse: a complex machinery for information processing
Maio, V. D. (2021) · Cognitive Neurodynamics · doi:10.1007/s11571-021-09679-w · Cited by 34 · see citing works
PRRT1 regulates basal and plasticity-induced AMPA receptor trafficking
Troyano‐Rodriguez, E., Mann, S. N., Ullah, R., & Ahmad, M. (2019) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2019.06.008 · Cited by 33 · see citing works
Self-citationSathler, M. F., Khatri, L., Roberts, J. P., Schmidt, I. G., Zaytseva, A., Kubrusly, R. C. C., Ziff, E. B., & Kim, S. (2021) · Journal of Cell Science · doi:10.1242/jcs.257972 · Cited by 35 · see citing works
The role of AMPAR lateral diffusion in memory
Choquet, D., & Opazo, P. (2022) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2022.01.009 · Cited by 31 · see citing works
Bakr, M., Jullié, D., Krapivkina, J., Paget-Blanc, V., Bouit, L., Petersen, J. D., Retailleau, N., Breillat, C., Herzog, É., Choquet, D., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109678 · Cited by 29 · see citing works
The dendritic SNARE fusion machinery involved in AMPARs insertion during long-term potentiation
Jurado, S. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00407 · Cited by 25 · see citing works
Ribeiro, L. F., Catarino, T., de Carvalho, M. L., Cortes, L., Santos, S. D., Opazo, P., Ribeiro, L. R., Oliveiros, B., Choquet, D., Esteban, J. A., et al. (2021) · Science Signaling · doi:10.1126/scisignal.abb1953 · Cited by 25 · see citing works
AMPA Receptor Function in Hypothalamic Synapses
Royo, M., Aznar-Escolano, B., Madrigal, M. P., & Jurado, S. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.833449 · Cited by 29 · see citing works
Bin, N.-R., Ma, K., Harada, H., Tien, C.-W., Bergin, F., Sugita, K., Luyben, T. T., Narimatsu, M., Jia, Z., Wrana, J. L., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.05.026 · Cited by 25 · see citing works
He, Y., Kulasiri, D., & Samarasinghe, S. (2016) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2016.05.015 · Cited by 25 · see citing works
Zhang, D., Marlin, M. C., Liang, Z., Ahmad, M., Ashpole, N. M., Sonntag, W. E., Zhao, Z. J., & Li, G. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.728550 · Cited by 25 · see citing works
Self-citationSynaptic Function of Rab11Fip5: Selective Requirement for Hippocampal Long-Term Depression
Bacaj, T., Ahmad, M., Jurado, S., Malenka, R. C., & Südhof, T. C. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1581-14.2015 · Cited by 24 · see citing works
Self-citationAlterations of transcriptome signatures in head trauma-related neurodegenerative disorders
Cho, H., Hyeon, S. J., Shin, J.-Y., Alvarez, V. E., Stein, T. D., Lee, J.-H., Kowall, N. W., McKee, A. C., Ryu, H., & Seo, J. (2020) · Scientific Reports · doi:10.1038/s41598-020-65916-y · Cited by 23 · see citing works
KIF13A drives AMPA receptor synaptic delivery for long-term potentiation via endosomal remodeling
Gutiérrez, Y., López-García, S., Lario, A., Gutiérrez-Eisman, S., Delevoye, C., & Esteban, J. A. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.202003183 · Cited by 24 · see citing works
Wu, H.-F., Yen, H.-J., Huang, C., Lee, Y., Wu, S.-Z., Lee, T., & Lin, H. (2015) · Journal of Biomedical Science · doi:10.1186/s12929-015-0202-7 · Cited by 22 · see citing works
Dynamics of Hippocampal Protein Expression During Long-term Spatial Memory Formation
Borovok, N., Nesher, E., Levin, Y., Reichenstein, M., Pinhasov, A., & Michaelevski, I. (2015) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m115.051318 · Cited by 21 · see citing works
Synaptotagmins: Beyond Presynaptic Neurotransmitter Release
Wu, X., Hu, S., Kang, X., & Wang, C. (2019) · The Neuroscientist · doi:10.1177/1073858419844497 · Cited by 22 · see citing works
Ying, M., Sui, X., Zhang, Y., Sun, Q., Qu, Z., Luo, X., Chang, R. C., Ni, J., Liu, J., & Yang, X. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-9959-2 · Cited by 21 · see citing works
Self-citationAMPA/NMDA cooperativity and integration during a single synaptic event
Maio, V. D., Ventriglia, F., & Santillo, S. (2016) · Journal of Computational Neuroscience · doi:10.1007/s10827-016-0609-5 · Cited by 17 · see citing works
Hippocampal Subcellular Organelle Proteomic Alteration of Copper-Treated Mice
Yu, H., Jiang, X., Lin, X., Zhang, Z., Wu, D., Zhou, L., Liu, J., & Yang, X. (2018) · Toxicological Sciences · doi:10.1093/toxsci/kfy082 · Cited by 18 · see citing works
Self-citationNeuronal Vesicular Trafficking and Release in Age-Related Cognitive Impairment
Deák, F. (2014) · The Journals of Gerontology Series A · doi:10.1093/gerona/glu061 · Cited by 18 · see citing works
Activity-dependent diffusion trapping of AMPA receptors as a key step for expression of early LTP
Nowacka, A., Getz, A. M., Bessa‐Neto, D., & Choquet, D. (2024) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2023.0220 · Cited by 19 · see citing works
Walus, M., Kida, E., Rabe, A., Albertini, G., & Golabek, A. A. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.08.015 · Cited by 15 · see citing works
He, Y., Kulasiri, D., & Samarasinghe, S. (2014) · Biosystems · doi:10.1016/j.biosystems.2014.06.005 · Cited by 15 · see citing works
Omidi, G., Karimi, S. A., Shahidi, ., Faraji, N., & Komaki, A. (2019) · Brain Research · doi:10.1016/j.brainres.2019.146475 · Cited by 15 · see citing works
Regulation of AMPAR expression by microRNAs
Hanley, J. G. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108723 · Cited by 15 · see citing works
Interaction and Subcellular Association of PRRT1/SynDIG4 With AMPA Receptors
Martin, E. E., Wleklinski, E., Hoang, H., & Ahmad, M. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.705664 · Cited by 14 · see citing works
Self-citationSumi, T., & Harada, K. (2023) · iScience · doi:10.1016/j.isci.2023.106133 · Cited by 8 · see citing works
Nagaraja, R. Y., Stiles, M. A., Sherry, D. M., Agbaga, M., & Ahmad, M. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0378-23.2023 · Cited by 12 · see citing works
Self-citationWoo, D. H., Hur, Y.-N., Jang, M. W., Lee, C. J., & Park, M. (2020) · Animal Cells and Systems · doi:10.1080/19768354.2020.1838607 · Cited by 11 · see citing works
From cells to sensations: A window to the physics of mind
Vadakkan, K. I. (2019) · Physics of Life Reviews · doi:10.1016/j.plrev.2019.10.002 · Cited by 10 · see citing works
Proteasomal-Mediated Degradation of AKAP150 Accompanies AMPAR Endocytosis during cLTD
Cheng, W., Siedlecki‐Wullich, D., Català-Solsona, J., Fábregas, C., Fadó, R., Casals, N., Solé, M., Unzeta, M., Saura, C. A., Rodrı́guez-Álvarez, J., et al. (2020) · eNeuro · doi:10.1523/eneuro.0218-19.2020 · Cited by 10 · see citing works
Hirano, T. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00442 · Cited by 9 · see citing works
Bowers, M. S., Cacheaux, L. P., Sahu, S. U., Schmidt, M. E., Sennello, J. A., Leaderbrand, K., Khan, M. A., Kroes, R. A., & Moskal, J. R. (2019) · Journal of Neurochemistry · doi:10.1111/jnc.14845 · Cited by 9 · see citing works
Vadakkan, K. I. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.11.038 · Cited by 8 · see citing works
Multisynaptic cooperation shapes single glutamatergic synapse response
Maio, V. D., Santillo, S., & Ventriglia, F. (2018) · Brain Research · doi:10.1016/j.brainres.2018.06.016 · Cited by 7 · see citing works
Mihalaş, Ş., Ardiles, Á. O., He, K., Palacios, A. G., & Kirkwood, A. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.703621 · Cited by 6 · see citing works
Robust GRK2/3/6-dependent desensitization of oxytocin receptor in neurons
George, K., Hoang, H., Tibbs, T., Nagaraja, R. Y., Li, G., Troyano‐Rodriguez, E., & Ahmad, M. (2024) · iScience · doi:10.1016/j.isci.2024.110047 · Cited by 7 · see citing works
Self-citationYu, S., Fan, Y., You, B., Zhang, H., Cai, Z., Zhang, S., & Tian, H. (2026) · Biology · doi:10.3390/biology15020154 · Cited by 6 · see citing works
Lux, U. T., Ehrenberg, J., Joachimsthaler, A., Atorf, J., Pircher, B., Reim, K., Kremers, J., Gießl, A., & Brandstätter, J. H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158131 · Cited by 6 · see citing works
3D Modeling of Dendritic Spines with Synaptic Plasticity
Antunes, G., & de Souza, F. M. S. (2020) · Journal of Visualized Experiments · doi:10.3791/60896 · Cited by 6 · see citing works
Wang, Y., Chow, C. H., Zhang, Y., Huang, M., Higazy, R., Ramakrishnan, N., Chen, L., Chen, X., Deng, Y., Wang, S., et al. (2025) · PLoS Biology · doi:10.1371/journal.pbio.3003023 · Cited by 5 · see citing works
Trafficking of Glutamate Receptors and Associated Proteins in Synaptic Plasticity
Hořák, M., Seabold, G. K., & Petralia, R. S. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-418675-0.00008-0 · Cited by 4 · see citing works
Hippocampal place code plasticity in CA1 requires postsynaptic membrane fusion
Plitt, M. H., Kaganovsky, K., Say, E., Sosa, M., Südhof, T. C., & Giocomo, L. M. (2026) · Neuron · doi:10.1016/j.neuron.2026.03.006 · Cited by 4 · see citing works
Self-citationKulasiri, D., Liang, J., He, Y., & Samarasinghe, S. (2017) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2017.02.003 · Cited by 3 · see citing works
Liu, Y.-S., Wang, M., Hu, N.-Y., Li, Z., Wu, J., Li, H., Li, J., Li, X., Yang, J., Gao, T., et al. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1195327 · Cited by 3 · see citing works
- Authors
- Ahmad, M., Polepalli, J. S., Goswami, D., Yang, X., Kaeser-Woo, Y. J., Südhof, T. C., & Malenka, R. C.
- Affiliations
- Stanford Medicine (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Malenka, Robert C.
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2012-01
- Volume
- 73
- Issue
- 2
- Pages
- 260-267
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3269030
- OpenAlex
- W2085433160
- Cited by
- 133
- References
- 51
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 6 · 2023: 5 · 2022: 4 · 2021: 9 · 2020: 10 · 2019: 8 · 2018: 15 · 2017: 11 · 2016: 12 · 2015: 18 · 2014: 10 · 2013: 13 · 2012: 3
- FWCI
- 5.80
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (MH06334, R01MH063394, P50MH086403, P50 MH0864)
- 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
- complexin, long-term potentiation, SNARE complex, NMDA receptor activation, synaptotagmin-1, hippocampal neurons, neurotransmitter release regulation
- MeSH terms
- Animals, Exocytosis, Nerve Tissue Proteins, Synaptic Transmission, Neurons, Long-Term Potentiation, Receptors, AMPA, Excitatory Postsynaptic Potentials, Protein Transport, Adaptor Proteins, Vesicular Transport, SNARE Proteins, Synaptotagmin I, Mice, CA1 Region, Hippocampal, Post-Synaptic Density
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