Potentiated transmission and prevention of further LTP by increased CaMKII activity in postsynaptic hippocampal slice neurons
Abstract
Calcium-calmodulin-dependent protein kinase II (CaMKII) is a necessary component of the cellular machinery underlying learning and memory. Here, a constitutively active form of this enzyme, CaMKII(1-290), was introduced into neurons of hippocampal slices with a recombinant vaccinia virus to test the hypothesis that increased postsynaptic activity of this enzyme is sufficient to produce long-term synaptic potentiation (LTP), a prominent cellular model of learning and memory. Postsynaptic expression of CaMKII(1-290) increased CaMKII activity, enhanced synaptic transmission, and prevented more potentiation by an LTP-inducing protocol. These results, together with previous studies, suggest that postsynaptic CaMKII activity is necessary and sufficient to generate LTP.
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?
Calcium ions play a crucial role in initiating downstream signaling during long-term potentiation (LTP) and depression (LTD) and influx of calcium is both necessary and sufficient for structural synaptic plasticity.
“Calcium ions play a crucial role in initiating downstream signaling during long-term potentiation (LTP) and depression (LTD) and influx of calcium is both necessary and sufficient for structural synaptic plasticity (Pettit et al., 1994; Lledo et al., 1995; Otmakhov et al., 2004).”
From Barriers in the brain: resolving dendritic spine morphology and compartmentalization (2014) · cites this paper as Pettit et al., 1994
CaMKII occludes LTP.
“This is indeed the case (199, 209).”
From Synaptic memory and CaMKII (2023) · cites this paper as [209]
Expression of active CaMKII or direct delivery into the cell via the recording electrode has repeatedly revealed a roughly two- to threefold enhancement in the AMPAR EPSC but little change in the NMDAR EPSC.
“Expression of active CaMKII (121, 130–132, 209, 210, 212) or direct delivery into the cell via the recording electrode (199) has repeatedly revealed a roughly two- to threefold enhancement in the AMPAR EPSC but little change in the NMDAR EPSC (130–132).”
From Synaptic memory and CaMKII (2023) · cites this paper as [209]
Cites
Morris, R. G. M., Anderson, E., Lynch, G. S., & Baudry, M. (1986) · Nature · doi:10.1038/319774a0 · Cited by 3,640 · see citing works
Collingridge, G. L., Kehl, S. J., & McLennan, H. (1983) · The Journal of Physiology · doi:10.1113/jphysiol.1983.sp014478 · Cited by 2,413 · see citing works
MacDermott, A. B., Mayer, M. L., Westbrook, G. L., Smith, S. J., & Barker, J. L. (1986) · Nature · doi:10.1038/321519a0 · Cited by 1,835 · see citing works
Deficient Hippocampal Long-Term Potentiation in α-Calcium-Calmodulin Kinase II Mutant Mice
Silva, A. J., Stevens, C. F., Tonegawa, S., & Wang, Y. (1992) · Science · doi:10.1126/science.1378648 · Cited by 1,472 · see citing works
Inhibition of Postsynaptic PKC or CaMKII Blocks Induction But Not Expression of LTP
Malinow, R., Schulman, H., & Tsien, R. W. (1989) · Science · doi:10.1126/science.2549638 · Cited by 1,325 · see citing works
Self-citationAn essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation
Malenka, R. C., Kauer, J. A., Perkel, D. J., Mauk, M. D., Kelly, P. T., Nicoll, R. A., & Waxham, M. N. (1989) · Nature · doi:10.1038/340554a0 · Cited by 1,025 · see citing works
Long-term potentiation in the hippocampus involves activation of N-methyl-D-aspartate receptors
Harris, E. W., Ganong, A. H., & Cotman, C. W. (1984) · Brain Research · doi:10.1016/0006-8993(84)90275-0 · Cited by 903 · see citing works
Miller, S. (1986) · Cell · doi:10.1016/0092-8674(86)90008-5 · Cited by 864 · see citing works
Malinow, R., & Tsien, R. W. (1990) · Nature · doi:10.1038/346177a0 · Cited by 797 · see citing works
Self-citationSynaptic enhancement in fascia dentata: Cooperativity among coactive afferents
McNaughton, B. L., Douglas, R. M., & Goddard, G. V. (1978) · Brain Research · doi:10.1016/0006-8993(78)90030-6 · Cited by 647 · see citing works
Neuronal Ca2+/calmodulin-dependent protein kinases.
Hanson, P., & Schulman, H. (1992) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.61.070192.003015 · Cited by 628 · see citing works
Kennedy, M. B., Bennett, M. K., & Erondu, N. E. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.23.7357 · Cited by 610 · see citing works
Persistent protein kinase activity underlying long-term potentiation
Malinow, R., Madison, D. V., & Tsien, R. W. (1988) · Nature · doi:10.1038/335820a0 · Cited by 552 · see citing works
Self-citationLong-term potentiation in the hippocampus is blocked by tyrosine kinase inhibitors
O’Dell, T. J., Kandel, E. R., & Grant, S. G. N. (1991) · Nature · doi:10.1038/353558a0 · Cited by 521 · see citing works
Dendritic spines as individual neuronal compartments for synaptic Ca2+ responses
Müller, W. S., & Connor, J. A. (1991) · Nature · doi:10.1038/354073a0 · Cited by 479 · see citing works
Lorca, T., Cruzalegui, F. H., Fesquet, D., Cavadore, J., Méry, J., Means, A. R., & Dorée, M. (1993) · Nature · doi:10.1038/366270a0 · Cited by 446 · see citing works
McGlade-McCulloh, E., Yamamoto, H., Tan, S.-E., Brickey, D. A., & Soderling, T. (1993) · Nature · doi:10.1038/362640a0 · Cited by 441 · see citing works
Fukunaga, K., Stoppini, L., Miyamoto, E., & Muller, D. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53037-4 · Cited by 398 · see citing works
Kelly, P., McGuinness, T. L., & Greengard, P. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.3.945 · Cited by 386 · see citing works
Weisskopf, M. G., Zalutsky, R. A., & Nicoll, R. A. (1993) · Nature · doi:10.1038/362423a0 · Cited by 337 · see citing works
Hu, G., Hvalby, Ø., Walaas, S. I., Albert, K. A., Skjeflo, P., Andersen, P. N., & Greengard, P. (1987) · Nature · doi:10.1038/328426a0 · Cited by 333 · see citing works
McNaughton, B. L. (1982) · The Journal of Physiology · doi:10.1113/jphysiol.1982.sp014110 · Cited by 332 · see citing works
Bliss, T. V. P., Goddard, G. V., & Riives, M. L. (1983) · The Journal of Physiology · doi:10.1113/jphysiol.1983.sp014507 · Cited by 293 · see citing works
Nichols, R. A., Sihra, T. S., Czernik, A. J., Nairn, A. C., & Greengard, P. (1990) · Nature · doi:10.1038/343647a0 · Cited by 283 · see citing works
Lisman, J. E., & Goldring, M. A. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.14.5320 · Cited by 257 · see citing works
Raastad, M., Storm, J. F., & Andersen, P. N. (1992) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1992.tb00114.x · Cited by 250 · see citing works
Postsynaptic NMDA receptor-mediated calcium accumulation in hippocampal CAl pyramidal cell dendrites
Regehr, W. G., & Tank, D. W. (1990) · Nature · doi:10.1038/345807a0 · Cited by 234 · see citing works
Phorbol esters block a voltage-sensitive chloride current in hippocampal pyramidal cells
Madison, D. V., Malenka, R. C., & Nicoll, R. A. (1986) · Nature · doi:10.1038/321695a0 · Cited by 226 · see citing works
Alford, S. T., Frenguelli, B. G., Schofield, J., & Collingridge, G. L. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019838 · Cited by 221 · see citing works
Goldenring, J. R., McGuire, J. S., & DeLorenzo, R. J. (1984) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1984.tb12713.x · Cited by 219 · see citing works
Molecular cloning of a brain-specific calcium/calmodulin-dependent protein kinase.
Lin, C.-J. R., Kapiloff, M., Durgerian, S., Tatemoto, K., Russo, A., Hanson, P., Schulman, H., & Rosenfeld, M. G. (1987) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.84.16.5962 · Cited by 214 · see citing works
Wagner, J. A., Cozens, A., Schulman, H., Gruenert, D. C., Stryer, L., & Gardner, P. I. (1991) · Nature · doi:10.1038/349793a0 · Cited by 189 · see citing works
Protein kinase C phosphorylates a 47 Mr protein (F1) directly related to synaptic plasticity
Akers, R. F., & Routtenberg, A. (1985) · Brain Research · doi:10.1016/0006-8993(85)90576-1 · Cited by 183 · see citing works
Synaptic efficacy and EPSP summation in granule cells of rat fascia dentata studied in vitro.
McNaughton, B. L., Barnes, C. A., & Andersen, P. N. (1981) · Journal of Neurophysiology · doi:10.1152/jn.1981.46.5.952 · Cited by 181 · see citing works
Reymann, K. G., Frey, U., Jork, R., & Matthies, H. (1988) · Brain Research · doi:10.1016/0006-8993(88)91000-1 · Cited by 178 · see citing works
Baitinger, C., Alderton, J. M., Poenie, M., Schulman, H., & Steinhardt, R. A. (1990) · The Journal of Cell Biology · doi:10.1083/jcb.111.5.1763 · Cited by 169 · see citing works
Steward, O., & Reeves, T. M. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-01-00176.1988 · Cited by 144 · see citing works
Perkel, D. J., Petrozzino, J. J., Nicoll, R. A., & Connor, J. A. (1993) · Neuron · doi:10.1016/0896-6273(93)90111-4 · Cited by 138 · see citing works
Calcium/calmodulin-dependent protein kinase mediates a pathway for transcriptional regulation.
Kapiloff, M. S., Mathis, J. M., Nelson, C. A., Lin, C. R., & Rosenfeld, M. G. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.9.3710 · Cited by 119 · see citing works
Steward, O., & Falk, P. M. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903140311 · Cited by 114 · see citing works
Dingledine, R. J. (1984) · Springer eBooks · doi:10.1007/978-1-4684-4583-1 · Cited by 106 · see citing works
Malinow, R., Otmakhov, N., Blum, K. I., & Lisman, J. E. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.17.8170 · Cited by 88 · see citing works
Self-citationRapid activation of hippocampal casein kinase II during long-term potentiation.
Charriaut‐Marlangue, C., Otani, S., Creuzet, C., Ben‐Ari, Y., & Loeb, J. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.22.10232 · Cited by 86 · see citing works
Steward, O. (1983) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1983.048.01.077 · Cited by 80 · see citing works
Müller, W. S., Petrozzino, J. J., Griffith, L. C., Danho, W., & Connor, J. A. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.6.2264 · Cited by 76 · see citing works
Gustafsson, B., Huang, Y.-Y., & Wigström, H. (1988) · Neuroscience Letters · doi:10.1016/0304-3940(88)90432-6 · Cited by 75 · see citing works
Phorbol ester-induced synaptic facilitation is different than long-term potentiation.
Müller, D., Turnbull, J., Baudry, M., & LYNCH, G. S. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.18.6997 · Cited by 71 · see citing works
Steward, O., & Ribak, C. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-10-03079.1986 · Cited by 63 · see citing works
Cohen, M. E., Reinlib, L., Watson, A. J. M., Gorelick, F. S., Rys‐Sikora, K. E., Tse, M. C., Rood, R. P., Czernik, A. J., Sharp, G. W. G., & Donowitz, M. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.22.8990 · Cited by 57 · see citing works
Reymann, K. G., Matthies, H. K., Frey, U., Vorobjev, V. S., & Matthies, H. J. G. (1986) · Brain Research Bulletin · doi:10.1016/0361-9230(86)90234-0 · Cited by 49 · see citing works
Yamagata, Y., Czernik, A. J., & Greengard, P. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)98628-x · Cited by 43 · see citing works
Asztely, F., Hanse, E., Wigström, H., & Gustafsson, B. (1992) · Synapse · doi:10.1002/syn.890110409 · Cited by 18 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Synaptic Plasticity: Multiple Forms, Functions, and Mechanisms
Citri, A., & Malenka, R. C. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301559 · Cited by 2,323 · see citing works
Long-Term Potentiation and Memory
Lynch, M. A. (2004) · Physiological Reviews · doi:10.1152/physrev.00014.2003 · Cited by 2,001 · see citing works
The molecular basis of CaMKII function in synaptic and behavioural memory
Lisman, J., Schulman, H., & Cline, H. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn753 · Cited by 1,860 · see citing works
Emergent Properties of Networks of Biological Signaling Pathways
Bhalla, U. S., & Iyengar, R. (1999) · Science · doi:10.1126/science.283.5400.381 · Cited by 1,686 · 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-citationRegulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation
Barria, A., Muller, D., Derkach, V., Griffith, L. C., & Soderling, T. R. (1997) · Science · doi:10.1126/science.276.5321.2042 · Cited by 1,049 · see citing works
Balancing Structure and Function at Hippocampal Dendritic Spines
Bourne, J. N., & Harris, K. M. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125646 · Cited by 916 · see citing works
Derkach, V., Barria, A., & Soderling, T. R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.6.3269 · Cited by 842 · 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
NMDA Receptor Subunit Composition Controls Synaptic Plasticity by Regulating Binding to CaMKII
Barria, A., & Malinow, R. (2005) · Neuron · doi:10.1016/j.neuron.2005.08.034 · Cited by 709 · see citing works
Self-citationDeisseroth, K., Bito, H., & Tsien, R. W. (1996) · Neuron · doi:10.1016/s0896-6273(00)80026-4 · Cited by 698 · see citing works
Shen, K., & Meyer, T. (1999) · Science · doi:10.1126/science.284.5411.162 · Cited by 673 · see citing works
Lee, H.-K., Kameyama, K., Huganir, R. L., & Bear, M. F. (1998) · Neuron · doi:10.1016/s0896-6273(00)80632-7 · Cited by 668 · see citing works
Hudmon, A., & Schulman, H. (2002) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.71.110601.135410 · Cited by 654 · see citing works
Structure–function of the multifunctional Ca2+/calmodulin-dependent protein kinase II
HUDMON, A., & SCHULMAN, H. (2002) · Biochemical Journal · doi:10.1042/bj20020228 · Cited by 615 · see citing works
Ehrlich, I., & Malinow, R. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4733-03.2004 · Cited by 567 · see citing works
Self-citationMaturation of a Central Glutamatergic Synapse
Wu, G.-Y., Malinow, R., & Cline, H. T. (1996) · Science · doi:10.1126/science.274.5289.972 · Cited by 546 · see citing works
Self-citationMayford, M. R., Wang, J., Kandel, E. R., & O’Dell, T. J. (1995) · Cell · doi:10.1016/0092-8674(95)90009-8 · Cited by 525 · see citing works
Wu, L., Wells, D., Tay, J., Mendis, D., Abbott, M.-A., Barnitt, A., Quinlan, E., Heynen, A., Fallon, J. R., & Richter, J. D. (1998) · Neuron · doi:10.1016/s0896-6273(00)80630-3 · Cited by 488 · see citing works
Lledo, P. M., Hjelmstad, G. O., Mukherji, S., Soderling, T. R., Malenka, R. C., & Nicoll, R. A. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.24.11175 · Cited by 456 · see citing works
The neuronal calcium sensor family of Ca2+-binding proteins
Burgoyne, R. D., & Weiss, J. L. (2000) · Biochemical Journal · doi:10.1042/bj3530001 · Cited by 444 · see citing works
Strack, S., & Colbran, R. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.33.20689 · Cited by 466 · see citing works
Mammen, A. L., Kameyama, K., Roche, K. W., & Huganir, R. L. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.51.32528 · Cited by 441 · see citing works
Calcium/calmodulin signaling controls osteoblast growth and differentiation
Zayzafoon, M. (2005) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20675 · Cited by 437 · see citing works
CaMKII: a central molecular organizer of synaptic plasticity, learning and memory
Yasuda, R., Hayashi, Y., & Hell, J. W. (2022) · Nature Reviews Neuroscience · doi:10.1038/s41583-022-00624-2 · Cited by 431 · 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
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
Barría, A., Derkach, V. A., & Soderling, T. R. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.52.32727 · Cited by 392 · see citing works
Jörntell, H., & Hansel, C. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.032 · Cited by 382 · see citing works
Boehm, J., Kang, M.-G., Johnson, R. C., Esteban, J., Huganir, R. L., & Malinow, R. (2006) · Neuron · doi:10.1016/j.neuron.2006.06.013 · Cited by 382 · see citing works
Self-citationStabilization of Dendritic Arbor Structure in Vivo by CaMKII
Wu, G., & Cline, H. T. (1998) · Science · doi:10.1126/science.279.5348.222 · Cited by 373 · see citing works
Strack, S., McNeill, R. B., & Colbran, R. J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m001471200 · Cited by 356 · see citing works
Metaplasticity: A new vista across the field of synaptic plasticity
Abraham, W. C., & Tate, W. P. (1997) · Progress in Neurobiology · doi:10.1016/s0301-0082(97)00018-x · Cited by 354 · see citing works
Calcium signaling in neurodegeneration
Marambaud, P., Dreses‐Werringloer, U., & Vingtdeux, V. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-20 · Cited by 352 · see citing works
Molecular mechanisms of dendritic spine development and remodeling
Ethell, I. M., & Pasquale, E. B. (2005) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2005.02.003 · Cited by 349 · see citing works
All-or-none potentiation at CA3-CA1 synapses
Petersen, C. C. H., Malenka, R. C., Nicoll, R. A., & Hopfield, J. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.8.4732 · Cited by 330 · see citing works
Postsynaptic CAMP pathway gates early LTP in hippocampal CA1 region
Blitzer, R. D., Wong, T., Nouranifar, R., Iyengar, R., & Landau, E. M. (1995) · Neuron · doi:10.1016/0896-6273(95)90018-7 · Cited by 325 · see citing works
Omkumar, R. V., Kiely, M. J., Rosenstein, A. J., Min, K.-T., & Kennedy, M. B. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.49.31670 · Cited by 304 · see citing works
Regulation of ligand-gated ion channels by protein phosphorylation.
Swope, S., Moss, S., Raymond, L., & Huganir, R. (1999) · Advances in second messenger and phosphoprotein research · doi:10.1016/s1040-7952(99)80005-6 · Cited by 307 · see citing works
Strack, S., Choi, S., Lovinger, D. M., & Colbran, R. J. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.21.13467 · Cited by 296 · see citing works
Kameyama, K., Lee, H.-K., Bear, M. F., & Huganir, R. L. (1998) · Neuron · doi:10.1016/s0896-6273(00)80633-9 · Cited by 283 · see citing works
Matsuda, S., Mikawa, S., & Hirai, H. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.731765.x · Cited by 265 · see citing works
Pu, L., Bao, G., Xu, N., Ma, L., & Pei, G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-05-01914.2002 · Cited by 242 · see citing works
Mechanism for a sliding synaptic modification threshold
Bear, M. F. (1995) · Neuron · doi:10.1016/0896-6273(95)90056-x · Cited by 239 · see citing works
αCaMKII Is Essential for Cerebellar LTD and Motor Learning
Hansel, C., de Jeu, M. T. G., Belmeguenaï, A., Houtman, S. H., Buitendijk, G. H. S., Andreev, D., Zeeuw, C. I. D., & Elgersma, Y. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.013 · Cited by 225 · see citing works
Characterization of a calmodulin kinase II inhibitor protein in brain
Chang, B. H., Mukherji, S., & Soderling, T. R. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.18.10890 · Cited by 227 · see citing works
Ouyang, Y., Kantor, D. B., Harris, K. M., Schuman, E. M., & Kennedy, M. B. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-14-05416.1997 · Cited by 227 · see citing works
Ionotropic glutamate receptors
Asztely, F., & Gustafsson, B. (1996) · Molecular Neurobiology · doi:10.1007/bf02740744 · Cited by 90 · see citing works
Synaptic plasticity and phosphorylation
Lee, H. (2006) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2006.06.003 · Cited by 215 · see citing works
Promotion of Dendritic Growth by CPG15, an Activity-Induced Signaling Molecule
Nedivi, E., Wu, G., & Cline, H. T. (1998) · Science · doi:10.1126/science.281.5384.1863 · Cited by 210 · see citing works
Blank, T., Nijholt, I. M., Eckart, K., & Spiess, J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03788.2002 · Cited by 210 · see citing works
Molecular memory by reversible translocation of calcium/calmodulin-dependent protein kinase II
Shen, K., Teruel, M. N., Connor, J. H., Shenolikar, S., & Meyer, T. (2000) · Nature Neuroscience · doi:10.1038/78783 · Cited by 206 · see citing works
Shi, Y., & Ethell, I. M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4091-05.2006 · Cited by 200 · see citing works
Postsynaptic Levels of [Ca2+]i Needed to Trigger LTD and LTP
Neveu, D., & Zucker, R. S. (1996) · Neuron · doi:10.1016/s0896-6273(00)80081-1 · Cited by 198 · see citing works
Okamoto, K., Bosch, M., & Hayashi, Y. (2009) · Physiology · doi:10.1152/physiol.00029.2009 · Cited by 197 · 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
Akerman, C. J., & Cline, H. T. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0319-06.2006 · Cited by 189 · see citing works
Toward a Molecular Explanation for Long-Term PotentiationPreprint
Sweatt, J. D. (1999) · Learning & Memory · doi:10.1101/lm.6.5.399 · Cited by 188 · see citing works
Ehrengruber, M. U., Lundstrom, K. H., Schweitzer, C., Heuss, C., Schlesinger, S., & Gähwiler, B. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.12.7041 · Cited by 183 · see citing works
Techniques for gene transfer into neurons
Washbourne, P., & McAllister, A. K. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00365-3 · Cited by 182 · see citing works
Kennedy, M. B. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00043-x · Cited by 181 · see citing works
Interactions between the NR2B Receptor and CaMKII Modulate Synaptic Plasticity and Spatial Learning
Zhou, Y., Takahashi, E., Li, W., Halt, A., Wiltgen, B., Ehninger, D., Li, G.-D., Hell, J. W., Kennedy, M. B., & Silva, A. J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4486-07.2007 · Cited by 179 · see citing works
Poncer, J. C., Esteban, J. A., & Malinow, R. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-11-04406.2002 · Cited by 177 · see citing works
Self-citationSynaptic plasticity: hippocampal LTP
Larkman, A. U., & Jack, J. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80045-x · Cited by 174 · see citing works
Postsynaptic injection of Ca2+/CaM induces synaptic potentiation requiring CaMKII and PKC activity
Wang, J.-H., & Kelly, P. T. (1995) · Neuron · doi:10.1016/0896-6273(95)90048-9 · Cited by 172 · see citing works
Incontro, S., Díaz-Alonso, J., Iafrati, J., Vieira, M., Asensio, C. S., Sohal, V. S., Roche, K. W., Bender, K. J., & Nicoll, R. A. (2018) · Nature Communications · doi:10.1038/s41467-018-04439-7 · Cited by 171 · see citing works
Varga, A. W., Yuan, L., Anderson, A. E., Schrader, L. A., Wu, G., Gatchel, J. R., Johnston, D., & Sweatt, J. D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0154-04.2004 · Cited by 166 · see citing works
Molecular basis for induction of ocular dominance plasticity
Bear, M. F., & Rittenhouse, C. D. (1999) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199910)41:1 · Cited by 99 · see citing works
Synaptic dysfunction in Parkinson's disease
Bagetta, V., Ghiglieri, V., Sgobio, C., Calabresi, P., & Picconi, B. (2010) · Biochemical Society Transactions · doi:10.1042/bst0380493 · Cited by 159 · see citing works
Picconi, B. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1224-04.2004 · Cited by 156 · see citing works
Pereda, A. E., Bell, T. D., Chang, B. H., Czernik, A. J., Nairn, A. C., Soderling, T. R., & Faber, D. S. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.22.13272 · Cited by 153 · see citing works
Regulation of NMDA glutamate receptor functions by the GluN2 subunits
Vieira, M., Yong, X. L. H., Roche, K. W., & Anggono, V. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.14970 · Cited by 151 · see citing works
Learning mechanisms: the case for CaM-KII
Lisman, J., Malenka, R. C., Nicoll, R. A., & Malinow, R. (1997) · Science · doi:10.1126/science.276.5321.2001 · Cited by 147 · see citing works
Self-citationLong-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
Cammarota, M., Bernabeu, R., de Stein, M. L., Izquierdo, I., & Medina, J. H. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00254.x · Cited by 141 · see citing works
Regulation of AMPA receptors and synaptic plasticity
Santos, S. D., Carvalho, A. L., Caldeira, M. V., & Duarte, C. B. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.037 · Cited by 139 · see citing works
Protein kinases: which one is the memory molecule?
Micheau, J. (1999) · Cellular and Molecular Life Sciences · doi:10.1007/s000180050312 · Cited by 135 · see citing works
Okabe, T., Nakamura, T., Nishimura, Y. N., Kohu, K., Ohwada, S., Morishita, Y., & Akiyama, T. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m208872200 · Cited by 129 · see citing works
Frizzled-5, a receptor for the synaptic organizer Wnt7a, regulates activity-mediated synaptogenesis
Sahores, M., Gibb, A. J., & Salinas, P. C. (2010) · Development · doi:10.1242/dev.046722 · Cited by 128 · see citing works
Nicoll, R. A., & Schulman, H. (2023) · Physiological Reviews · doi:10.1152/physrev.00034.2022 · Cited by 126 · see citing works
“This is indeed the case (199, 209).”
BackgroundIs Persistent Activity of Calcium/Calmodulin-Dependent Kinase Required for the Maintenance of LTP?
Chen, H.-X., Otmakhov, N., Strack, S., Colbran, R. J., & Lisman, J. E. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.4.1368 · Cited by 126 · see citing works
Zagaar, M. A., Alhaider, I. A., Dao, A. T., Levine, A. T., Alkarawi, A., Alzubaidy, M., & Alkadhi, K. A. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.12.039 · Cited by 127 · see citing works
Gating by Cyclic AMP: Expanded Role for an Old Signaling Pathway
Iyengar, R. (1996) · Science · doi:10.1126/science.271.5248.461 · Cited by 126 · see citing works
Pi, H. J., Otmakhov, N., Lemelin, D., De Koninck, P., & Lisman, J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0133-10.2010 · Cited by 125 · 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
A working model of CaM kinase II activity in hippocampal long-term potentiation and memory
Fukunaga, K., & Miyamoto, E. (2000) · Neuroscience Research · doi:10.1016/s0168-0102(00)00139-5 · Cited by 120 · see citing works
Neurobiological Consequences of Sleep Deprivation
Alkadhi, K. A., Zagaar, M. A., Alhaider, I. A., Salim, S., & Aleisa, A. M. (2013) · Current Neuropharmacology · doi:10.2174/1570159x11311030001 · Cited by 121 · see citing works
Nerve Ending “Signal” Proteins GAP‐43, MARCKS, and BASP1
Mosevitsky, M. I. (2005) · International review of cytology · doi:10.1016/s0074-7696(05)45007-x · Cited by 120 · see citing works
Autophosphorylation of αCaMKII Is Required for Ocular Dominance Plasticity
Taha, S. A., Hanover, J. L., Silva, A. J., & Stryker, M. P. (2002) · Neuron · doi:10.1016/s0896-6273(02)00966-2 · Cited by 119 · see citing works
A biochemist's view of long-term potentiation.Preprint
Roberson, E. D., English, J. D., & Sweatt, J. D. (1996) · Learning & Memory · doi:10.1101/lm.3.1.1 · Cited by 118 · see citing works
Dynamics of electrical transmission at club endings on the Mauthner cells
Pereda, A. E., Rash, J. E., Nagy, J. I., & Bennett, M. V. L. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.06.010 · Cited by 117 · see citing works
CaM kinase II in long-term potentiation.
Fukunaga, K., Muller, D., & Miyamoto, E. (1996) · Neurochemistry International · doi:10.1016/0197-0186(95)00097-6 · Cited by 113 · see citing works
Manahan‐Vaughan, D. (2002) · Cerebral Cortex · doi:10.1093/cercor/13.2.123 · Cited by 111 · see citing works
Makhinson, M., Chotiner, J. K., Watson, J. B., & O’Dell, T. J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-07-02500.1999 · Cited by 110 · see citing works
Ko, G. Y. ‐., & Kelly, P. T. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-16-06784.1999 · Cited by 108 · see citing works
Protein phosphorylation in neuronal plasticity and gene expression
Schulman, H. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80051-4 · Cited by 106 · see citing works
Martin, K., Corlett, A., Dubach, D., Mustafa, T., Coleman, H. A., Parkington, H. C., Merson, T. D., Bourne, J. A., Porta, S., Arbonés, M. L., et al. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds134 · Cited by 105 · see citing works
- Authors
- Pettit, D. L., Perlman, S., & Malinow, R.
- Affiliations
- University of Iowa (US)
- Venue
- Science
- Published
- 1994-12-16
- Volume
- 266
- Issue
- 5192
- Pages
- 1881-1885
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2076782463
- Cited by
- 329
- References
- 52
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 7 · 2023: 8 · 2022: 9 · 2021: 6 · 2020: 2 · 2019: 3 · 2018: 3 · 2017: 5 · 2016: 7 · 2015: 8 · 2014: 6 · 2013: 11 · 2012: 16
- FWCI
- 6.55
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Keywords
- CaMKII, long-term potentiation, synaptic transmission, hippocampal neurons, postsynaptic activity, learning and memory, synaptic plasticity, recombinant vaccinia virus
- MeSH terms
- Animals, Cell Line, Genetic Vectors, Hippocampus, Membrane Potentials, Synaptic Transmission, Recombinant Proteins, Transfection, Vaccinia virus, 2-Amino-5-phosphonovalerate, Long-Term Potentiation, Calcium-Calmodulin-Dependent Protein Kinases, Pyramidal Cells, Patch-Clamp Techniques, Rats, Calcium-Calmodulin-Dependent Protein Kinase Type 2, 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