CA1 Long-Term Potentiation Is Diminished but Present in Hippocampal Slices from α-CaMKII Mutant Mice
Open accessAbstract
Previous work has shown that mice missing the alpha-isoform of calcium-calmodulin-dependent protein kinase II (alpha-CaMKII) have a deficiency in CA1 hippocampal long-term potentiation (LTP). Follow-up studies on subsequent generations of these mutant mice in a novel inbred background by our laboratories have shown that whereas a deficiency in CA1 LTP is still present in alpha-CaMKII mutant mice, it is different both quantitatively and qualitatively from the deficiency first described. Mice of a mixed 129SvOla/SvJ;BALB/c;C57B1/6 background derived from brother/sister mating of the alpha-CaMKII mutant line through multiple generations (>10) were produced by use of in vitro fertilization. Although LTP at 60 min post-tetanus was clearly deficient in these (-/-) alpha-CaMKII mice (42.6%, n = 33) compared with (+/+) alpha-CaMKII control animals (81.7%, n = 17), alpha-CaMKII mutant mice did show a significant level of LTP. The amount of LTP observed in alpha-CaMKII mutants was normally distributed, blocked by APV (2.7%, n = 8), and did not correlate with age. Although this supports a role for alpha-CaMKII in CA1 LTP, it also suggests that a form of alpha-CaMKII-independent LTP is present in mice that could be dependent on another kinase, such as the beta-isoform of CaMKII. A significant difference in input/output curves was also observed between (-/-) alpha-CaMKII and (+/+) alpha-CaMKII animals, suggesting that differences in synaptic transmission may be contributing to the LTP deficit in mutant mice. However, tetani of increasing frequency (50, 100, and 200 Hz) did not reveal a higher threshold for potentiation in (-/-) alpha-CaMKII mice compared with (+/+) alpha-CaMKII controls.
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?
The results with genetic deletion of CaMKIIα are variable, some showing roughly a 50% block and some showing a complete block.
“the results with the genetic deletion of CaMKIIα are more variable, some showing roughly a 50% block (87, 204–206) but some showing a complete block (121, 207, 208).”
From Synaptic memory and CaMKII (2023) · cites this paper as [206]
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
A synaptic model of memory: long-term potentiation in the hippocampus
Bliss, T. V. P., & Collingridge, G. L. (1993) · Nature · doi:10.1038/361031a0 · Cited by 11,566 · 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
Self-citationLiao, D., Hessler, N. A., & Malinow, R. (1995) · Nature · doi:10.1038/375400a0 · Cited by 1,365 · see citing works
Self-citationImpaired Spatial Learning in α-Calcium-Calmodulin Kinase II Mutant Mice
Silva, A. J., Paylor, R. E., Wehner, J. M., & Tonegawa, S. (1992) · Science · doi:10.1126/science.1321493 · Cited by 1,351 · see citing works
Self-citationInhibition 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-citationEvidence for silent synapses: Implications for the expression of LTP
Isaac, J. T. R., Nicoll, R. A., & Malenka, R. C. (1995) · Neuron · doi:10.1016/0896-6273(95)90046-2 · Cited by 1,233 · see citing works
Autophosphorylation at Thr <sup>286</sup> of the α Calcium-Calmodulin Kinase II in LTP and Learning
Giese, K. P., Fedorov, N. B., Filipkowski, R. K., & Silva, A. J. (1998) · Science · doi:10.1126/science.279.5352.870 · Cited by 1,055 · see citing works
Regulatory 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
An 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
Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype?
Gerlai, R. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)20020-7 · Cited by 881 · see citing works
Miller, S. (1986) · Cell · doi:10.1016/0092-8674(86)90008-5 · Cited by 864 · see citing works
The Multifunctional Calcium/Calmodulin-Dependent Protein Kinase: From Form to Function
Braun, A. P., & Schulman, H. (1995) · Annual Review of Physiology · doi:10.1146/annurev.ph.57.030195.002221 · Cited by 820 · see citing works
Malinow, R., & Tsien, R. W. (1990) · Nature · doi:10.1038/346177a0 · Cited by 797 · see citing works
Self-citationLong-term potentiation and functional synapse induction in developing hippocampus
Durand, G. M., Kovalchuk, Y., & Konnerth, A. (1996) · Nature · doi:10.1038/381071a0 · Cited by 789 · see citing works
Calmodulin Trapping by Calcium-Calmodulin-Dependent Protein Kinase
Meyer, T., Hanson, P. I., Stryer, L., & Schulman, H. (1992) · Science · doi:10.1126/science.256.5060.1199 · Cited by 637 · see citing works
Regional distribution of type II Ca2+/calmodulin-dependent protein kinase in rat brain
Erondu, N., & Kennedy, M. (1985) · The Journal of Neuroscience · doi:10.1523/jneurosci.05-12-03270.1985 · Cited by 630 · 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
Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus
Dudek, S. M., & Bear, M. F. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-07-02910.1993 · Cited by 595 · see citing works
Burgin, K., Waxham, M., Rickling, S., Westgate, S., Mobley, W. C., & Kelly, P. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-06-01788.1990 · Cited by 564 · see citing works
Maturation 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 523 · see citing works
The CaM kinase II hypothesis for the storage of synaptic memory
Lisman, J. E. (1994) · Trends in Neurosciences · doi:10.1016/0166-2236(94)90014-0 · Cited by 499 · see citing works
Mutant Mice and Neuroscience: Recommendations Concerning Genetic Background
Silva, A. J., Simpson, E. M., Takahashi, J. S., Lipp, H.-P., Nakanishi, S., Wehner, J. M., Giese, K. P., Tully, T., Abel, T., Chapman, P. F., et al. (1997) · Neuron · doi:10.1016/s0896-6273(00)80958-7 · Cited by 479 · see citing works
Self-citationLledo, 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
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
Regulation of hippocampal transmitter release during development and long-term potentiation.
Bolshakov, V. Y., & Siegelbaum, S. (1995) · Science · doi:10.1126/science.7569903 · Cited by 385 · 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 384 · see citing works
Mayford, M., Baranes, D., Podsypanina, K., & Kandel, E. (1996) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.93.23.13250 · Cited by 346 · see citing works
Pettit, D. L., Perlman, S., & Malinow, R. (1994) · Science · doi:10.1126/science.7997883 · Cited by 329 · see citing works
Self-citationMiller, S. G., & Kennedy, M. B. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)39454-1 · Cited by 304 · 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
Ca2+/calmodulin-dependent protein kinase II. Isozymic forms from rat forebrain and cerebellum.
McGuinness, T. L., Lai, Y. Y., & Greengard, P. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)89650-8 · Cited by 296 · see citing works
Immunocytochemical localization of calcium/calmodulin-dependent protein kinase II in rat brain.
Ouimet, C. C., McGuinness, T. L., & Greengard, P. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.17.5604 · Cited by 293 · see citing works
Hanson, P. I., Kapiloff, M. S., Lou, L. L., Rosenfeld, M. G., & Schulman, H. (1989) · Neuron · doi:10.1016/0896-6273(89)90115-3 · Cited by 290 · see citing works
Chen, C., Rainnie, D. G., Greene, R. W., & Tonegawa, S. (1994) · Science · doi:10.1126/science.7939668 · Cited by 286 · see citing works
Self-citationResistance to Leishmania major Induced by Tolerance to a Single Antigen
Julia, V., Rassoulzadegan, M., & Glaichenhaus, N. (1996) · Science · doi:10.1126/science.274.5286.421 · Cited by 261 · 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
Developmental onset of long‐term potentiation in area CA1 of the rat hippocampus.
Harris, K. M., & Teyler, T. J. (1984) · The Journal of Physiology · doi:10.1113/jphysiol.1984.sp015005 · Cited by 252 · 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
Fukunaga, K., Muller, D., & Miyamoto, E. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.11.6119 · Cited by 226 · 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
Otmakhov, N., Griffith, L. C., & Lisman, J. E. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-14-05357.1997 · Cited by 207 · see citing works
Fukunaga, K., Goto, S., & Miyamoto, E. (1988) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1988.tb03070.x · Cited by 185 · see citing works
The role of calcium–calmodulin kinase II in three forms of synaptic plasticity
Stevens, C. F., Tonegawa, S., & Wang, Y. (1994) · Current Biology · doi:10.1016/s0960-9822(00)00153-6 · Cited by 182 · see citing works
Self-citationUnusual behavioral phenotypes of inbred mouse strains
Crawley, J. N. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)20021-9 · Cited by 179 · see citing works
Studies of the Regulatory Mechanism of Ca2+/Calmodulin-dependent protein kinase II
Fong, Y. L., Taylor, W. L., Means, A. R., & Soderling, T. R. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)84770-1 · Cited by 164 · see citing works
Requirement for α-CaMKII in Experience-Dependent Plasticity of the Barrel Cortex
Glazewski, S., Chen, C.-M., Silva, A. J., & Fox, K. D. (1996) · Science · doi:10.1126/science.272.5260.421 · Cited by 147 · see citing works
Mice, gene targeting and behaviour: more than just genetic background
Lathe, R. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)20022-0 · Cited by 145 · see citing works
Butler, L., Silva, A. J., Abeliovich, A., Watanabe, Y., Tonegawa, S., & McNamara, J. O. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.15.6852 · Cited by 135 · see citing works
Self-citationWaldmann, R., Hanson, P. I., & Schulman, H. (1990) · Biochemistry · doi:10.1021/bi00459a002 · Cited by 126 · see citing works
Developmental changes in synaptic properties in hippocampus of neonatal rats
Müller, D., Oliver, M. W., & LYNCH, G. S. (1989) · Developmental Brain Research · doi:10.1016/0165-3806(89)90063-1 · Cited by 124 · see citing works
Ito, I., Hidaka, H., & Sugiyama, H. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90663-e · Cited by 123 · 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
Gordon, J. A., Cioffi, D., Silva, A. J., & Stryker, M. P. (1996) · Neuron · doi:10.1016/s0896-6273(00)80181-6 · Cited by 111 · see citing works
Gene-targeting studies: new methods, old problems
Crusio, W. E. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)20023-2 · Cited by 107 · see citing works
4 Calmodulin-Dependent Protein Kinases
Stull, J. T., Nunnally, M. H., & Michnoff, C. H. (1986) · The Enzymes · doi:10.1016/s1874-6047(08)60429-1 · Cited by 105 · see citing works
Changes in the subcellular distribution of calmodulin-kinase II during brain development
Kelly, P. T., & Vernon, P. J. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90265-2 · Cited by 95 · see citing works
Deficiency in induction but not expression of LTP in hippocampal slices from young rats.Preprint
Liao, D., & Malinow, R. (1996) · Learning & Memory · doi:10.1101/lm.3.2-3.138 · Cited by 84 · see citing works
Self-citation[Ca2(+)-calmodulin-dependent protein kinase II].
Yamauchi, T., & Ohsako, S. (1990) · PubMed · Cited by 70 · see citing works
Waxham, M. N., Aronowski, J. A., Westgate, S. A., & Kelly, P. T. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.4.1273 · Cited by 60 · see citing works
Vallano, M. L., Goldenring, J. R., Lasher, R. S., & DeLorenzo, R. J. (1986) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1986.tb38406.x · Cited by 56 · see citing works
Hayashi, Y., Ishida, A., Katagiri, H., Mishina, M., Fujisawa, H., Manabe, T., & Takahashi, T. (1997) · Brain Research. Molecular Brain Research · doi:10.1016/s0169-328x(97)00073-9 · Cited by 40 · see citing works
(1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)20024-4 · Cited by 19 · see citing works
Flagged first, then by citations
1 of the 66 references couldn’t be matched to a known paper.
Research works printed but not linked: 2
- References Banbury conference. 1997. Neuron 19: 755-759.
- Butler, L.S., A.J. Silva, A. Abelovich, Y. Watanabe, S. ␣-CaMKII AND LTP Tonegawa, and J.O. McNamara. 1995. Limbic epilepsy in ␣-calcium-calmodulin kinase II mutant mice. Proc. Natl. Acad. Sci. 92: 6852-6855.
Cited by
Sorted by citations
Synaptic Plasticity and Memory: An Evaluation of the Hypothesis
Martin, S. J., Grimwood, P. D., & Morris, R. G. M. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.649 · Cited by 2,794 · 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
Hudmon, A., & Schulman, H. (2002) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.71.110601.135410 · Cited by 654 · see citing works
Miller, S., Yasuda, M., Coats, J., Jones, Y., Martone, M. E., & Mayford, M. R. (2002) · Neuron · doi:10.1016/s0896-6273(02)00978-9 · Cited by 507 · see citing works
Neural plasticity and behavior – sixty years of conceptual advances
Sweatt, J. D. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13580 · Cited by 341 · see citing works
CaMKII regulation in information processing and storage
Coultrap, S. J., & Bayer, K. U. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.05.003 · Cited by 313 · see citing works
Inhibitory Autophosphorylation of CaMKII Controls PSD Association, Plasticity, and Learning
Elgersma, Y., Fedorov, N. B., Ikonen, S., Choi, E. S., Elgersma, M., Carvalho, O. M., Giese, K. P., & Silva, A. J. (2002) · Neuron · doi:10.1016/s0896-6273(02)01007-3 · Cited by 290 · see citing works
Weeber, E. J., Jiang, Y., Elgersma, Y., Varga, A. W., Carrasquillo, Y., Brown, S. E., Christian, J. M., Mirnikjoo, B., Silva, A. J., Beaudet, A. L., et al. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-07-02634.2003 · Cited by 262 · 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
Coultrap, S. J., Freund, R. K., O’Leary, H., Sanderson, J. L., Roche, K. W., Dell’Acqua, M. L., & Bayer, K. U. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.01.005 · Cited by 207 · 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-citationVarga, 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
Elgersma, Y., Sweatt, J. D., & Giese, K.-P. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3622-04.2004 · Cited by 150 · see citing works
Yamagata, Y., Kobayashi, S., Umeda, T., Inoue, A., Sakagami, H., Fukaya, M., Watanabe, M., Hatanaka, N., Totsuka, M., Yagi, T., et al. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0707-09.2009 · Cited by 146 · see citing works
Gardoni, F., Mauceri, D., Malinverno, M., Polli, F., Costa, C., Tozzi, A., Siliquini, S., Picconi, B., Cattabeni, F., Calabresi, P., et al. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3921-08.2009 · Cited by 142 · 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
Nicoll, R. A., & Schulman, H. (2023) · Physiological Reviews · doi:10.1152/physrev.00034.2022 · Cited by 126 · see citing works
“206).”
Jiang, X. J., Lautermilch, N. J., Watari, H., Westenbroek, R. E., Scheuer, T., & Catterall, W. A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710213105 · Cited by 124 · see citing works
The role of α-CaMKII autophosphorylation in neocortical experience-dependent plasticity
Glazewski, S., Giese, K.-P., Silva, A. J., & Fox, K. D. (2000) · Nature Neuroscience · doi:10.1038/78820 · Cited by 114 · see citing works
LTP induction by structural rather than enzymatic functions of CaMKII
Tullis, J. E., Larsen, M. E., Rumian, N. L., Freund, R. K., Boxer, E. E., Brown, C. N., Coultrap, S. J., Schulman, H., Aoto, J., Dell’Acqua, M. L., et al. (2023) · Nature · doi:10.1038/s41586-023-06465-y · Cited by 112 · see citing works
Transient and sustained types of long‐term potentiation in the CA1 area of the rat hippocampus
Volianskis, A., & Jensen, M. S. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.044214 · Cited by 107 · see citing works
Hayashi, Y. (2022) · Neuroscience Research · doi:10.1016/j.neures.2021.08.001 · Cited by 102 · see citing works
Reversal of Synaptic Memory by Ca2+/Calmodulin-Dependent Protein Kinase II Inhibitor
Sanhueza, M., McIntyre, C., & Lisman, J. E. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5049-06.2007 · Cited by 100 · see citing works
Gerges, N. Z., Aleisa, A. M., Schwarz, L. A., & Alkadhi, K. A. (2004) · Hippocampus · doi:10.1002/hipo.10193 · Cited by 95 · see citing works
Memory Erasure Experiments Indicate a Critical Role of CaMKII in Memory Storage
Rossetti, T., Banerjee, S., Kim, C., Leubner, M., Lamar, C., Gupta, P., Lee, B., Neve, R., & Lisman, J. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.010 · Cited by 94 · see citing works
αCaMKII autophosphorylation: a fast track to memory
Irvine, E. E., von Hertzen, L. S. J., Plattner, F., & Giese, K.-P. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.06.009 · Cited by 92 · see citing works
Hinds, H. L., Goussakov, I. V., Nakazawa, K., Tonegawa, S., & Bolshakov, V. Y. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0530202100 · Cited by 89 · see citing works
Self-citationAleisa, A. M., Alzoubi, K. H., Gerges, N. Z., & Alkadhi, K. A. (2005) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145705005912 · Cited by 86 · see citing works
Cooke, S. F., Wu, J., Plattner, F., Errington, M., Rowan, M., Peters, M., Hirano, A., Bradshaw, K. D., Anwyl, R., Bliss, T. V. P., et al. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.111559 · Cited by 77 · see citing works
CAMK2-Dependent Signaling in Neurons Is Essential for Survival
Kool, M. J., Onori, M. P., Borgesius, N. Z., van de Bree, J. E., Elgersma, M., Nio, E., Bezstarosti, K., Buitendijk, G. H. S., Jolfaei, M. A., Demmers, J., et al. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1341-18.2019 · Cited by 77 · see citing works
CaMKII holoenzyme mechanisms that govern the LTP versus LTD decision
Cook, S. G., Buonarati, O. R., Coultrap, S. J., & Bayer, K. U. (2021) · Science Advances · doi:10.1126/sciadv.abe2300 · Cited by 74 · see citing works
Synaptic memory requires CaMKII
Tao, W., Lee, J., Chen, X., Díaz-Alonso, J., Zhou, J., Pleasure, S., & Nicoll, R. A. (2021) · eLife · doi:10.7554/elife.60360 · Cited by 72 · see citing works
Bevilaqua, L. R., Medina, J. H., Izquierdo, I., & Cammarota, M. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.007 · Cited by 69 · see citing works
Participation of CaMKII in Neuronal Plasticity and Memory Formation
Cammarota, M., Bevilaqua, L. R., Viola, H., Kerr, D. S., Reichmann, B. P., Teixeira, V., Bulla, M. C., Izquierdo, I., & Medina, J. H. (2002) · Cellular and Molecular Neurobiology · doi:10.1023/a:1020763716886 · Cited by 65 · see citing works
Nicotinic modulation of hippocampal cell signaling and associated effects on learning and memory
Kutlu, M. G., & Gould, T. J. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.12.008 · Cited by 62 · see citing works
Alzoubi, K. H., Aleisa, A. M., Gerges, N. Z., & Alkadhi, K. A. (2006) · Journal of Neuroscience Research · doi:10.1002/jnr.21014 · Cited by 60 · see citing works
Mohanan, A. G., Gunasekaran, S., Jacob, R. S., & Omkumar, R. V. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.855752 · Cited by 57 · see citing works
Mayeux‐Portas, V., File, S. E., Stewart, C. L., & Morris, R. J. (2000) · Current Biology · doi:10.1016/s0960-9822(99)00278-x · Cited by 53 · see citing works
A fresh look at the role of CaMKII in hippocampal synaptic plasticity and memory
Rongo, C. (2002) · BioEssays · doi:10.1002/bies.10057 · Cited by 50 · see citing works
Klug, J. R., Mathur, B. N., Kash, T. L., Wang, H.-D., Matthews, R. T., Robison, A. J., Anderson, M. E., Deutch, A. Y., Lovinger, D. M., Colbran, R. J., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045323 · Cited by 49 · 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
LTP in hippocampal neurons is associated with a CaMKII-mediated increase in GluA1 surface expression
Appleby, V. J., Corrêa, S. A. L., Duckworth, J. K., Nash, J. E., Noël, J., Fitzjohn, S. M., Collingridge, G. L., & Molnár, E. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.07133.x · Cited by 43 · see citing works
ERK1/2 and CaMKII-mediated events in memory formation: Is 5HT regulation involved?
Cammarota, M., Bevilaqua, L. R., Medina, J. H., & Izquierdo, I. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.11.029 · Cited by 40 · see citing works
Molecular Alterations in the Hippocampus after Experimental Subarachnoid Hemorrhage
Han, S. M., Wan, H., Kudo, G., Foltz, W. D., Vines, D. C., Green, D. E., Zoerle, T., Tariq, A., Brathwaite, S., D’Abbondanza, J. A., et al. (2013) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2013.170 · Cited by 40 · see citing works
Matthies, H., Schröeder, H., Becker, A., Loh, H. H., Höllt, V., & Krug, M. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(99)00203-8 · Cited by 40 · see citing works
Moutal, A., Cai, S., Yu, J., Stratton, H. J., Chefdeville, A., Gómez, K., Ran, D., Madura, C. L., Boinon, L., Soto, M., et al. (2020) · Pain · doi:10.1097/j.pain.0000000000001951 · Cited by 37 · see citing works
Half a century legacy of long-term potentiation
Caya-Bissonnette, L., & Béïque, J.-C. (2024) · Current Biology · doi:10.1016/j.cub.2024.05.008 · Cited by 36 · see citing works
Gao, J., Peng, S.-J., Xiang, S.-Q., Huang, J., & Chen, P. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.11.061 · Cited by 36 · see citing works
Long-Term Potentiation and Depression as Putative Mechanisms for Memory Formation
Escobar, M. L., & Derrick, B. E. (2007) · Frontiers in neuroscience · doi:10.1201/9781420008418.ch2 · Cited by 36 · see citing works
Hippocampal glutamate receptors in fear memory consolidation
Cammarota, M., Bevilaqua, L. R., Bonini, J. S., Rossato, J. I., Medina, J. H., & Izquierdo, N. (2004) · Neurotoxicity Research · doi:10.1007/bf03033222 · Cited by 34 · see citing works
Developmental and Activity Dependent Regulation of Ionotropic Glutamate Receptors at Synapses
Molnár, E., & Isaac, J. T. R. (2002) · The Scientific World JOURNAL · doi:10.1100/tsw.2002.74 · Cited by 33 · see citing works
Gartside, S. E., Leitch, M. M., McQuade, R., & Swarbrick, D. J. (2002) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300104 · Cited by 32 · see citing works
Hippocampal long term potentiation: silent synapses and beyond
Poncer, J. C. (2003) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2004.01.003 · Cited by 31 · see citing works
Winder, D. G., & Schramm‐Sapyta, N. L. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00514-5 · Cited by 30 · see citing works
Inducible molecular switches for the study of long-term potentiation
Hédou, G., & Mansuy, I. M. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1245 · Cited by 25 · see citing works
StimDuino: An Arduino-based electrophysiological stimulus isolator
Sheinin, A., Lavi, A., & Michaelevski, I. (2015) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2015.01.016 · Cited by 23 · see citing works
Nuclear transcription factors in the hippocampus
Hinoi, E., Balcar, V. J., Kuramoto, N., Nakamichi, N., & Yoneda, Y. (2002) · Progress in Neurobiology · doi:10.1016/s0301-0082(02)00078-3 · Cited by 20 · see citing works
Kaitsuka, T., Fukunaga, K., Soeda, F., Shirasaki, T., Miyamoto, E., & Takahama, K. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.10.051 · Cited by 19 · see citing works
Zhou, R., Holmes, A., Du, J., Malkesman, O., Yuan, P., Wang, Y., Damschroder-Williams, P. J., Chen, G., Guitart, X., & Manji, H. K. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.07022.x · Cited by 18 · see citing works
(−)Clausenamide facilitates synaptic transmission at hippocampal Schaffer collateral-CA1 synapses
Ning, N., Hu, J., Sun, J., Han, N., Zhang, J., & Chen, N. (2012) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2012.02.004 · Cited by 18 · see citing works
In memoriam: John Lisman – commentaries on CaMKII as a memory molecule
Bear, M. F., Cooke, S. F., Giese, K.-P., Kaang, B., Kennedy, M. B., Kim, J., Morris, R., & Park, P. (2018) · Molecular Brain · doi:10.1186/s13041-018-0419-y · Cited by 17 · see citing works
The role of regulatory domain interactions in UNC-43 CaMKII localization and trafficking
Umemura, T., Rapp, P., & Rongo, C. (2005) · Journal of Cell Science · doi:10.1242/jcs.02457 · Cited by 16 · see citing works
Loss of MsrB1 perturbs spatial learning and long-term potentiation/long-term depression in mice
Shi, T., Yang, Y., Zhang, Z.-H., Zhang, L., Song, J., Ping, Y., Du, X., Song, G.-L., Liu, Q., & Li, N. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107104 · Cited by 17 · see citing works
Villers, A., Giese, K. P., & Ris, L. (2014) · Learning & Memory · doi:10.1101/lm.035972.114 · Cited by 16 · see citing works
Lee, H., & Huganir, R. L. (2008) · Elsevier eBooks · doi:10.1016/b978-012370509-9.00035-8 · Cited by 15 · see citing works
Developmental restoration of LTP deficits in heterozygous CaMKIIα KO mice
Goodell, D. J., Benke, T. A., & Bayer, K. U. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00518.2016 · Cited by 12 · see citing works
Rigter, P. M. F., Wallaard, I., Jolfaei, M. A., Kingma, J., Post, L. C., Elgersma, M., Elgersma, Y., & van Woerden, G. M. (2022) · iScience · doi:10.1016/j.isci.2022.105303 · Cited by 10 · see citing works
Noel, S. C., Madranges, J. F., Gothié, J. M., Ewald, J., Milnerwood, A. J., Kennedy, T. E., & Scott, M. E. (2024) · Scientific Reports · doi:10.1038/s41598-024-60865-2 · Cited by 6 · see citing works
Baumgärtel, K., Fernández, C., Johansson, T., & Mansuy, I. M. (2007) · Springer eBooks · doi:10.1007/978-3-540-35109-2_13 · Cited by 5 · 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
The Organization and Integrative Function of the Post-Synaptic Proteome
Grant, S. G. N., Husi, H., Choudhary, J. S., Cumiskey, M. A., Blackstock, W. P., & Armstrong, J. D. (2003) · Springer eBooks · doi:10.1007/978-1-4615-0039-1_2 · Cited by 4 · see citing works
Ingram, R., Volianskis, R., Georgiou, J., Jane, D. E., Michael-Titus, A. T., Collingridge, G. L., & Volianskis, A. (2024) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2023.0239 · Cited by 3 · see citing works
Two selected models of missense mutations in mice for the study of learning behaviour
Mohajeri, M. H., & Giese, K.-P. (2011) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2011.12.003 · Cited by 2 · see citing works
Biochemical Mechanisms for Short-Term Information Storage at the Cellular Level
Sweatt, J. D. (2003) · Elsevier eBooks · doi:10.1016/b978-012678957-7/50009-8 · Cited by 2 · see citing works
Andrus, M. D., Vu, T., Juarez, B., & Walker, D. M. (2025) · Neuropharmacology · doi:10.1016/j.neuropharm.2025.110629 · Cited by 1 · see citing works
Transcriptional Mechanisms Underlying the Mammalian Circadian Clock
Cheng, H. M., & Obrietan, K. H. (2007) · Springer eBooks · doi:10.1007/978-0-387-73609-9_16 · Cited by 1 · see citing works
Ishikawa, Y., & Shiosaka, S. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1761-7_4 · Cited by 1 · see citing works
Sweatt, J. D. (2003) · Elsevier eBooks · doi:10.1016/b978-012678957-7/50011-6 · Cited by 1 · see citing works
Biochemical Mechanisms for Information Storage at the Cellular Level
Sweatt, J. D. (2010) · Elsevier eBooks · doi:10.1016/b978-0-12-374951-2.00009-3
Whissell, P. D. (2014) · TSpace (University of Toronto)
Ishikawa, Y., & Shiosaka, S. (2024) · Springer eBooks · doi:10.1007/978-3-031-54864-2_9
- Authors
- Hinds, H. L., Tonegawa, S., & Malinow, R.
- Affiliations
- Howard Hughes Medical Institute (US)
- Venue
- Learning & Memory
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 1998-09-01
- Volume
- 5
- Issue
- 4
- Pages
- 344-354
- ISSN
- 1072-0502 (ISSN-L)
- 1549-5485
- PMC
- PMC311262
- OpenAlex
- W2146518447
- Cited by
- 86
- References
- 66
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 4 · 2023: 2 · 2022: 3 · 2021: 3 · 2020: 1 · 2019: 2 · 2018: 1 · 2017: 1 · 2016: 2 · 2015: 2 · 2014: 4 · 2013: 2 · 2012: 4
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Learning & Memory (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (NS-32925, R01NS032925)
- 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
- CaMKIIα, calcium/calmodulin-dependent protein kinase II, long-term potentiation, hippocampal CA1, mouse mutants, synaptic transmission, input-output curves, tetanic stimulation, APV
- MeSH terms
- Animals, Crosses, Genetic, Electric Stimulation, Female, Hippocampus, Male, Mice, Inbred BALB C, Mice, Inbred C57BL, Mice, Inbred Strains, Neurons, Regression Analysis, Synapses, Long-Term Potentiation, Calcium-Calmodulin-Dependent Protein Kinases, Mice, Knockout, Mice, 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