Mechanism for long-term memory formation when synaptic strengthening is impaired
Open accessAbstract
Long-term memory (LTM) formation has been linked with functional strengthening of existing synapses and other processes including de novo synaptogenesis. However, it is unclear whether synaptogenesis can contribute to LTM formation. Here, using α-calcium/calmodulin kinase II autophosphorylation-deficient (T286A) mutants, we demonstrate that when functional strengthening is severely impaired, contextual LTM formation is linked with training-induced PSD95 up-regulation followed by persistent generation of multiinnervated spines, a type of synapse that is characterized by several presynaptic terminals contacting the same postsynaptic spine. Both PSD95 up-regulation and contextual LTM formation in T286A mutants required signaling by the mammalian target of rapamycin (mTOR). Furthermore, we show that contextual LTM resists destabilization in T286A mutants, indicating that LTM is less flexible when synaptic strengthening is impaired. Taken together, we suggest that activation of mTOR signaling, followed by overexpression of PSD95 protein and synaptogenesis, contributes to formation of invariant LTM when functional strengthening is impaired.
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NMDAR-dependent LTP is greatly impaired when T286 is replaced by T286A.
“Foremost are data, now long accepted, that NMDAR-dependent LTP is greatly impaired when T286 is replaced by T286A (43, 121, 381–384).”
From Synaptic memory and CaMKII (2023) · cites this paper as [384]
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Cites
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · 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
Rapid formation and selective stabilization of synapses for enduring motor memories
Xu, T., Yu, X., Perlik, A. J., Tobin, W. F., Zweig, J. A., Tennant, K., Jones, T., & Zuo, Y. (2009) · Nature · doi:10.1038/nature08389 · Cited by 1,193 · see citing works
Stably maintained dendritic spines are associated with lifelong memories
Yang, G., Pan, F., & Gan, W.-B. (2009) · Nature · doi:10.1038/nature08577 · Cited by 1,182 · 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
Self-citationJones, M. W., Errington, M. L., French, P. J., Fine, A., Bliss, T., Garel, S., Charnay, P., Bozon, B., Laroche, S., & Davis, S. (2001) · Nature Neuroscience · doi:10.1038/85138 · Cited by 899 · see citing works
A single standard for memory: The case for reconsolidation
Nader, K., & Hardt, O. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2590 · Cited by 811 · see citing works
Postsynaptic receptor trafficking underlying a form of associative learning
Rumpel, S., LeDoux, J., Zador, A., & Malinow, R. (2005) · Science · doi:10.1126/science.1103944 · Cited by 775 · see citing works
Rampon, C., Tang, Y.-P., Goodhouse, J., Shimizu, E., Kyin, M., & Tsien, J. Z. (2000) · Nature Neuroscience · doi:10.1038/72945 · Cited by 737 · see citing works
Translational Regulatory Mechanisms in Persistent Forms of Synaptic Plasticity
Kelleher, R. J., Govindarajan, A., & Tonegawa, S. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.013 · Cited by 592 · see citing works
Associative Memory Formation Increases the Observation of Dendritic Spines in the Hippocampus
Leuner, B., Falduto, J., & Shors, T. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-02-00659.2003 · Cited by 403 · see citing works
Fleischmann, A., Hvalby, Ø., Jensen, V., Strekalova, T. V., Zacher, C., Layer, L. E., Kvello, A., Reschke, M., Spanagel, R., Sprengel, R., et al. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-27-09116.2003 · Cited by 382 · see citing works
Rapid Erasure of Long-Term Memory Associations in the Cortex by an Inhibitor of PKMζ
Shema, R., Sacktor, T. C., & Dudai, Y. (2007) · Science · doi:10.1126/science.1144334 · Cited by 353 · see citing works
Role of mTOR in physiology and pathology of the nervous system
Swiech, L., Perycz, M., Malik, A., & Jaworski, J. (2008) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2007.08.015 · Cited by 338 · see citing works
A developmental switch in the signaling cascades for LTP induction
Yasuda, H., Barth, A. L., Stellwagen, D., & Malenka, R. C. (2003) · Nature Neuroscience · doi:10.1038/nn985 · Cited by 325 · see citing works
Restivo, L., Vetere, G., Bontempi, B., & Ammassari‐Teule, M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0966-09.2009 · Cited by 322 · see citing works
Spine-Type-Specific Recruitment of Newly Synthesized AMPA Receptors with Learning
Matsuo, N., Reijmers, L. G. J. E., & Mayford, M. R. (2008) · Science · doi:10.1126/science.1149967 · Cited by 296 · see citing works
Associative Learning Elicits the Formation of Multiple-Synapse Boutons
Geinisman, Y., Berry, R. W., Disterhoft, J. F., Power, J., & van der Zee, E. A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-15-05568.2001 · Cited by 254 · see citing works
Parsons, R. G., Gafford, G. M., & Helmstetter, F. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4209-06.2006 · Cited by 251 · see citing works
Lee, C.-C., Huang, C., Wu, M.-Y., & Hsu, K. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m414112200 · Cited by 199 · see citing works
Memory Reconsolidation Engages Only a Subset of Immediate-Early Genes Induced during Consolidation
von Hertzen, L. S. J., & Giese, K.-P. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4707-04.2005 · Cited by 185 · see citing works
Self-citationPopov, V. I., Medvedev, N. I., Davies, H. A., & Stewart, M. G. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20682 · Cited by 175 · see citing works
Self-citationPSD-95 promotes synaptogenesis and multiinnervated spine formation through nitric oxide signaling
Nikonenko, I., Boda, B., Steen, S., Knott, G. W., Welker, E., & Müller, D. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200805132 · Cited by 173 · see citing works
Chapter 11 Spine dynamics and synapse remodeling during LTP and memory processes
Roo, M. D., Klauser, P., Garcia, P. M., Poglia, L., & Müller, D. (2008) · Progress in brain research · doi:10.1016/s0079-6123(07)00011-8 · Cited by 135 · see citing works
Popov, V. I., Davies, H. A., Rogachevsky, V. V., Patrushev, I., Errington, M. L., Gabbott, P. L. A., Bliss, T. V. P., & Stewart, M. G. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.06.029 · Cited by 121 · see citing works
Self-citationαCaMKII autophosphorylation contributes to rapid learning but is not necessary for memory
Irvine, E. E., Vernon, J., & Giese, K. P. (2005) · Nature Neuroscience · doi:10.1038/nn1431 · Cited by 119 · see citing works
Self-citationPetrak, L. J., Harris, K. M., & Kirov, S. A. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20468 · Cited by 112 · see citing works
Sensory Input Enhances Synaptogenesis of Adult-Born Neurons
Livneh, Y., Feinstein, N., Klein, M. E., & Mizrahi, A. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4105-08.2009 · Cited by 106 · 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
Self-citationModulation of excitability as a learning and memory mechanism: A molecular genetic perspective
Giese, K.-P., Peters, M., & Vernon, J. D. R. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00517-0 · Cited by 66 · see citing works
Self-citationBelelovsky, K., Kaphzan, H., Elkobi, A., & Rosenblum, K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3809-08.2009 · Cited by 62 · see citing works
Kimura, R., Silva, A. J., & Ohno, M. (2008) · Learning & Memory · doi:10.1101/lm.1049608 · Cited by 44 · see citing works
Parsons, R. G., Riedner, B. A., Gafford, G. M., & Helmstetter, F. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.04.078 · Cited by 40 · see citing works
Properties of Contextual Memory Formed in the Absence of αCaMKII Autophosphorylation
Irvine, E. E., Danhiez, A., Radwańska, K., Nassim, C., Lucchesi, W., Godaux, E., Ris, L., & Giese, K.-P. (2011) · Molecular Brain · doi:10.1186/1756-6606-4-8 · Cited by 34 · see citing works
Self-citationOhno, M., Sametsky, E. A., Silva, A. J., & Disterhoft, J. F. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04746.x · Cited by 34 · see citing works
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Mechanisms of CaMKII action in long-term potentiation
Lisman, J., Yasuda, R., & Raghavachari, S. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3192 · Cited by 1,134 · see citing works
Decay happens: the role of active forgetting in memory
Hardt, O., Nader, K., & Nadel, L. (2013) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.01.001 · Cited by 416 · see citing works
CaM Kinase: Still Inspiring at 40
Bayer, K. U., & Schulman, H. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.033 · Cited by 307 · see citing works
The roles of protein kinases in learning and memoryPreprint
Giese, K.-P., & Mizuno, K. (2013) · Learning & Memory · doi:10.1101/lm.028449.112 · Cited by 229 · see citing works
Self-citationCalcium/calmodulin-dependent kinase II and Alzheimer’s disease
Ghosh, A., & Giese, K. P. (2015) · Molecular Brain · doi:10.1186/s13041-015-0166-2 · Cited by 205 · see citing works
Self-citationCalmodulin kinases: essential regulators in health and disease
Takemoto‐Kimura, S., Suzuki, K., Horigane, S., Kamijo, S., Inoue, M., Sakamoto, M., Fujii, H., & Bito, H. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14020 · Cited by 171 · see citing works
Yuki, D., Sugiura, Y., Zaima, N., Akatsu, H., Takei, S., Yao, I., Maesako, M., Kinoshita, A., Yamamoto, T., Kon, R., et al. (2014) · Scientific Reports · doi:10.1038/srep07130 · Cited by 137 · see citing works
Targeting the mTOR Signaling Network for Alzheimer’s Disease Therapy
Wang, C., Yu, J., Miao, D., Wu, Z., Tan, M., & Tan, L. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8505-8 · Cited by 133 · see citing works
Jarome, T. J., & Helmstetter, F. J. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.03.009 · Cited by 133 · see citing works
Nicoll, R. A., & Schulman, H. (2023) · Physiological Reviews · doi:10.1152/physrev.00034.2022 · Cited by 126 · see citing works
Tan, M. C., Widagdo, J., Chau, Y. Q., Zhu, T., Wong, J. J. L., Cheung, A., & Anggono, V. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00124 · Cited by 83 · see citing works
Downregulated AKT-mTOR signaling pathway proteins in dorsolateral prefrontal cortex in Schizophrenia
Chadha, R., & Meador-Woodruff, J. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0614-2 · Cited by 63 · see citing works
Synaptic modifications in learning and memory – A dendritic spine story
Ma, S., & Zuo, Y. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.05.015 · Cited by 64 · see citing works
Upregulation of AMPK Ameliorates Alzheimer’s Disease-Like Tau Pathology and Memory Impairment
Wang, L., Li, N., Shi, F.-X., Xu, W., Cao, Y., Lei, Y., Wang, J., Tian, Q., & Zhou, X. (2020) · Molecular Neurobiology · doi:10.1007/s12035-020-01955-w · Cited by 57 · see citing works
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Tyrtyshnaia, A. A., & Manzhulo, I. (2020) · Journal of Pain Research · doi:10.2147/jpr.s238458 · Cited by 58 · see citing works
Eltokhi, A., Santuy, A., Merchán-Pérez, Á., & Sprengel, R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010059 · Cited by 52 · 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
Sun, Y., Smirnov, M., Kamasawa, N., & Yasuda, R. (2021) · The Journal of Neuroscience · doi:10.1523/jneurosci.1964-20.2021 · Cited by 51 · see citing works
Santuy, A., Rodríguez, J., DeFelipe, J., & Merchán-Pérez, Á. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1470-7 · Cited by 49 · see citing works
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Martínez-Serra, R., Alonso‐Nanclares, L., Cho, K., & Giese, K.-P. (2022) · Brain Communications · doi:10.1093/braincomms/fcac083 · Cited by 47 · see citing works
Self-citationAziz, W., Kraev, I., Mizuno, K., Kirby, A. J., Fang, T., Rupawala, H., Kasbi, K., Rothe, S., Jozsa, F., Rosenblum, K., et al. (2019) · Current Biology · doi:10.1016/j.cub.2019.08.064 · Cited by 44 · see citing works
Self-citationPena, R. R., Pereira-Caixeta, A. R., Moraes, M. F. D., & Pereira, G. S. (2014) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2014.10.009 · Cited by 43 · see citing works
Self-citationHo, J. K., & Nation, D. A. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.05.005 · Cited by 45 · see citing works
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Gao, C., Tronson, N. C., & Radulović, J. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.04.014 · Cited by 41 · see citing works
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Roesler, R. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.04.015 · Cited by 37 · see citing works
Burgdorf, C. E., Schierberl, K. C., Lee, A. S., Fischer, D. K., Kempen, T. A. V., Mudragel, V., Huganir, R. L., Milner, T. A., Glass, M. J., & Rajadhyaksha, A. M. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2397-17.2017 · Cited by 36 · see citing works
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Self-citationPattern and predictability in memory formation: From molecular mechanisms to clinical relevance
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Coultrap, S. J., Barcomb, K., & Bayer, K. U. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037176 · Cited by 33 · see citing works
Generation of multi-innervated dendritic spines as a novel mechanism of long-term memory formation
Giese, K.-P., Aziz, W., Kraev, I., & Stewart, M. G. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.04.009 · Cited by 32 · see citing works
Self-citationObject recognition memory and temporal lobe activation after delayed estrogen replacement therapy
Fonseca, C. S., Gusmão, I. D., Raslan, A. C. S., Monteiro, B. M. M., Massensini, A. R., Moraes, M. F. D., & Pereira, G. S. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.12.016 · Cited by 32 · see citing works
Self-citationMicroRNAs and gene regulation in breast cancer
Abdalla, F., Singh, B. P., & Bhat, H. K. (2020) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.22567 · Cited by 31 · see citing works
Xu, J., Sui, W., Wang, S., Xu, X., Yuan, R.-R., Chen, X., Ma, H., Zhu, Y., Sun, J., Yi, F., et al. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2773-16.2017 · Cited by 30 · see citing works
Doria, J. G., de Souza, J. M., da Silva, F. R., Olmo, I. G., Carvalho, T. G., Alves‐Silva, J., Ferreira-Vieira, T. H., Santos, J. T., Xavier, C. Q. S., Silva, N. C., et al. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14555 · Cited by 29 · see citing works
Song, J., Cheon, S. Y., Lee, W. T., Park, K. A., & Lee, J. E. (2015) · Neural Plasticity · doi:10.1155/2015/374520 · Cited by 29 · see citing works
Changes of Synaptic Structures Associated with Learning, Memory and Diseases
Yang, Y., Lu, J., & Zuo, Y. (2018) · Brain Science Advances · doi:10.26599/bsa.2018.2018.9050012 · Cited by 27 · see citing works
Harda, Z., Łukasiewicz, K., Ziółkowska, M., Lipiński, M., Cały, A., Matuszek, Ż., Łęski, S., & Radwańska, K. (2015) · Addiction Biology · doi:10.1111/adb.12327 · Cited by 25 · see citing works
Self-citationThe importance of ultrastructural analysis of memory
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Self-citationAngiotensin-(1-7)/Mas axis modulates fear memory and extinction in mice
Lazaroni, T. L. D. N., Bastos, C. P., Moraes, M. F. D., Santos, R. A. S., & Pereira, G. S. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.11.012 · Cited by 22 · see citing works
Self-citationStructure and Complexity of the Synapse and Dendritic Spine
Stewart, M. G., Popov, V. I., Kraev, I., Medvedev, N. I., & Davies, H. A. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-418675-0.00001-8 · Cited by 21 · see citing works
Self-citationDietary cholesterol alters memory and synaptic structural plasticity in young rat brain
Ya, B., Liu, W., Feng, G., Zhang, Y., Zhu, B., & Bai, B. (2012) · Neurological Sciences · doi:10.1007/s10072-012-1241-4 · Cited by 20 · see citing works
Treadmill Exercise Improves Memory Function Depending on Circadian Rhythm Changes in Mice
Hwang, D. S., Kwak, H. B., Ko, I. G., Kim, S. E., Jin, J. J., Ji, E. S., Choi, H. H., & Kwon, O. Y. (2016) · International Neurourology Journal · doi:10.5213/inj.1632738.369 · Cited by 20 · see citing works
Phosphorylation of PSD-95 at serine 73 in dCA1 is required for extinction of contextual fear
Ziółkowska, M., Borczyk, M., Cały, A., Nalberczak‐Skóra, M., Śliwińska, M. A., Robacha, M., Łukasiewicz, K., Skonieczna, E., Tomaszewski, K. F., Tomaszewski, K. F., et al. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3002106 · Cited by 18 · see citing works
Śliwińska, M. A., Cały, A., Borczyk, M., Ziółkowska, M., Skonieczna, E., Chilimoniuk, M., Bernaś, T., Giese, K.-P., & Radwańska, K. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz261 · Cited by 16 · see citing works
Self-citationVillers, A., Giese, K. P., & Ris, L. (2014) · Learning & Memory · doi:10.1101/lm.035972.114 · Cited by 16 · see citing works
Self-citationChen, C., Gung, P., Ho, Y., Hamdin, C. D., & Yet, S. (2023) · British Journal of Pharmacology · doi:10.1111/bph.16157 · Cited by 14 · see citing works
Wnt Signaling Through Nitric Oxide Synthase Promotes the Formation of Multi-Innervated Spines
McLeod, F., Boyle, K. A., Marzo, A., Martín‐Flores, N., Moe, T. Z., Palomer, E., Gibb, A. J., & Salinas, P. C. (2020) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2020.575863 · Cited by 14 · see citing works
Sheppard, P. A. S., Asling, H. A., Mooradally, A. W., Armstrong, S. E., Elad, V. M., Lalonde, J., & Choleris, E. (2021) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2021.105232 · Cited by 14 · see citing works
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Yamagata, Y., Yanagawa, Y., & Imoto, K. (2018) · eNeuro · doi:10.1523/eneuro.0133-18.2018 · Cited by 12 · see citing works
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Puścian, A., Winiarski, M. J., Borowska, J., Łęski, S., Górkiewicz, T., Chaturvedi, M., Nowicka, K., Wołyniak, M., Chmielewska, J. J., Nikolaev, T., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01527-5 · Cited by 11 · see citing works
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Self-citationHan, W., Xian-fen, Z., Yang, S.-M., Dai, P., Liu, J., Wu, W., Huang, D., & Han, D. (2011) · PubMed · Cited by 9 · see citing works
March, A., Borchelt, D., Golde, T. E., & Janus, C. (2014) · PubMed Central · Cited by 9 · see citing works
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Andersen, J. M., Opdal, S. H., Müller, C. P., & Boix, F. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112676 · Cited by 7 · see citing works
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Carneiro, C. F. D., Amorim, F. E., & Amaral, O. B. (2023) · Peer Community Journal · doi:10.24072/pcjournal.339 · Cited by 5 · see citing works
Fang, T., Kasbi, K., Rothe, S., Aziz, W., & Giese, K.-P. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.06.012 · Cited by 5 · see citing works
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Sun, Y., Smirnov, M., Kamasawa, N., & Yasuda, R. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/840629 · Cited by 4 · see citing works
Herpich, M. E., Guarnieri, L. D. O., de Oliveira, A. C. P., & Moraes, M. F. D. (2024) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2024.110076 · Cited by 3 · see citing works
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Garofalo, S. (2023) · Peer community in neuroscience. · doi:10.24072/pci.neuro.100144 · Cited by 1 · see citing works
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Mohajeri, M. H., & Giese, K.-P. (2011) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2011.12.003 · Cited by 2 · see citing works
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Ziółkowska, M., Borczyk, M., Nowacka, A., Nalberczak‐Skóra, M., Śliwińska, M. A., Robacha, M., Łukasiewicz, K., Cały, A., Skonieczna, E., Tomaszewski, K. F., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.13.381368 · Cited by 1 · see citing works
Hung, J. (2014) · Libraries and Cultural Resources (University of Calgary) · doi:10.5072/prism/27087
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Radwańska, K., & Giese, K.-P. (2015) · Springer eBooks · doi:10.1007/978-3-319-24364-1_5
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Ritchie, L. (2015) · STAX · doi:10.48730/t659-vj95
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Vigil, F. A., & Giese, K.-P. (2015) · Springer eBooks · doi:10.1007/978-3-319-24364-1_4
Self-citationSheppard, P. A. S. (2018) · The Atrium (University of Guelph)
Astrocyte-neuron lactate shuttle and pain
Miyamoto, K., & Ohsawa, M. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-820589-1.00014-2
Rusakov, D. A., Giese, K.-P., Sandi, C., Dommett, E. J., & Overton, P. G. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.108962
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Rusakov, D. A. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.01.003
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Tomaszewski, K. F., Łukasiewicz, K., Robacha, M., & Radwańska, K. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.09.17.558133
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Ziółkowska, M., Sotoudeh, N., Cały, A., Puchalska, M., Pagano, R., Śliwińska, M. A., Salamian, A., & Radwańska, K. (2024) · eLife · doi:10.7554/elife.101736
Ziółkowska, M., Sotoudeh, N., Cały, A., Puchalska, M., Pagano, R., Śliwińska, M. A., Salamian, A., & Radwańska, K. (2024) · eLife · doi:10.7554/elife.101736.1
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Bayer, K. U., Brown, C. N., & Giese, K.-P. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15754-7.00057-2
Self-citationComputational analysis of learning in young and ageing brains
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Self-citationMartínez-Serra, R., Lee, S., Kraev, I., & Giese, K.-P. (2025) · Molecular Brain · doi:10.1186/s13041-025-01265-z
Self-citation
- Authors
- Radwanska, K., Medvedev, N. I., Pereira, G. S., Engmann, O., Thiede, N., Moraes, M. F. D., Villers, A., Irvine, E. E., Maunganidze, N. S., Pyza, E. M., Ris, L., Szymańska, M., Lipiński, M., Kaczmarek, L., Stewart, M. G., & Giese, K. P.
- Affiliations
- Institute of Psychiatry, King's College London, London SE5 9NU, United Kingdom;
- The Open University (GB)
- Universidade Federal de Minas Gerais (BR)
- King's College London (GB)
- University of Freiburg (DE)
- University of Mons (BE)
- University College London (GB)
- Jagiellonian University (PL)
- Instytut Biologii Doświadczalnej im. Marcelego Nenckiego (PL)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2011-10-24
- Volume
- 108
- Issue
- 45
- Pages
- 18471-18475
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3215030
- OpenAlex
- W2110813649
- Cited by
- 97
- References
- 35
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 8 · 2023: 8 · 2022: 8 · 2021: 8 · 2020: 9 · 2019: 7 · 2018: 8 · 2017: 7 · 2016: 1 · 2015: 9 · 2014: 6 · 2013: 7 · 2012: 4
- FWCI
- 3.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Research Portal (King's College London) (submittedVersion)
- ORBi UMONS (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH087463)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- long-term memory formation, synaptic strengthening, synaptogenesis, calcium/calmodulin-dependent protein kinase II, PSD-95, mTOR signaling, contextual memory, memory stability
- MeSH terms
- Disks Large Homolog 4 Protein, Animals, Hippocampus, Membrane Proteins, Phosphorylation, Synapses, Up-Regulation, Genes, Immediate-Early, Sirolimus, Mice, Guanylate Kinases, Calcium-Calmodulin-Dependent Protein Kinase Type 2, Memory, Long-Term, TOR Serine-Threonine Kinases
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