PKMζ maintains memories by regulating GluR2-dependent AMPA receptor trafficking
Abstract
The maintenance of long-term memory in hippocampus, neocortex and amygdala requires the persistent action of the atypical protein kinase C isoform, protein kinase Mzeta (PKMzeta). We found that inactivating PKMzeta in the amygdala impaired fear memory in rats and that the extent of the impairment was positively correlated with a decrease in postsynaptic GluR2. Blocking the GluR2-dependent removal of postsynaptic AMPA receptors abolished the behavioral impairment caused by PKMzeta inhibition and the associated decrease in postsynaptic GluR2 expression, which correlated with performance. Similarly, blocking this pathway for removal of GluR2-containing receptors from postsynaptic sites in amygdala slices prevented the reversal of long-term potentiation caused by inactivating PKMzeta. Similar behavioral results were obtained in the hippocampus for unreinforced recognition memory of object location. Together, these findings indicate that PKMzeta maintains long-term memory by regulating the trafficking of GluR2-containing AMPA receptors, the postsynaptic expression of which directly predicts memory retention.
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?
These effects were regulated by glutamate subunit 2-dependent AMPA-R.
“these effects were regulated by glutamate subunit 2-dependent AMPA-R”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Migues et al., 2010
Cites
Modality-Specific Retrograde Amnesia of Fear
Kim, J. J., & Fanselow, M. S. (1992) · Science · doi:10.1126/science.1585183 · Cited by 2,483 · see citing works
Learning induces long-term potentiation in the hippocampus
Whitlock, J. R., Heynen, A. J., Shuler, M. G., & Bear, M. F. (2006) · Science · doi:10.1126/science.1128134 · Cited by 1,913 · see citing works
Synaptic AMPA receptor plasticity and behavior
Kessels, H. W., & Malinow, R. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.015 · Cited by 993 · see citing works
Storage of spatial information by the maintenance mechanism of LTP
Pastalkova, E., Serrano, P., Pinkhasova, D., Wallace, E., Fenton, A. A., & Sacktor, T. C. (2006) · Science · doi:10.1126/science.1128657 · Cited by 848 · see citing works
Self-citationPostsynaptic receptor trafficking underlying a form of associative learning
Rumpel, S., LeDoux, J., Zador, A., & Malinow, R. (2005) · Science · doi:10.1126/science.1103944 · Cited by 775 · see citing works
Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts
Mumby, D. G., Gaskin, S., Glenn, M. J., Schramek, T. E., & Lehmann, H. (2002) · Learning & Memory · doi:10.1101/lm.41302 · Cited by 714 · see citing works
Man, H., Lin, J., Ju, W. H., Ahmadian, G., Liu, L., Becker, L. E., Sheng, M., & Wang, Y. T. (2000) · Neuron · doi:10.1016/s0896-6273(00)81067-3 · Cited by 698 · see citing works
Self-citationNSF Binding to GluR2 Regulates Synaptic Transmission
Nishimune, A., Isaac, J. T. R., Molnár, E., Noël, J., Nash, S. R., Tagaya, M., Collingridge, G. L., Nakanishi, S., & Henley, J. M. (1998) · Neuron · doi:10.1016/s0896-6273(00)80517-6 · Cited by 544 · see citing works
Role of the Basolateral Amygdala in the Storage of Fear Memories across the Adult Lifetime of Rats
Gale, G. D., Anagnostaras, S., Godsil, B. P., Mitchell, S., Nozawa, T., Sage, J. R., Wiltgen, B. J., & Fanselow, M. S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4100-03.2004 · Cited by 427 · see citing works
Protein kinase Mζ is necessary and sufficient for LTP maintenance
Ling, D. S. F., Benardo, L. S., Serrano, P. A., Blace, N., Kelly, M. T., Crary, J. F., & Sacktor, T. C. (2002) · Nature Neuroscience · doi:10.1038/nn829 · Cited by 419 · see citing works
Self-citationInteraction of the N-Ethylmaleimide–Sensitive Factor with AMPA Receptors
Song, I., Kamboj, S. K., Xia, J., Dong, H., Liao, D., & Huganir, R. L. (1998) · Neuron · doi:10.1016/s0896-6273(00)80548-6 · Cited by 398 · see citing works
Osten, P., Srivastava, S., Inman, G. J., Vilim, F. S., Khatri, L., Lee, L. M., States, B. A., Einheber, S., Milner, T. A., Hanson, P. I., et al. (1998) · Neuron · doi:10.1016/s0896-6273(00)80518-8 · Cited by 358 · 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
Self-citationAnterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions
Winocur, G. (1990) · Behavioural Brain Research · doi:10.1016/0166-4328(90)90012-4 · Cited by 352 · see citing works
Extracellular interactions between GluR2 and N-cadherin in spine regulation
Saglietti, L., Dequidt, C., Kamieniarz, K., Rousset, M.-C., Valnegri, P., Thoumine, O., Beretta, F., Fagni, L., Choquet, D., Sala, C., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.04.012 · Cited by 341 · see citing works
Experience Strengthening Transmission by Driving AMPA Receptors into Synapses
Takahashi, T., Svoboda, K., & Malinow, R. (2003) · Science · doi:10.1126/science.1079886 · Cited by 306 · see citing works
Noël, J., Ralph, G. S., Pickard, L., Williams, J., Molnár, E., Uney, J. B., Collingridge, G. L., & Henley, J. M. (1999) · Neuron · doi:10.1016/s0896-6273(00)80786-2 · Cited by 299 · see citing works
Ahmadian, G., Ju, W., Liu, L., Wyszynski, M., Lee, S. H., Dunah, A. W., Taghibiglou, C., Wang, Y., Lu, J., Wong, T. P., et al. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600126 · Cited by 296 · see citing works
Self-citationNucleus Accumbens Long-Term Depression and the Expression of Behavioral Sensitization
Brebner, K., Wong, T. P., Liu, L., Liu, Y., Campsall, P. A., Gray, S. L., Phelps, L., Phillips, A. G., & Wang, Y. T. (2005) · Science · doi:10.1126/science.1116894 · Cited by 289 · see citing works
Self-citationPKMζ Maintains Spatial, Instrumental, and Classically Conditioned Long-Term Memories
Serrano, P., Friedman, E., Kenney, J., Taubenfeld, S., Zimmerman, J. M., Hanna, J., Alberini, C., Kelley, A., Maren, S., Rudy, J., et al. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060318 · Cited by 273 · see citing works
Self-citationHuang, Y.-Y., Martin, K. C., & Kandel, E. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-17-06317.2000 · Cited by 269 · see citing works
Yao, Y., Kelly, M. T., Sajikumar, S., Serrano, P. A., Tian, D., Bergold, P. J., Frey, J. U., & Sacktor, T. C. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0223-08.2008 · Cited by 268 · see citing works
Self-citationSubunit Rules Governing the Sorting of Internalized AMPA Receptors in Hippocampal Neurons
Lee, S. H., Simonetta, A., & Sheng, M. (2004) · Neuron · doi:10.1016/j.neuron.2004.06.015 · Cited by 268 · see citing works
Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus
Xu, L., Anwyl, R., & Rowan, M. J. (1998) · Nature · doi:10.1038/29783 · Cited by 260 · see citing works
NSF ATPase and α-/β-SNAPs Disassemble the AMPA Receptor-PICK1 Complex
Hanley, J. G., Khatri, L., Hanson, P. I., & Ziff, E. B. (2002) · Neuron · doi:10.1016/s0896-6273(02)00638-4 · Cited by 197 · see citing works
Tyrosine phosphorylation and regulation of the AMPA receptor by SRC family tyrosine kinases
Hayashi, T., & Huganir, R. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0799-04.2004 · Cited by 177 · see citing works
Synaptic AMPA Receptor Exchange Maintains Bidirectional Plasticity
McCormack, S. G., Stornetta, R. L., & Zhu, J. (2006) · Neuron · doi:10.1016/j.neuron.2006.02.027 · Cited by 92 · see citing works
Hardt, O., Migues, P. V., Hastings, M., Wong, J., & Nader, K. (2010) · Hippocampus · doi:10.1002/hipo.20708 · Cited by 79 · see citing works
Self-citationYu, S. Y., Wu, D., Liu, L., Ge, Y., & Wang, Y. T. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05461.x · Cited by 72 · see citing works
Self-citationFeligioni, M., Holman, D., Haglerød, C., Davanger, S., & Henley, J. M. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04087.x · Cited by 43 · see citing works
Migues, P. V., Lehmann, I. T., Fluechter, L., Cammarota, M., Gurd, J. W., Sim, A. T. R., Dickson, P. W., & Rostas, J. A. P. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03876.x · Cited by 41 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Molecular mechanisms of fear learning and memory
Johansen, J. P., Cain, C. K., Ostroff, L. E., & LeDoux, J. E. (2011) · Cell · doi:10.1016/j.cell.2011.10.009 · Cited by 1,012 · see citing works
Long-term depression in the CNS
Collingridge, G. L., Peineau, S., Howland, J. G., & Wang, Y. T. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2867 · Cited by 926 · see citing works
Self-citationPharmacological brake-release of mRNA translation enhances cognitive memory
Sidrauski, C., Acosta‐Alvear, D., Khoutorsky, A., Vedantham, P., Hearn, B. R., Li, H., Gamache, K., Gallagher, C. M., Ang, K. K. H., Wilson, C. G. M., et al. (2013) · eLife · doi:10.7554/elife.00498 · Cited by 732 · see citing works
Self-citationThe synaptic plasticity and memory hypothesis: encoding, storage and persistence
Takeuchi, T., Duszkiewicz, A. J., & Morris, R. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0288 · Cited by 664 · see citing works
Mahan, A. L., & Ressler, K. J. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.06.007 · Cited by 616 · see citing works
How does PKMζ maintain long-term memory?
Sacktor, T. C. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn2949 · Cited by 431 · see citing works
Self-citationDecay 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
Self-citationAlleviating Neuropathic Pain Hypersensitivity by Inhibiting PKMζ in the Anterior Cingulate Cortex
Li, X., Ko, H., Chen, T., Descalzi, G., Koga, K., Wang, H., Kim, S. S., Shang, Y., Kwak, C., Park, S., et al. (2010) · Science · doi:10.1126/science.1191792 · Cited by 407 · see citing works
Long-term potentiation and long-term depression: a clinical perspective
Bliss, T. V. P., & Cooke, S. F. (2011) · Clinics · doi:10.1590/s1807-59322011001300002 · Cited by 333 · see citing works
The Biology of Forgetting—A Perspective
Davis, R. L., & Zhong, Y. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.039 · Cited by 324 · see citing works
The Persistence and Transience of Memory
Richards, B. A., & Frankland, P. W. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.037 · Cited by 304 · see citing works
Expression of NMDA receptor-dependent LTP in the hippocampus: bridging the divide
Bliss, T. V., & Collingridge, G. L. (2013) · Molecular Brain · doi:10.1186/1756-6606-6-5 · Cited by 305 · see citing works
Seeking a Spotless Mind: Extinction, Deconsolidation, and Erasure of Fear Memory
Maren, S. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.023 · Cited by 259 · see citing works
“Within the amygdala, for example, it has been shown that inhibition of PKMzeta with a pseudosubstrate of the kinase (zeta inhibitory peptide or ZIP) impairs the expression of consolidated fear memories (Kwapis et al., 2009; Migues et al., 2010; Serrano et al., 2008).”
BackgroundInfluentialPrkcz null mice show normal learning and memory
Lee, A. M., Kanter, B. R., Wang, D., Lim, J. P., Zou, M. E., Qiu, C., McMahon, T., Dadgar, J., Fischbach-Weiss, S., & Messing, R. O. (2013) · Nature · doi:10.1038/nature11803 · Cited by 259 · see citing works
AMPA receptor trafficking and the mechanisms underlying synaptic plasticity and cognitive aging
Henley, J. M., & Wilkinson, K. A. (2013) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2013.15.1/jhenley · Cited by 236 · 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
Update on Memory Systems and Processes
Nadel, L., & Hardt, O. M. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.169 · Cited by 216 · see citing works
Self-citationStress hormones and AMPA receptor trafficking in synaptic plasticity and memory
Krugers, H. J., Hoogenraad, C. C., & Groc, L. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2913 · Cited by 197 · see citing works
Protein kinase C pharmacology: refining the toolbox
Wu-Zhang, A. X., & Newton, A. C. (2013) · Biochemical Journal · doi:10.1042/bj20130220 · Cited by 195 · see citing works
Long-term potentiation decay and memory loss are mediated by AMPAR endocytosis
Dong, Z., Han, H., Li, H., Bai, Y., Wang, W., Tu, M., Yan, P., Zhou, L., He, W., Wu, X., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci77888 · Cited by 194 · see citing works
Self-citationRetrieval-specific endocytosis of GluA2-AMPARs underlies adaptive reconsolidation of contextual fear
Rao-Ruiz, P., Rotaru, D. C., van der Loo, R. J., Mansvelder, H. D., Stiedl, O., Smit, A. B., & Spijker, S. (2011) · Nature Neuroscience · doi:10.1038/nn.2907 · Cited by 192 · see citing works
The role of metaplasticity mechanisms in regulating memory destabilization and reconsolidation
Finnie, P. S. B., & Nader, K. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.03.008 · Cited by 189 · see citing works
Self-citationEnhancement of Consolidated Long-Term Memory by Overexpression of Protein Kinase Mζ in the Neocortex
Shema, R., Haramati, S., Ron, S., Hazvi, S., Chen, A., Sacktor, T. C., & Dudai, Y. (2011) · Science · doi:10.1126/science.1200215 · Cited by 173 · see citing works
Self-citationCompensation for PKMζ in long-term potentiation and spatial long-term memory in mutant mice
Tsokas, P., Hsieh, C., Yao, Y., Lesburguères, E., Wallace, E. J. C., Tcherepanov, A., Jothianandan, D., Hartley, B. R., Pan, L., Rivard, B., et al. (2016) · eLife · doi:10.7554/elife.14846 · Cited by 166 · see citing works
Self-citationChao, O. Y., de Souza Silva, M. A., Yang, Y.-M., & Huston, J. P. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.04.007 · Cited by 158 · see citing works
Routes, destinations and delays: recent advances in AMPA receptor trafficking
Henley, J. M., Barker, E. A., & Glebov, O. O. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.02.004 · Cited by 158 · see citing works
Migues, P. V., Liu, L., Archbold, G. E. B., Einarsson, E. Ö., Wong, J., Bonasia, K., Ko, S. H., Wang, Y. T., & Hardt, O. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.3333-15.2016 · Cited by 153 · see citing works
Self-citationNMDA and AMPA receptors dysregulation in Alzheimer's disease
Babaei, P. (2021) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2021.174310 · Cited by 149 · see citing works
Commonalities Between Pain and Memory Mechanisms and Their Meaning for Understanding Chronic Pain
Price, T. J., & Inyang, K. E. (2015) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2014.11.010 · Cited by 143 · see citing works
Engram neurons: Encoding, consolidation, retrieval, and forgetting of memory
Guskjolen, A. J., & Cembrowski, M. S. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02137-5 · Cited by 148 · see citing works
Adasme, T., Haeger, P. A., Paula-Lima, A. C., Espinoza, I., Casas-Alarcón, M. M., Carrasco, M. A., & Hidalgo, C. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013580108 · Cited by 135 · see citing works
Protein Kinase M Maintains Long-Term Sensitization and Long-Term Facilitation inAplysia
Cai, D., Pearce, K. C., Chen, S., & Glanzman, D. L. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4744-10.2011 · Cited by 131 · 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
Synaptotagmin-3 drives AMPA receptor endocytosis, depression of synapse strength, and forgetting
Awasthi, A., Ramachandran, B., Ahmed, S., Benito, E., Shinoda, Y., Nitzan, N., Heukamp, A. S., Rannio, S., Martens, H., Barth, J., et al. (2018) · Science · doi:10.1126/science.aav1483 · Cited by 133 · see citing works
Self-citationMEF2 negatively regulates learning-induced structural plasticity and memory formation
Cole, C. J., Mercaldo, V., Restivo, L., Yiu, A. P., Sekeres, M. J., Han, J., Vetere, G., Pekar, T., Ross, P. J., Neve, R. L., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3189 · Cited by 131 · see citing works
Learning and memory consolidation: linking molecular and behavioral data
Morgado-Bernal, I. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2010.12.056 · Cited by 121 · see citing works
Asiedu, M. N., Tillu, D. V., Melemedjian, O. K., Shy, A., Sanoja, R., Bodell, B., Ghosh, S., Porreca, F., & Price, T. J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6286-10.2011 · Cited by 122 · see citing works
A novel UCS memory retrieval-extinction procedure to inhibit relapse to drug seeking
Luo, Y., Xue, Y.-X., Liu, J., Shi, H., Jian, M., Han, Y., Zhu, W., Bao, Y., Wu, P., Ding, Z., et al. (2015) · Nature Communications · doi:10.1038/ncomms8675 · Cited by 115 · see citing works
Lopez, J., Gamache, K., Schneider, R. E., & Nader, K. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0735-14.2015 · Cited by 114 · see citing works
Self-citationHow to erase memory traces of pain and fear
Sandkühler, J., & Lee, J. L. C. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.03.004 · Cited by 106 · see citing works
The Pharmacology of Nociceptor Priming
Kandasamy, R., & Price, T. J. (2015) · Handbook of experimental pharmacology · doi:10.1007/978-3-662-46450-2_2 · Cited by 107 · see citing works
The Synaptic Theory of Memory: A Historical Survey and Reconciliation of Recent Opposition
Langille, J. J., & Brown, R. E. (2018) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2018.00052 · Cited by 109 · see citing works
Iñiguez, S. D., Aubry, A., Riggs, L. M., Alipio, J. B., Zanca, R. M., Flores-Ramirez, F. J., Hernandez, M. A., Nieto, S. J., Musheyev, D., & Serrano, P. A. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.07.001 · Cited by 105 · see citing works
Inhibition of PKMζ in Nucleus Accumbens Core Abolishes Long-Term Drug Reward Memory
Li, Y.-Q., Xue, Y.-X., He, Y., Li, F., Xue, L., Xu, C., Sacktor, T. C., Shaham, Y., & Lü, L. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5884-10.2011 · Cited by 104 · see citing works
Self-citationPKCλ is critical in AMPA receptor phosphorylation and synaptic incorporation during LTP
Ren, S., Yan, J., Zhang, X., Bu, Y.-F., Pan, W.-W., Yao, W., Tian, T., & Lü, W. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.60 · Cited by 107 · see citing works
Memory maintenance by PKMζ — an evolutionary perspective
Sacktor, T. C. (2012) · Molecular Brain · doi:10.1186/1756-6606-5-31 · Cited by 99 · see citing works
Self-citationHaubrich, J., & Nader, K. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_463 · Cited by 100 · see citing works
Self-citationSun, M., & Alkon, D. L. (2014) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-420170-5.00002-7 · Cited by 92 · see citing works
Wnt Signaling in Amygdala-Dependent Learning and Memory
Maguschak, K. A., & Ressler, K. J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3248-11.2011 · Cited by 88 · see citing works
Interplay of Amygdala and Cingulate Plasticity in Emotional Fear
Toyoda, H., Li, X., Wu, L., Zhao, M., Descalzi, G., Chen, T., Koga, K., & Zhuo, M. (2011) · Neural Plasticity · doi:10.1155/2011/813749 · Cited by 85 · see citing works
Aleksandrova, L. R., Wang, Y. T., & Phillips, A. G. (2020) · Molecular Brain · doi:10.1186/s13041-020-00627-z · Cited by 85 · see citing works
Self-citationMechanisms of memory enhancement
Stern, S. A., & Alberini, C. M. (2012) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1196 · Cited by 86 · see citing works
Hardt, O. M., Nader, K., & Wang, Y.-T. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0141 · Cited by 82 · see citing works
Self-citationAutophagy Enhances Memory Erasure through Synaptic Destabilization
Shehata, M. H., Abdou, K., Choko, K., Matsuo, M., Nishizono, H., & Inokuchi, K. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.3505-17.2018 · Cited by 83 · see citing works
Sebastian, V., Estil, J. B., Chen, D., Schrott, L. M., & Serrano, P. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0079077 · Cited by 80 · see citing works
Odaira, T., Nakagawasai, O., Takahashi, K., Nemoto, W., Sakuma, W., Lin, J.-R., & Tan–No, K. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.03.026 · Cited by 80 · see citing works
Krugers, H. J., Karst, H., & Joëls, M. (2012) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2012.00015 · Cited by 77 · see citing works
TrkB and Protein Kinase M ζ Regulate Synaptic Localization of PSD-95 in Developing Cortex
Yoshii, A., Murata, Y., Kim, J., Zhang, C., Shokat, K. M., & Constantine‐Paton, M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2190-11.2011 · Cited by 76 · see citing works
Cooke, S. F., & Bear, M. F. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.09.006 · Cited by 74 · see citing works
Sachser, R. M., Santana, F., Crestani, A. P., Lunardi, P. S., Pedraza, L. K., Quillfeldt, J. A., Hardt, O. M., & Alvares, L. D. O. (2016) · Scientific Reports · doi:10.1038/srep22771 · Cited by 75 · see citing works
Self-citationHolehonnur, R., Phensy, A. J., Kim, L. J., Milivojevic, M., Vuong, D., Daison, D. K., Alex, S., Tiner, M., Jones, L. E., Kroener, S., et al. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.1743-16.2016 · Cited by 74 · see citing works
Molecular signatures and mechanisms of long-lasting memory consolidation and storage
Katche, C., Cammarota, M., & Medina, J. H. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.06.018 · Cited by 74 · see citing works
Initial memory consolidation and the synaptic tagging and capture hypothesis
Okuda, K., Højgaard, K., Privitera, L., Bayraktar, G., & Takeuchi, T. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14902 · Cited by 71 · see citing works
BDNF Facilitates L-LTP Maintenance in the Absence of Protein Synthesis through PKMζ
Mei, F., Nagappan, G., Ke, Y., Sacktor, T. C., & Lu, B. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021568 · Cited by 73 · see citing works
Self-citationKIBRA (KIdney/BRAin protein) regulates learning and memory and stabilizes Protein kinase Mζ
Vogt-Eisele, A. K., Krüger, C., Duning, K., Weber, D., Spoelgen, R., Pitzer, C., Plaas, C., Eisenhardt, G., Meyer, A., Vogt, G., et al. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12480 · Cited by 71 · see citing works
Kukushkin, N. V., & Carew, T. J. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.029 · Cited by 68 · see citing works
Haubrich, J., Bernabo, M., & Nader, K. (2020) · eLife · doi:10.7554/elife.57010 · Cited by 68 · see citing works
Self-citationHe, Y., Xue, Y.-X., Wang, J., Fang, Q., Liu, J., Xue, L., & Lü, L. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.63 · Cited by 67 · see citing works
Hara, Y., Punsoni, M., Yuk, F., Park, C. S., Janssen, W. G. M., Rapp, P. R., & Morrison, J. H. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0605-12.2012 · Cited by 66 · see citing works
Li, Q., Rothkegel, M., Xiao, Z., Abraham, W. C., Körte, M., & Sajikumar, S. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs315 · Cited by 66 · see citing works
Memory as a new therapeutic target
Nader, K., Hardt, O. M., & Lanius, R. A. (2013) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2013.15.4/knader · Cited by 64 · see citing works
Self-citationPersistent increased PKMζ in long-term and remote spatial memory
Hsieh, C., Tsokas, P., Serrano, P. A., Hernandez, A. I., Tian, D., Cottrell, J. E., Shouval, H. Z., Fenton, A. A., & Sacktor, T. C. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.07.008 · Cited by 61 · see citing works
Self-citationThe genetics of PKMζ and memory maintenance
Sacktor, T. C., & Hell, J. W. (2017) · Science Signaling · doi:10.1126/scisignal.aao2327 · Cited by 59 · see citing works
Self-citationSmolen, P. D., Baxter, D. A., & Byrne, J. H. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002620 · Cited by 59 · see citing works
Temporary disruption of fear-potentiated startle following PKMζ inhibition in the amygdala
Parsons, R. G., & Davis, M. (2011) · Nature Neuroscience · doi:10.1038/nn.2745 · Cited by 57 · see citing works
Feld, G. B., Lange, T., Gais, S., & Jan Born, A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.179 · Cited by 55 · see citing works
In search of a recognition memory engram
Brown, M. W., & Banks, P. J. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.09.016 · Cited by 56 · see citing works
Cellular Pharmacology of Protein Kinase Mζ (PKMζ) Contrasts with Its in Vitro Profile
Wu-Zhang, A. X., Schramm, C. L., Nabavi, S., Malinow, R., & Newton, A. C. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.357244 · Cited by 54 · see citing works
Smolen, P., Baxter, D. A., & Byrne, J. H. (2019) · Learning & Memory · doi:10.1101/lm.049395.119 · Cited by 53 · see citing works
Yao, Y., Shao, C., Jothianandan, D., Tcherepanov, A., Shouval, H. Z., & Sacktor, T. C. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.07.018 · Cited by 53 · see citing works
Self-citationRapid synaptic potentiation within the anterior cingulate cortex mediates trace fear learning
Descalzi, G., Li, X., Chen, T., Mercaldo, V., Koga, K., & Zhuo, M. (2012) · Molecular Brain · doi:10.1186/1756-6606-5-6 · Cited by 53 · see citing works
Sachser, R. M., Haubrich, J., Lunardi, P. S., & Alvares, L. D. O. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.07.015 · Cited by 52 · see citing works
Memory suppressor genes: Modulating acquisition, consolidation, and forgetting
Noyes, N. C., Phan, A., & Davis, R. L. (2021) · Neuron · doi:10.1016/j.neuron.2021.08.001 · Cited by 55 · see citing works
Remapping revisited: how the hippocampus represents different spaces
Fenton, A. A. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00817-x · Cited by 56 · see citing works
Wang, S., Sheng, T., Ren, S., Tian, T., & Lü, W. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.07.030 · Cited by 52 · see citing works
A Putative Biochemical Engram of Long-Term Memory
Li, L., Sanchez, C. P., Slaughter, B. D., Zhao, Y., Khan, M. R., Unruh, J. R., RUBINSTEIN, B. Y., & Si, K. (2016) · Current Biology · doi:10.1016/j.cub.2016.09.054 · Cited by 50 · see citing works
King, T. E., Qu, C., Okun, A., Melemedjian, O. K., Mandell, E. K., Maskaykina, I. Y., Navratilova, E., Dussor, G. O., Ghosh, S., Price, T. J., et al. (2012) · Pain · doi:10.1016/j.pain.2012.03.006 · Cited by 49 · see citing works
Molecular Mechanisms of Stress-Induced Increases in Fear Memory Consolidation within the Amygdala
Aubry, A., Serrano, P. A., & Burghardt, N. S. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00191 · Cited by 47 · see citing works
Hu, J., Adler, K., Farah, C. A., Hastings, M. H., Sossin, W. S., & Schacher, S. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2805-16.2017 · Cited by 44 · see citing works
Does PKM(zeta) maintain memory?
Kwapis, J. L., & Helmstetter, F. J. (2013) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2013.09.005 · Cited by 47 · see citing works
PKM and the maintenance of memory
Glanzman, D. L. (2013) · F1000 Biology Reports · doi:10.3410/b5-4 · Cited by 46 · see citing works
Haubrich, J., Bernabo, M., Baker, A. G., & Nader, K. (2020) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-091319-024636 · Cited by 44 · see citing works
Self-citationPauli, W. M., Clark, A. D., Guenther, H. J., O’Reilly, R. C., & Rudy, J. W. (2012) · Learning & Memory · doi:10.1101/lm.025148.111 · Cited by 44 · see citing works
FXR1P Limits Long-Term Memory, Long-Lasting Synaptic Potentiation, and De Novo GluA2 Translation
Cook, D., Nuro, E., Jones, E. V., Altimimi, H. F., Farmer, W. T., Gandin, V., Hanna, E., Zong, R.-T., Barbon, A., Nelson, D. L., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.10.028 · Cited by 43 · see citing works
Connor, S. A., Wang, Y. T., & Nguyen, P. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.209379 · Cited by 42 · see citing works
Self-citationVillers, A., Godaux, E., & Ris, L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040823 · Cited by 42 · see citing works
Cabrera‐Pastor, A., Hernández‐Rabaza, V., Taoro‐González, L., Balzano, T., Llansola, M., & Felipo, V. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.05.011 · Cited by 42 · see citing works
What does LTP tell us about the roles of CaMKII and PKMζ in memory?
Sacktor, T. C., & Fenton, A. A. (2018) · Molecular Brain · doi:10.1186/s13041-018-0420-5 · Cited by 43 · see citing works
Self-citationAtypical PKCs in memory maintenance: the roles of feedback and redundancyPreprint
Jalil, S., Sacktor, T. C., & Shouval, H. Z. (2015) · Learning & Memory · doi:10.1101/lm.038844.115 · Cited by 42 · see citing works
Self-citationRegulation of excitatory synapses and fearful memories by stress hormones
Krugers, H. J. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00062 · Cited by 40 · see citing works
- Authors
- Migues, P. V., Hardt, O., Wu, D. C., Gamache, K., Sacktor, T. C., Wang, Y. T., & Nader, K.
- Affiliations
- McGill University (CA)
- University of British Columbia (CA)
- SUNY Downstate Health Sciences University (US)
- Corresponding author
- Migues, Paola Virginia
- Venue
- Nature Neuroscience
- Published
- 2010-04-11
- Volume
- 13
- Issue
- 5
- Pages
- 630-634
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W1974491267
- Cited by
- 283
- References
- 31
- Citations by year
- 2026: 7 · 2025: 10 · 2024: 8 · 2023: 10 · 2022: 8 · 2021: 10 · 2020: 16 · 2019: 15 · 2018: 22 · 2017: 14 · 2016: 23 · 2015: 17 · 2014: 16 · 2013: 33 · 2012: 26
- FWCI
- 20.76
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research
- National Institute of Mental Health (MH 57068, R01MH53576, R01MH053576)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- PKMzeta, GluR2, AMPA receptor trafficking, long-term memory, fear memory, amygdala, hippocampus, long-term potentiation, object recognition memory, memory maintenance
- MeSH terms
- Analysis of Variance, Animals, Avidin, Behavior, Animal, Cerebral Cortex, Conditioning, Psychological, Electroshock, Fear, Hippocampus, Male, Memory, Synaptic Transmission, Peptides, Protein Kinase C, Subcellular Fractions, Rats, Sprague-Dawley, Long-Term Potentiation, Receptors, AMPA, Patch-Clamp Techniques, Statistics, Nonparametric, Biotinylation, Rats, Long-Evans, Protein Transport, Recognition, Psychology, Freezing Reaction, Cataleptic, Rats
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