Synaptic Tagging and Capture: Functional Implications and Molecular Mechanisms

• Abel T, Nguyen PV (2008) Regulation of hippocampus-dependent memory by cyclic AMP-dependent protein kinase. Prog Brain Res 169:97. https://doi.org/10.1016/S0079-6123(07)00006-4

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Alberts B, Johnson A, Lewis J, Morgan D, Raff M, Roberts K, Walter P (2017) Molecular biology of the cell. Garland Science. https://doi.org/10.1201/9781315735368

  Book  Google Scholar 

• Andersen P (2008) Long‐lasting facilitation of synaptic transmission. In: Ciba foundation symposium 58‐functions of the septo‐hippocampal system, vol 58. Wiley, pp 87–108. https://doi.org/10.1002/9780470720394.ch6

  Chapter  Google Scholar 

• Asrar S, Zhou Z, Ren W, Jia Z (2009) Ca2+ permeable AMPA receptor induced long-term potentiation requires PI3/MAP kinases but not Ca/CaM-dependent kinase II. PLoS One 4(2):e4339. https://doi.org/10.1371/journal.pone.0004339

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Ballarini F, Moncada D, Martinez MC, Alen N, Viola H (2009) Behavioral tagging is a general mechanism of long-term memory formation. Proc Natl Acad Sci 106(34):14599–14604. https://doi.org/10.1073/pnas.0907078106

  Article  PubMed  PubMed Central  Google Scholar 

• Ballarini F, Martínez MC, Díaz Perez M, Moncada D, Viola H (2013) Memory in elementary school children is improved by an unrelated novel experience. PLoS One 8(6):e66875. https://doi.org/10.1371/journal.pone.0066875

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Barco A, Patterson S, Alarcon JM, Gromova P, Mata-Roig M, Morozov A, Kandel ER (2005) Gene expression profiling of facilitated L-LTP in VP16-CREB mice reveals that BDNF is critical for the maintenance of LTP and its synaptic capture. Neuron 48(1):123–137. https://doi.org/10.1016/j.neuron.2005.09.005

  Article  CAS  PubMed  Google Scholar 

• Barrett AB, Billings GO, Morris RGM, van Rossum MCW (2009) State based model of long-term potentiation and synaptic tagging and capture. PLoS Comput Biol 5(1):e1000259. https://doi.org/10.1371/journal.pcbi.1000259

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Bell M, Bartol T, Sejnowski T, Rangamani P (2019) Dendritic spine geometry and spine apparatus organization govern the spatiotemporal dynamics of calcium. J Gen Physiol 151(8):1017–1034. https://doi.org/10.1085/jgp.201812261

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Bennett MK, Erondu NE, Kennedy MB (1983) Purification and characterization of a calmodulin-dependent protein kinase that is highly concentrated in brain. J Biol Chem 258(20):12735–12744. https://doi.org/10.1016/S0021-9258(17)44239-6

  Article  CAS  PubMed  Google Scholar 

• Benovic JL, Bouvier M, Caron MG, Lefkowitz RJ (1988) Regulation of adenylyl cyclase-coupled beta-adrenergic receptors. Annu Rev Cell Biol 4(1):405–428. https://doi.org/10.1146/annurev.cb.04.110188.002201

  Article  CAS  PubMed  Google Scholar 

• Bito H, Nonaka M, Kawashima T, Yagishita-Kyo N, Takemoto-Kimura S, Okuno H (2011) Deciphering the signaling from the synapse to the nucleus. Neurosci Res 71:e13. https://doi.org/10.1016/j.neures.2011.07.050

  Article  Google Scholar 

• Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361(6407):31–39. https://doi.org/10.1038/361031a0

  Article  CAS  PubMed  Google Scholar 

• Bliss TVP, Lømo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232(2):331–356. https://doi.org/10.1113/jphysiol.1973.sp010273

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Bliss TVP, Collingridge GL, Cooke S, Georgiou J, Morris RGM (2023) Chapter 10 long term potentiation. In: Morris et al (eds) The hippocampus book, 2nd edn. Oxford University Press, New York

  Google Scholar 

• Blitzer RD, Connor JH, Brown GP, Wong T, Shenolikar S, Iyengar R, Landau EM (1998) Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science 280(5371):1940–1943. https://doi.org/10.1126/science.280.5371.1940

  Article  CAS  PubMed  Google Scholar 

• Bloodgood BL, Sabatini BL (2005) Neuronal activity regulates diffusion across the neck of dendritic spines. Science 310(5749):866–869. https://doi.org/10.1126/science.1114816

  Article  CAS  PubMed  Google Scholar 

• Bosch M, Castro J, Saneyoshi T, Matsuno H, Sur M, Hayashi Y (2014) Structural and molecular remodeling of dendritic spine substructures during long-term potentiation. Neuron 82(2):444–459. https://doi.org/10.1016/j.neuron.2014.03.021

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Brakeman PR, Lanahan AA, O’Brien R, Roche K, Barnes CA, Huganir RL, Worley PF (1997) Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 386(6622):284–288. https://doi.org/10.1038/386284a0

  Article  CAS  PubMed  Google Scholar 

• Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, Pai B, Panja D, Schubert M, Soule J, Tiron A, Wibrand K (2010) The arc of synaptic memory. Exp Brain Res 200(2):125–140. https://doi.org/10.1007/s00221-009-1959-2

  Article  PubMed  Google Scholar 

• Buard I, Coultrap SJ, Freund RK, Lee Y-S, Dell’Acqua ML, Silva AJ, Bayer KU (2010) CaMKII “autonomy” is required for initiating but not for maintaining neuronal long-term information storage. J Neurosci 30(24):8214–8220. https://doi.org/10.1523/JNEUROSCI.1469-10.2010

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Canossa M, Griesbeck O, Berninger B, Campana G, Kolbeck R, Thoenen H (1997) Neurotrophin release by neurotrophins: implications for activity-dependent neuronal plasticity. Proc Natl Acad Sci 94(24):13279–13286. https://doi.org/10.1073/pnas.94.24.13279

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Ch’Ng TH, DeSalvo M, Lin P, Vashisht A, Wohlschlegel JA, Martin KC (2015) Cell biological mechanisms of activity-dependent synapse to nucleus translocation of CRTC1 in neurons. Front Mol Neurosci 8:48. https://doi.org/10.3389/fnmol.2015.00048

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Chang J-Y, Parra-Bueno P, Laviv T, Szatmari EM, Lee S-JR, Yasuda R (2017) CaMKII autophosphorylation is necessary for optimal integration of Ca 2+ signals during LTP induction, but not maintenance. Neuron 94(4):800–808.e4. https://doi.org/10.1016/j.neuron.2017.04.041

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Chen X, Ye H, Kuruvilla R, Ramanan N, Scangos KW, Zhang C, Johnson NM, England PM, Shokat KM, Ginty DD (2005) A chemical-genetic approach to studying neurotrophin signaling. Neuron 46(1):13–21. https://doi.org/10.1016/j.neuron.2005.03.009

  Article  CAS  PubMed  Google Scholar 

• Choquet D, Hosy E (2020) AMPA receptor nanoscale dynamic organization and synaptic plasticities. Curr Opin Neurobiol 63:137–145. https://doi.org/10.1016/j.conb.2020.04.003

  Article  CAS  PubMed  Google Scholar 

• Chowdhury S, Shepherd JD, Okuno H, Lyford G, Petralia RS, Plath N, Kuhl D, Huganir RL, Worley PF (2006) Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52(3):445–459. https://doi.org/10.1016/j.neuron.2006.08.033

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Citri A, Malenka RC (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33(1):18–41. https://doi.org/10.1038/sj.npp.1301559

  Article  PubMed  Google Scholar 

• Clifton NE, Cameron D, Trent S, Sykes LH, Thomas KL, Hall J (2017) Hippocampal regulation of postsynaptic density homer1 by associative learning. Neural Plast 2017:1–11. https://doi.org/10.1155/2017/5959182

  Article  CAS  Google Scholar 

• Clifton NE, Trent S, Thomas KL, Hall J (2019) Regulation and function of activity-dependent Homer in synaptic plasticity. Complex Psychiatry 5(3):147–161. https://doi.org/10.1159/000500267

  Article  CAS  Google Scholar 

• Clopath C, Ziegler L, Vasilaki E, Büsing L, Gerstner W (2008) Tag-trigger-consolidation: A model of early and late long-term-potentiation and depression. PLoS Comput Biol 4(12):e1000248. https://doi.org/10.1371/journal.pcbi.1000248

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Colbran RJ, Smith MK, Schworer CM, Fong YL, Soderling TR (1989) Regulatory domain of calcium/calmodulin-dependent protein kinase II. J Biol Chem 264(9):4800–4804. https://doi.org/10.1016/S0021-9258(18)83661-4

  Article  CAS  PubMed  Google Scholar 

• DaSilva LLP, Wall MJP, de Almeida L, Wauters SC, Januário YC, Müller J, Corrêa SAL (2016) Activity-regulated cytoskeleton-associated protein controls AMPAR endocytosis through a direct interaction with clathrin-adaptor protein 2. Eneuro 3(3):15. https://doi.org/10.1523/ENEURO.0144-15.2016

  Article  Google Scholar 

• Dillon C, Goda Y (2005) The actin cytoskeleton: integrating form and function at the synapse. Annu Rev Neurosci 28(1):25–55. https://doi.org/10.1146/annurev.neuro.28.061604.135757

  Article  CAS  PubMed  Google Scholar 

• Ding Y, Wang Y, Cao L (2022) A simplified plasticity model based on synaptic tagging and capture theory: simplified STC. Front Comput Neurosci 15:23. https://doi.org/10.3389/fncom.2021.798418

  Article  Google Scholar 

• Dittmer PJ, Dell’Acqua ML, Sather WA (2019) Synaptic crosstalk conferred by a zone of differentially regulated Ca 2+ signaling in the dendritic shaft adjoining a potentiated spine. Proc Natl Acad Sci 116(27):13611–13620. https://doi.org/10.1073/pnas.1902461116

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55(1):51–86. https://doi.org/10.1146/annurev.psych.55.090902.142050

  Article  PubMed  Google Scholar 

• Dudai Y, Morris RGM (2000) To consolidate or not to consolidate: what are the questions? In: Brain, perception, memory: advances in cognitive neuroscience. Oxford University Press, Oxford, pp 149–162. https://doi.org/10.1093/acprof:oso/9780198524823.003.0011

  Chapter  Google Scholar 

• Dudek SM, Bear MF (1995) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci 89(10):4363–4367. https://doi.org/10.1142/9789812795885_0013

  Article  Google Scholar 

• Dunsmoor JE, Murty VP, Davachi L, Phelps EA (2015) Emotional learning selectively and retroactively strengthens memories for related events. Nature 520(7547):345–348. https://doi.org/10.1038/nature14106

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Dunsmoor JE, Murty VP, Clewett D, Phelps EA, Davachi L (2022) Tag and capture: how salient experiences target and rescue nearby events in memory. Trends Cogn Sci 26(9):782–795. https://doi.org/10.1016/j.tics.2022.06.009

  Article  PubMed  PubMed Central  Google Scholar 

• Duszkiewicz AJ, McNamara CG, Takeuchi T, Genzel L (2019) Novelty and dopaminergic modulation of memory persistence: A tale of two systems. Trends Neurosci 42(2):102–114. https://doi.org/10.1016/j.tins.2018.10.002

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Fonseca R (2012) Activity-dependent actin dynamics are required for the maintenance of long-term plasticity and for synaptic capture. Eur J Neurosci 35(2):195–206. https://doi.org/10.1111/j.1460-9568.2011.07955.x

  Article  PubMed  Google Scholar 

• Fonseca R, Vabulas RM, Hartl FU, Bonhoeffer T, Nägerl UV (2006) A balance of protein synthesis and proteasome-dependent degradation determines the maintenance of LTP. Neuron 52(2):239–245. https://doi.org/10.1016/j.neuron.2006.08.015

  Article  CAS  PubMed  Google Scholar 

• Frey U, Morris RGM (1997) Synaptic tagging and long-term potentiation. Nature 385(6616):533–536. https://doi.org/10.1038/385533a0

  Article  CAS  PubMed  Google Scholar 

• Frey U, Morris RGM (1998a) Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37(4–5):545–552. https://doi.org/10.1016/S0028-3908(98)00040-9

  Article  CAS  PubMed  Google Scholar 

• Frey U, Morris RGM (1998b) Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci 21(5):181–188. https://doi.org/10.1016/S0166-2236(97)01189-2

  Article  CAS  PubMed  Google Scholar 

• Frey U, Matthies H, Reymann KG, Matthies H (1991) The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro. Neurosci Lett 129(1):111–114. https://doi.org/10.1016/0304-3940(91)90732-9

  Article  CAS  PubMed  Google Scholar 

• Frey U, Huang Y-Y, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260(5114):1661–1664. https://doi.org/10.1126/science.8389057

  Article  CAS  PubMed  Google Scholar 

• Gonzalez A, Moya-Alvarado G, Gonzalez-Billaut C, Bronfman FC (2016) Cellular and molecular mechanisms regulating neuronal growth by brain-derived neurotrophic factor. Cytoskeleton 73(10):612–628. https://doi.org/10.1002/cm.21312

  Article  CAS  PubMed  Google Scholar 

• Govindarajan A, Kelleher RJ, Tonegawa S (2006) A clustered plasticity model of long-term memory engrams. Nat Rev Neurosci 7(7):575–583. https://doi.org/10.1038/nrn1937

  Article  CAS  PubMed  Google Scholar 

• Govindarajan A, Israely I, Huang S-Y, Tonegawa S (2011) The dendritic branch is the preferred integrative unit for protein synthesis-dependent LTP. Neuron 69(1):132–146. https://doi.org/10.1016/j.neuron.2010.12.008

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Guzowski JF, McNaughton BL, Barnes CA, Worley PF (1999) Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2(12):1120–1124. https://doi.org/10.1038/16046

  Article  CAS  PubMed  Google Scholar 

• Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279(5350):509–514. https://doi.org/10.1126/science.279.5350.509

  Article  CAS  PubMed  Google Scholar 

• Hao L, Yang Z, Lei J (2018) Underlying mechanisms of cooperativity, input specificity, and associativity of long-term potentiation through a positive feedback of local protein synthesis. Front Comput Neurosci 12. https://doi.org/10.3389/fncom.2018.00025

• Harvey CD, Svoboda K (2007) Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 450(7173):1195–1200. https://doi.org/10.1038/nature06416

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Harward SC, Hedrick NG, Hall CE, Parra-Bueno P, Milner TA, Pan E, Laviv T, Hempstead BL, Yasuda R, McNamara JO (2016) Autocrine BDNF–TrkB signalling within a single dendritic spine. Nature 538(7623):99–103. https://doi.org/10.1038/nature19766

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Häusser M (2021) Optogenetics – the might of light. N Engl J Med 385(17):1623–1626. https://doi.org/10.1056/NEJMcibr2111915

  Article  PubMed  Google Scholar 

• Hayashi MK, Ames HM, Hayashi Y (2006) Tetrameric hub structure of postsynaptic scaffolding protein Homer. J Neurosci 26(33):8492–8501. https://doi.org/10.1523/JNEUROSCI.2731-06.2006

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Hebb DO (2005) The organization of behavior: a neuropsychological theory. Psychology Press, London

  Book  Google Scholar 

• Hedrick NG, Harward SC, Hall CE, Murakoshi H, McNamara JO, Yasuda R (2016) Rho GTPase complementation underlies BDNF-dependent homo- and heterosynaptic plasticity. Nature 538(7623):104–108. https://doi.org/10.1038/nature19784

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Holt CE, Schuman EM (2013) The central dogma decentralized: new perspectives on RNA function and local translation in neurons. Neuron 80(3):648–657

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Huang T, McDonough CB, Abel T (2006) Compartmentalized PKA signaling events are required for synaptic tagging and capture during hippocampal late-phase long-term potentiation. Eur J Cell Biol 85(7):635–642. https://doi.org/10.1016/j.ejcb.2006.02.005

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Ikeda A, Okuno S, Fujisawa H (1991) Studies on the generation of Ca2+/calmodulin-independent activity of calmodulin-dependent protein kinase II by autophosphorylation. Autothiophosphorylation of the enzyme. J Biol Chem 266(18):11582–11588. https://doi.org/10.1016/S0021-9258(18)98996-9

  Article  CAS  PubMed  Google Scholar 

• Inoue N, Nakao H, Migishima R, Hino T, Matsui M, Hayashi F, Nakao K, Manabe T, Aiba A, Inokuchi K (2009) Requirement of the immediate early gene vesl-1S/homer-1a for fear memory formation. Mol Brain 2(1):7. https://doi.org/10.1186/1756-6606-2-7

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Ishikawa Y, Horii Y, Tamura H, Shiosaka S (2008) Neuropsin (KLK8)-dependent and -independent synaptic tagging in the Schaffer-collateral pathway of mouse hippocampus. J Neurosci 28(4): 843–849. https://doi.org/10.1523/JNEUROSCI.4397-07.2008

• Jedlicka P, Vlachos A, Schwarzacher SW, Deller T (2008) A role for the spine apparatus in LTP and spatial learning. Behav Brain Res 192(1):12–19. https://doi.org/10.1016/j.bbr.2008.02.033

  Article  PubMed  Google Scholar 

• Jędrzejewska-Szmek J, Blackwell KT (2019) From membrane receptors to protein synthesis and actin cytoskeleton: mechanisms underlying long lasting forms of synaptic plasticity. Semin Cell Dev Biol 95:120–129. https://doi.org/10.1016/j.semcdb.2019.01.006

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Ji Y, Pang PT, Feng L, Lu B (2005) Cyclic AMP controls BDNF-induced TrkB phosphorylation and dendritic spine formation in mature hippocampal neurons. Nat Neurosci 8(2):164–172. https://doi.org/10.1038/nn1381

  Article  CAS  PubMed  Google Scholar 

• Kandel ER (2012) The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Mol Brain 5(1):14. https://doi.org/10.1186/1756-6606-5-14

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Kastellakis G, Cai DJ, Mednick SC, Silva AJ, Poirazi P (2015) Synaptic clustering within dendrites: an emerging theory of memory formation. Prog Neurobiol 126:19–35. https://doi.org/10.1016/j.pneurobio.2014.12.002

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Kastellakis G, Silva AJ, Poirazi P (2016) Linking memories across time via neuronal and dendritic overlaps in model neurons with active dendrites. Cell Rep 17(6):1491–1504. https://doi.org/10.1016/j.celrep.2016.10.015

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Kato A, Ozawa F, Saitoh Y, Hirai K, Inokuchi K (1997) Vesl, a gene encoding VASP/Ena family related protein, is upregulated during seizure, long-term potentiation and synaptogenesis 1. FEBS Lett 412(1):183–189. https://doi.org/10.1016/S0014-5793(97)00775-8

  Article  CAS  PubMed  Google Scholar 

• Kempadoo KA, Mosharov EV, Choi SJ, Sulzer D, Kandel ER (2016) Dopamine release from the locus coeruleus to the dorsal hippocampus promotes spatial learning and memory. Proc Natl Acad Sci 113(51):14835–14840. https://doi.org/10.1073/pnas.1616515114

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Korobova F, Svitkina T (2010) Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol Biol Cell 21(1):165–176. https://doi.org/10.1091/mbc.e09-07-0596

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Kyrke-Smith M, Volk LJ, Cooke SF, Bear MF, Huganir RL, Shepherd JD (2021) The immediate early gene arc is not required for hippocampal long-term potentiation. J Neurosci 41(19):4202–4211. https://doi.org/10.1523/JNEUROSCI.0008-20.2021

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Leal G, Afonso PM, Salazar IL, Duarte CB (2015) Regulation of hippocampal synaptic plasticity by BDNF. Brain Res 1621:82–101. https://doi.org/10.1016/j.brainres.2014.10.019

  Article  CAS  PubMed  Google Scholar 

• LeBlancq MJ, McKinney TL, Dickson CT (2016) ZIP it: neural silencing is an additional effect of the PKM-zeta inhibitor zeta-inhibitory peptide. J Neurosci 36(23):6193–6198. https://doi.org/10.1523/JNEUROSCI.4563-14.2016

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Lee AM, Kanter BR, Wang D, Lim JP, Zou ME, Qiu C, McMahon T, Dadgar J, Fischbach-Weiss SC, Messing RO (2013) Prkcz null mice show normal learning and memory. Nature 493(7432):416–419

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Lehr AB, Luboeinski J, Tetzlaff C (2022) Neuromodulator-dependent synaptic tagging and capture retroactively controls neural coding in spiking neural networks. Sci Rep 12(1):17772

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Lemon N, Manahan-Vaughan D (2006) Dopamine D1/D5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. J Neurosci 26(29):7723–7729. https://doi.org/10.1523/JNEUROSCI.1454-06.2006

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Ling DSF, Benardo LS, Sacktor TC (2006) Protein kinase Mζ enhances excitatory synaptic transmission by increasing the number of active postsynaptic AMPA receptors. Hippocampus 16(5):443–452. https://doi.org/10.1002/hipo.20171

  Article  CAS  PubMed  Google Scholar 

• Lisman JE, Grace AA (2005) The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46(5):703–713. https://doi.org/10.1016/j.neuron.2005.05.002

  Article  CAS  PubMed  Google Scholar 

• Lu J, Zuo Y (2017) Clustered structural and functional plasticity of dendritic spines. Brain Res Bull 129:18–22. https://doi.org/10.1016/j.brainresbull.2016.09.008

  Article  PubMed  Google Scholar 

• Lu Y, Ji Y, Ganesan S, Schloesser R, Martinowich K, Sun M, Mei F, Chao MV, Lu B (2011) TrkB as a potential synaptic and behavioral tag. J Neurosci 31(33):11762–11771

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Luboeinski J, Tetzlaff C (2021) Memory consolidation and improvement by synaptic tagging and capture in recurrent neural networks. Commun Biol 4(1):275

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Lüscher C, Huber KM (2010) Group 1 mGluR-dependent synaptic long-term depression: mechanisms and implications for circuitry and disease. Neuron 65(4):445–459. https://doi.org/10.1016/j.neuron.2010.01.016

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Luscher C, Malenka RC (2012) NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harb Perspect Biol 4(6):a005710–a005710. https://doi.org/10.1101/cshperspect.a005710

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Magó Á, Weber JP, Ujfalussy BB, Makara JK (2020) Synaptic plasticity depends on the Fine-scale input pattern in thin dendrites of CA1 pyramidal neurons. J Neurosci 40(13):2593–2605. https://doi.org/10.1523/JNEUROSCI.2071-19.2020

  Article  PubMed  PubMed Central  Google Scholar 

• Malenka RC, Bear MF (2004) LTP and LTD. Neuron 44(1):5–21

  Article  CAS  PubMed  Google Scholar 

• Marr D (1971) Simple memory: A theory for archicortex. Philos Trans R Soc Lond 262:23–81

  CAS  Google Scholar 

• Martin KC, Casadio A, Zhu HEY, Rose JC, Chen M, Bailey CH, Kandel ER (1997) Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: A function for local protein synthesis in memory storage. Cell 91(7):927–938. https://doi.org/10.1016/S0092-8674(00)80484-5

  Article  CAS  PubMed  Google Scholar 

• Martin SJ, Grimwood PD, Morris RGM (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23(1):649–711. https://doi.org/10.1146/annurev.neuro.23.1.649

  Article  CAS  PubMed  Google Scholar 

• Martínez MC, Alen N, Ballarini F, Moncada D, Viola H (2012) Memory traces compete under regimes of limited arc protein synthesis: implications for memory interference. Neurobiol Learn Mem 98(2):165–173. https://doi.org/10.1016/j.nlm.2012.05.007

  Article  CAS  PubMed  Google Scholar 

• McNamara CG, Tejero-Cantero Á, Trouche S, Campo-Urriza N, Dupret D (2014) Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence. Nat Neurosci 17(12):1658–1660. https://doi.org/10.1038/nn.3843

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Medvedeva AV, Zhuravlev AV, Savvateeva-Popova EV (2010) LIMK1, the key enzyme of actin remodeling bridges spatial organization of nucleus and neural transmission: from heterochromatin via non-coding RNAs to complex behavior. Horiz Neurosci Res 4:161–193

  Google Scholar 

• Messaoudi E, Kanhema T, Soule J, Tiron A, Dagyte G, da Silva B, Bramham CR (2007) Sustained Arc/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo. J Neurosci 27(39):10445–10455. https://doi.org/10.1523/JNEUROSCI.2883-07.2007

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Migues PV, Hardt O, Wu DC, Gamache K, Sacktor TC, Wang YT, Nader K (2010) PKMζ maintains memories by regulating GluR2-dependent AMPA receptor trafficking. Nat Neurosci 13(5):630–634. https://doi.org/10.1038/nn.2531

  Article  CAS  PubMed  Google Scholar 

• Mikuni T, Nishiyama J, Sun Y, Kamasawa N, Yasuda R (2016) High-throughput, high-resolution mapping of protein localization in mammalian brain by in vivo genome editing. Cell 165(7):1803–1817. https://doi.org/10.1016/j.cell.2016.04.044

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Moncada D (2017) Evidence of VTA and LC control of protein synthesis required for the behavioral tagging process. Neurobiol Learn Mem 138:226–237. https://doi.org/10.1016/j.nlm.2016.06.003

  Article  CAS  PubMed  Google Scholar 

• Moncada D, Viola H (2007) Induction of long-term memory by exposure to novelty requires protein synthesis: evidence for a behavioral tagging. J Neurosci 27(28):7476–7481. https://doi.org/10.1523/JNEUROSCI.1083-07.2007

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Moncada D, Ballarini F, Martinez MC, Frey JU, Viola H (2011) Identification of transmitter systems and learning tag molecules involved in behavioral tagging during memory formation. Proc Natl Acad Sci 108(31):12931–12936. https://doi.org/10.1073/pnas.1104495108

  Article  PubMed  PubMed Central  Google Scholar 

• Moncada D, Ballarini F, Viola H (2015) Behavioral tagging: A translation of the synaptic tagging and capture hypothesis. Neural Plast 2015:1–21. https://doi.org/10.1155/2015/650780

  Article  Google Scholar 

• Morris RGM (2006) Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 23(11):2829–2846. https://doi.org/10.1111/j.1460-9568.2006.04888.x

  Article  CAS  PubMed  Google Scholar 

• Morris RGM, Amaral D, Bliss TVP, Duff K, O’Keefe J (2024) The hippocampus book, 2nd edn. Oxford University Press, New York

  Google Scholar 

• Murakoshi H, Wang H, Yasuda R (2011) Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature 472(7341):100–104. https://doi.org/10.1038/nature09823

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Murakoshi H, Shin ME, Parra-Bueno P, Szatmari EM, Shibata ACE, Yasuda R (2017) Kinetics of endogenous CaMKII required for synaptic plasticity revealed by optogenetic kinase inhibitor. Neuron 94(1):37–47.e5. https://doi.org/10.1016/j.neuron.2017.02.036

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Muslimov IA, Nimmrich V, Hernandez AI, Tcherepanov A, Sacktor TC, Tiedge H (2004) Dendritic transport and localization of protein kinase Mζ mRNA. J Biol Chem 279(50):52613–52622. https://doi.org/10.1074/jbc.M409240200

  Article  CAS  PubMed  Google Scholar 

• Nadella KS, Saji M, Jacob NK, Pavel E, Ringel MD, Kirschner LS (2009) Regulation of actin function by protein kinase A-mediated phosphorylation of Limk1. EMBO Rep 10(6):599–605. https://doi.org/10.1038/embor.2009.58

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Nagappan G, Zaitsev E, Senatorov VV, Yang J, Hempstead BL, Lu B (2009) Control of extracellular cleavage of ProBDNF by high frequency neuronal activity. Proc Natl Acad Sci 106(4):1267–1272. https://doi.org/10.1073/pnas.0807322106

  Article  PubMed  PubMed Central  Google Scholar 

• Nair RR, Patil S, Tiron A, Kanhema T, Panja D, Schiro L, Parobczak K, Wilczynski G, Bramham CR (2017) Dynamic arc SUMOylation and selective interaction with F-actin-binding protein Drebrin A in LTP consolidation in vivo. Front Synaptic Neurosci 9:25. https://doi.org/10.3389/fnsyn.2017.00008

  Article  CAS  Google Scholar 

• Nakahata Y, Yasuda R (2018) Plasticity of spine structure: local signaling, translation and cytoskeletal reorganization. Front Synaptic Neurosci 10:19. https://doi.org/10.3389/fnsyn.2018.00029

  Article  CAS  Google Scholar 

• Navakkode S (2005) Mitogen-activated protein kinase-mediated reinforcement of hippocampal early long-term depression by the type IV-specific phosphodiesterase inhibitor Rolipram and its effect on synaptic tagging. J Neurosci 25(46):10664–10670. https://doi.org/10.1523/JNEUROSCI.2443-05.2005

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Navakkode S, Sajikumar S, Sacktor TC, Frey JU (2010) Protein kinase Mζ is essential for the induction and maintenance of dopamine-induced long-term potentiation in apical CA1 dendrites. Learn Mem 17(12):605–611. https://doi.org/10.1101/lm.1991910

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Newey SE, Velamoor V, Govek E-E, Van Aelst L (2005) Rho GTPases, dendritic structure, and mental retardation. J Neurobiol 64(1):58–74. https://doi.org/10.1002/neu.20153

  Article  CAS  PubMed  Google Scholar 

• Newpher TM, Harris S, Pringle J, Hamilton C, Soderling S (2018) Regulation of spine structural plasticity by Arc/Arg3.1. Semin Cell Dev Biol 77:25–32. https://doi.org/10.1016/j.semcdb.2017.09.022

  Article  CAS  PubMed  Google Scholar 

• Nikolaienko O, Patil S, Eriksen MS, Bramham CR (2018) Arc protein: a flexible hub for synaptic plasticity and cognition. Semin Cell Dev Biol 77:33–42. https://doi.org/10.1016/j.semcdb.2017.09.006

  Article  CAS  PubMed  Google Scholar 

• Nomoto M, Inokuchi K (2018) Behavioral, cellular, and synaptic tagging frameworks. Neurobiol Learn Mem 153:13–20. https://doi.org/10.1016/j.nlm.2018.03.010

  Article  PubMed  Google Scholar 

• Nomoto M, Ohkawa N, Nishizono H, Yokose J, Suzuki A, Matsuo M, Tsujimura S, Takahashi Y, Nagase M, Watabe AM, Kato F, Inokuchi K (2016) Cellular tagging as a neural network mechanism for behavioural tagging. Nat Commun 7(1):12319. https://doi.org/10.1038/ncomms12319

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Okada D, Ozawa F, Inokuchi K (2009) Input-specific spine entry of Soma-derived Vesl-1S protein conforms to synaptic tagging. Science 324(5929):904–909. https://doi.org/10.1126/science.1171498

  Article  CAS  PubMed  Google Scholar 

• Okamoto K, Bosch M, Hayashi Y (2009) The roles of CaMKII and F-Actin in the structural plasticity of dendritic spines: a potential molecular identity of a synaptic tag? Physiology 24(6):357–366. https://doi.org/10.1152/physiol.00029.2009

  Article  CAS  PubMed  Google Scholar 

• Okuno H, Akashi K, Ishii Y, Yagishita-Kyo N, Suzuki K, Nonaka M, Kawashima T, Fujii H, Takemoto-Kimura S, Abe M, Natsume R, Chowdhury S, Sakimura K, Worley PF, Bito H (2012) Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIβ. Cell 149(4):886–898. https://doi.org/10.1016/j.cell.2012.02.062

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Panja D, Dagyte G, Bidinosti M, Wibrand K, Kristiansen Å-M, Sonenberg N, Bramham CR (2009) Novel translational control in Arc-dependent long term potentiation consolidation in vivo. J Biol Chem 284(46):31498–31511. https://doi.org/10.1074/jbc.M109.056077

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Park AJ, Havekes R, Choi JH, Luczak V, Nie T, Huang T, Abel T (2014) A presynaptic role for PKA in synaptic tagging and memory. Neurobiol Learn Mem 114:101–112. https://doi.org/10.1016/j.nlm.2014.05.005

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Park P, Sanderson TM, Amici M, Choi S-L, Bortolotto ZA, Zhuo M, Kaang B-K, Collingridge GL (2016) Calcium-permeable AMPA receptors mediate the induction of the protein kinase A-dependent component of long-term potentiation in the hippocampus. J Neurosci 36(2):622–631. https://doi.org/10.1523/JNEUROSCI.3625-15.2016

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Park AJ, Havekes R, Fu X, Hansen R, Tudor JC, Peixoto L, Li Z, Wu Y-C, Poplawski SG, Baraban JM, Abel T (2017) Learning induces the translin/trax RNase complex to express activin receptors for persistent memory. ELife 6: e27872. https://doi.org/10.7554/eLife.27872

• Park P, Kang H, Sanderson TM, Bortolotto ZA, Georgiou J, Zhuo M, Kaang B-K, Collingridge GL (2018) The role of calcium-permeable AMPARs in long-term potentiation at principal neurons in the rodent hippocampus. Front Synaptic Neurosci 10:65. https://doi.org/10.3389/fnsyn.2018.00042

  Article  CAS  Google Scholar 

• Park P, Kang H, Sanderson TM, Bortolotto ZA, Georgiou J, Zhuo M, Kaang B-K, Collingridge GL (2019) On the role of calcium-permeable AMPARs in long-term potentiation and synaptic tagging in the rodent hippocampus. Front Synaptic Neurosci 11:14–22. https://doi.org/10.3389/fnsyn.2019.00004

  Article  CAS  Google Scholar 

• Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313(5790):1141–1144. https://doi.org/10.1126/science.1128657

  Article  CAS  PubMed  Google Scholar 

• Patterson SL, Pittenger C, Morozov A, Martin KC, Scanlin H, Drake C, Kandel ER (2001) Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase. Neuron 32(1):123–140. https://doi.org/10.1016/S0896-6273(01)00443-3

  Article  CAS  PubMed  Google Scholar 

• Peng J, Kim MJ, Cheng D, Duong DM, Gygi SP, Sheng M (2004) Semiquantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry. J Biol Chem 279(20):21003–21011. https://doi.org/10.1074/jbc.M400103200

  Article  CAS  PubMed  Google Scholar 

• Pinho J, Marcut C, Fonseca R (2020) Actin remodeling, the synaptic tag and the maintenance of synaptic plasticity. IUBMB Life 72(4):577–589. https://doi.org/10.1002/iub.2261

  Article  CAS  PubMed  Google Scholar 

• Plath N, Ohana O, Dammermann B, Errington ML, Schmitz D, Gross C, Mao X, Engelsberg A, Mahlke C, Welzl H, Kobalz U, Stawrakakis A, Fernandez E, Waltereit R, Bick-Sander A, Therstappen E, Cooke SF, Blanquet V, Wurst W et al (2006) Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52(3):437–444. https://doi.org/10.1016/j.neuron.2006.08.024

• Pradhan J, Noakes PG, Bellingham MC (2019) The role of altered BDNF/TrkB signaling in amyotrophic lateral sclerosis. Front Cell Neurosci 13:14. https://doi.org/10.3389/fncel.2019.00368

  Article  CAS  Google Scholar 

• Prodan A, Davies H, Eneqvist H, Mastroberardino G, Wijayathunga H, Wardlaw K, Morris RGM (2022) Memory recall: new behavioral protocols for examining distinct forms of context specific recall in animals. Neurobiol Learn Mem 195:107685. https://doi.org/10.1016/j.nlm.2022.107685

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Racz B, Weinberg RJ (2006) Spatial organization of cofilin in dendritic spines. Neuroscience 138(2):447–456. https://doi.org/10.1016/j.neuroscience.2005.11.025

  Article  CAS  PubMed  Google Scholar 

• Ramachandran B, Frey JU (2009) Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices in vitro. J Neurosci 29(39):12167–12173. https://doi.org/10.1523/JNEUROSCI.2045-09.2009

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Ramirez Butavand D, Hirsch I, Tomaiuolo M, Moncada D, Viola H, Ballarini F (2020) Novelty improves the formation and persistence of memory in a naturalistic school scenario. Front Psychol 11:44. https://doi.org/10.3389/fpsyg.2020.00048

  Article  Google Scholar 

• Redondo RL, Morris RGM (2011) Making memories last: the synaptic tagging and capture hypothesis. Nat Rev Neurosci 12(1):17–30. https://doi.org/10.1038/nrn2963

  Article  CAS  PubMed  Google Scholar 

• Redondo RL, Okuno H, Spooner PA, Frenguelli BG, Bito H, Morris RGM (2010) Synaptic tagging and capture: differential role of distinct Calcium/Calmodulin kinases in protein synthesis-dependent long-term potentiation. J Neurosci 30(14):4981–4989. https://doi.org/10.1523/JNEUROSCI.3140-09.2010

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Reichardt LF (2006) Neurotrophin-regulated signalling pathways. Philos Trans R Soc B Biol Sci 361(1473):1545–1564. https://doi.org/10.1098/rstb.2006.1894

  Article  CAS  Google Scholar 

• Rodríguez JJ, Davies HA, Silva AT, De Souza IEJ, Peddie CJ, Colyer FM, Lancashire CL, Fine A, Errington ML, Bliss TVP, Stewart MG (2005) Long-term potentiation in the rat dentate gyrus is associated with enhanced arc/Arg3.1 protein expression in spines, dendrites and glia. Eur J Neurosci 21(9):2384–2396. https://doi.org/10.1111/j.1460-9568.2005.04068.x

  Article  PubMed  Google Scholar 

• Rudy JW (2015) Actin dynamics and the evolution of the memory trace. Brain Res 1621:17–28. https://doi.org/10.1016/j.brainres.2014.12.007

  Article  CAS  PubMed  Google Scholar 

• Ryan XP, Alldritt J, Svenningsson P, Allen PB, Wu G-Y, Nairn AC, Greengard P (2005) The rho-specific GEF Lfc interacts with neurabin and spinophilin to regulate dendritic spine morphology. Neuron 47(1):85–100. https://doi.org/10.1016/j.neuron.2005.05.013

  Article  CAS  PubMed  Google Scholar 

• Sajikumar S (2004) Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD. Neurobiol Learn Mem 82(1):12–25. https://doi.org/10.1016/j.nlm.2004.03.003

  Article  CAS  PubMed  Google Scholar 

• Sajikumar S (2005) Synaptic tagging and cross-tagging: the role of protein kinase M in maintaining long-term potentiation but not long-term depression. J Neurosci 25(24):5750–5756. https://doi.org/10.1523/JNEUROSCI.1104-05.2005

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Sajikumar S, Frey JU (2003) Anisomycin inhibits the late maintenance of long-term depression in rat hippocampal slices in vitro. Neurosci Lett 338(2):147–150. https://doi.org/10.1016/S0304-3940(02)01400-3

• Sajikumar S, Frey JU (2004) Resetting of ‘synaptic tags’ is time- and activity-dependent in rat hippocampal CA1in vitro. Neuroscience 129:503–507. https://doi.org/10.1016/j.neuroscience.2004.08.014

  Article  CAS  PubMed  Google Scholar 

• Sajikumar S, Korte M (2011) Metaplasticity governs compartmentalization of synaptic tagging and capture through brain-derived neurotrophic factor (BDNF) and protein kinase Mζ (PKMζ). Proc Natl Acad Sci 108(6):2551–2556. https://doi.org/10.1073/pnas.1016849108

• Sajikumar S, Navakkode S, Frey JU (2007) Identification of compartment and process-specific molecules required for “synaptic tagging” during long-term potentiation and long-term depression in hippocampal CA1. J Neurosci 27(19):5068–5080. https://doi.org/10.1523/JNEUROSCI.4940-06.2007

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Sajikumar S, Navakkode S, Frey JU (2008) Distinct single but not necessarily repeated tetanization is required to induce hippocampal late-LTP in the rat CA1: figure 1. Learn Mem 15(2):46–49. https://doi.org/10.1101/lm.816908

  Article  PubMed  Google Scholar 

• Sajikumar S, Morris RGM, Korte M (2014) Competition between recently potentiated synaptic inputs reveals a winner-take-all phase of synaptic tagging and capture. Proc Natl Acad Sci 111(33):12217–12221. https://doi.org/10.1073/pnas.1403643111

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Saneyoshi T, Matsuno H, Suzuki A, Murakoshi H, Hedrick NG, Agnello E, O’Connell R, Stratton MM, Yasuda R, Hayashi Y (2019) Reciprocal activation within a kinase-effector complex underlying persistence of structural LTP. Neuron 102(6):1199–1210.e6. https://doi.org/10.1016/j.neuron.2019.04.012

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Sarmiere PD, Bamburg JR (2004) Regulation of the neuronal actin cytoskeleton by ADF/cofilin. J Neurobiol 58(1):103–117. https://doi.org/10.1002/neu.10267

  Article  CAS  PubMed  Google Scholar 

• Sasi M, Vignoli B, Canossa M, Blum R (2017) Neurobiology of local and intercellular BDNF signaling. Pflugers Arch - Eur J Physiol 469(5–6):593–610. https://doi.org/10.1007/s00424-017-1964-4

  Article  CAS  Google Scholar 

• Scanziani M, Häusser M (2009) Electrophysiology in the age of light. Nature 461(7266):930–939. https://doi.org/10.1038/nature08540

  Article  CAS  PubMed  Google Scholar 

• Shema R, Haramati S, Ron S, Hazvi S, Chen A, Sacktor TC, Dudai Y (2011) Enhancement of consolidated long-term memory by overexpression of protein kinase Mζ in the neocortex. Science 331(6021):1207–1210. https://doi.org/10.1126/science.1200215

  Article  CAS  PubMed  Google Scholar 

• Shetty MS, Sharma M, Hui NS, Dasgupta A, Gopinadhan S, Sajikumar S (2015) Investigation of synaptic tagging/capture and cross-capture using acute hippocampal slices from rodents. J Vis Exp 103. https://doi.org/10.3791/53008

• Shires KL, Da Silva BM, Hawthorne JP, Morris RGM, Martin SJ (2012) Synaptic tagging and capture in the living rat. Nat Commun 3(1):1246. https://doi.org/10.1038/ncomms2250

  Article  CAS  PubMed  Google Scholar 

• Skeberdis VA, Chevaleyre V, Lau CG, Goldberg JH, Petti, DL, Suadicani SO, Lin Y, Bennett MVL, Yuste R, Castillo PE, Zukin RS (2006) Protein kinase A regulates calcium permeability of NMDA receptors. Nat Neurosci 9(4):501–510. https://doi.org/10.1038/nn1664

• Smith CC, Greene RW (2012) CNS dopamine transmission mediated by noradrenergic innervation. J Neurosci 32(18):6072–6080. https://doi.org/10.1523/JNEUROSCI.6486-11.2012

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Smolen P, Baxter DA, Byrne JH (2012) Molecular constraints on synaptic tagging and maintenance of long-term potentiation: A predictive model. PLoS Comput Biol 8(8):e1002620. https://doi.org/10.1371/journal.pcbi.1002620

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Squire LR, Genzel L, Wixted JT, Morris RG (2015) Memory consolidation. Cold Spring Harb Perspect Biol 7(8):a021766. https://doi.org/10.1101/cshperspect.a021766

  Article  PubMed  PubMed Central  Google Scholar 

• Steward O, Levy W (1982) Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J Neurosci 2(3):284–291. https://doi.org/10.1523/JNEUROSCI.02-03-00284.1982

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Symons M, Settleman J (2000) Rho family GTPases: more than simple switches. Trends Cell Biol 10(10):415–419. https://doi.org/10.1016/S0962-8924(00)01832-8

  Article  CAS  PubMed  Google Scholar 

• Takeuchi T, Duszkiewicz AJ, Sonneborn A, Spooner PA, Yamasaki M, Watanabe M, Smith CC, Fernández G, Deisseroth K, Greene RW, Morris RGM (2016) Locus coeruleus and dopaminergic consolidation of everyday memory. Nature 537(7620):357–362. https://doi.org/10.1038/nature19325

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Tanaka J, Horiike Y, Matsuzaki M, Miyazaki T, Ellis-Davies GCR, Kasai H (2008) Protein synthesis and Neurotrophin-dependent structural plasticity of single dendritic spines. Science 319(5870):1683–1687. https://doi.org/10.1126/science.1152864

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Tang S, Yasuda R (2017) Imaging ERK and PKA activation in single dendritic spines during structural plasticity. Neuron 93(6):1315–1324.e3. https://doi.org/10.1016/j.neuron.2017.02.032

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Teng HK (2005) ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and Sortilin. J Neurosci 25(22):5455–5463. https://doi.org/10.1523/JNEUROSCI.5123-04.2005

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Thiel G, Czernik AJ, Gorelick F, Nairn AC, Greengard P (1988) Ca2+/calmodulin-dependent protein kinase II: identification of threonine-286 as the autophosphorylation site in the alpha subunit associated with the generation of Ca2+−independent activity. Proc Natl Acad Sci 85(17):6337–6341. https://doi.org/10.1073/pnas.85.17.6337

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Tobimatsu T, Fujisawa H (1989) Tissue-specific expression of four types of rat calmodulin-dependent protein kinase II mRNAs. J Biol Chem 264(30):17907–17912. https://doi.org/10.1016/S0021-9258(19)84658-6

  Article  CAS  PubMed  Google Scholar 

• Tomaiuolo M, Katche C, Viola H, Medina JH (2015) Evidence of maintenance tagging in the hippocampus for the persistence of long-lasting memory storage. Neural Plast 2015:1–9. https://doi.org/10.1155/2015/603672

  Article  Google Scholar 

• Tønnesen J, Katona G, Rózsa B, Nägerl UV (2014) Spine neck plasticity regulates compartmentalization of synapses. Nat Neurosci 17(5):678–685. https://doi.org/10.1038/nn.3682

  Article  CAS  PubMed  Google Scholar 

• Tse D, Privitera L, Norton AC, Gobbo F, Spooner P, Takeuchi T, Martin SJ, Morris RGM (2023) Cell-type-specific optogenetic stimulation of the locus coeruleus induces slow-onset potentiation and enhances everyday memory in rats. Proc Natl Acad Sci 120(46): e2307275120. https://doi.org/10.1073/pnas.2307275120

• Tsokas P, Hsieh C, Yao Y, Lesburguères E, Wallace EJC, Tcherepanov A, Jothianandan D, Hartley BR, Pan L, Rivard B, Farese RV, Sajan MP, Bergold PJ, Hernández AI, Cottrell JE, Shouval HZ, Fenton AA, Sacktor TC (2016) Compensation for PKMζ in long-term potentiation and spatial long-term memory in mutant mice. elife 5:74. https://doi.org/10.7554/eLife.14846

  Article  Google Scholar 

• Tsumoto T (1993) Long-term depression in cerebral cortex: a possible substrate of “forgetting” that should not be forgotten. Neurosci Res 16(4):263–270. https://doi.org/10.1016/0168-0102(93)90036-P

  Article  CAS  PubMed  Google Scholar 

• Vickers CA, Dickson KS, Wyllie DJA (2005) Induction and maintenance of late-phase long-term potentiation in isolated dendrites of rat hippocampal CA1 pyramidal neurons. J Physiol 568(3):803–813. https://doi.org/10.1113/jphysiol.2005.092924

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Vilar M, Mira H (2016) Regulation of neurogenesis by Neurotrophins during adulthood: expected and unexpected roles. Front Neurosci 10:22. https://doi.org/10.3389/fnins.2016.00026

  Article  Google Scholar 

• Viola H, Ballarini F, Martínez MC, Moncada D (2014) The tagging and capture hypothesis from synapse to memory. Prog Mol Biol Transl Sci 122:391–423. https://doi.org/10.1016/B978-0-12-420170-5.00013-1

  Article  PubMed  Google Scholar 

• Vishnoi S, Raisuddin S, Parvez S (2022) Behavioral tagging: role of neurotransmitter receptor systems in novel object recognition long-term memory. ACS Omega 7(14):11587–11595. https://doi.org/10.1021/acsomega.1c05865

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Volk LJ, Bachman JL, Johnson R, Yu Y, Huganir RL (2013) PKM-ζ is not required for hippocampal synaptic plasticity, learning and memory. Nature 493(7432):420–423. https://doi.org/10.1038/nature11802

  Article  CAS  PubMed  Google Scholar 

• Wang S-H, Redondo RL, Morris RGM (2010) Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory. Proc Natl Acad Sci 107(45):19537–19542. https://doi.org/10.1073/pnas.1008638107

  Article  PubMed  PubMed Central  Google Scholar 

• Westmark PR, Westmark CJ, Wang S, Levenson J, O’Riordan KJ, Burger C, Malter JS (2010) Pin1 and PKMζ sequentially control dendritic protein synthesis. Sci Signal 3(112):55. https://doi.org/10.1126/scisignal.2000451

  Article  CAS  Google Scholar 

• Xie Z, Srivastava DP, Photowala H, Kai L, Cahill ME, Woolfrey KM, Shum CY, Surmeier DJ, Penzes P (2007) Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 56(4):640–656. https://doi.org/10.1016/j.neuron.2007.10.005

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Yamasaki M, Takeuchi T (2017) Locus coeruleus and dopamine-dependent memory consolidation. Neural Plast 2017:1–15. https://doi.org/10.1155/2017/8602690

  Article  CAS  Google Scholar 

• Yao R-Q, Qi D-S, Yu H-L, Liu J, Yang L-H, Wu X-X (2012) Quercetin attenuates cell apoptosis in focal cerebral ischemia rat brain via activation of BDNF–TrkB–PI3K/Akt signaling pathway. Neurochem Res 37(12):2777–2786. https://doi.org/10.1007/s11064-012-0871-5

  Article  CAS  PubMed  Google Scholar 

• Yasuda R, Murakoshi H (2011) The mechanisms underlying the spatial spreading of signaling activity. Curr Opin Neurobiol 21(2):313–321. https://doi.org/10.1016/j.conb.2011.02.008

  Article  CAS  PubMed  PubMed Central  Google Scholar 

• Young JZ, Isiegas C, Abel T, Nguyen PV (2006) Metaplasticity of the late-phase of long-term potentiation: a critical role for protein kinase A in synaptic tagging. Eur J Neurosci 23(7):1784–1794. https://doi.org/10.1111/j.1460-9568.2006.04707.x

  Article  PubMed  PubMed Central  Google Scholar 

Download references