Abstract
Most everyday memories, including numerous episodic memories formed automatically in the hippocampus, are forgotten. However, some memories are retained for extended periods through a memory stabilization process known as cellular or initial memory consolidation. Notably, in both animals and humans, the retention of everyday memories is enhanced during novel experiences occurring shortly before or after memory encoding, a process known as synaptic tagging and capture (STC). A growing body of evidence suggests that dopamine signaling via D1/D5 receptors in the hippocampus is crucial for the persistence of synaptic plasticity and memory, highlighting its significant role in novelty-associated memory enhancement. This chapter presents an overview of key findings related to the persistence of synaptic plasticity and memory in the hippocampus through hippocampal D1/D5 receptor dependency, with special emphasis on the emerging role of the locus coeruleus (LC) in novelty-associated dopamine-dependent memory consolidation. Furthermore, two distinct dopaminergic systems are explored (the ventral tegmental area (VTA)-hippocampal and LC-hippocampal systems), and the specialization mechanisms of each system in different memory consolidation processes are discussed. Additionally, the anatomical and molecular foundations of D1/D5 receptor-mediated signaling in the LC-hippocampal system are examined. Finally, the molecular mechanisms possibly underlying distinct novelty-associated memory enhancement are discussed, including the involvement of plasticity-related proteins (PRPs) in the stabilization of structural and functional changes at potentiated synapses, culminating in initial memory consolidation in the hippocampus.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abel T, Nguyen PV, Barad M, Deuel TA, Kandel ER, Bourtchouladze R (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615–626
Aleman-Zapata A, Morris RGM, Genzel L (2022) Sleep deprivation and hippocampal ripple disruption after one-session learning eliminate memory expression the next day. Proc Natl Acad Sci USA 119:e2123424119
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 USA 106:14599–14604
Ballarini F, Martinez MC, Diaz Perez M, Moncada D, Viola H (2013) Memory in elementary school children is improved by an unrelated novel experience. PLoS One 8:e66875
Baltaci SB, Mogulkoc R, Baltaci AK (2019) Molecular mechanisms of early and late LTP. Neurochem Res 44:281–296
Barco A, Alarcon JM, Kandel ER (2002) Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108:689–703
Battaglia FP, Benchenane K, Sirota A, Pennartz CM, Wiener SI (2011) The hippocampus: hub of brain network communication for memory. Trends Cogn Sci 15:310–318
Beaulieu JM, Espinoza S, Gainetdinov RR (2015) Dopamine receptors – IUPHAR review 13. Br J Pharmacol 172:1–23
Bernabeu R, Bevilaqua L, Ardenghi P, Bromberg E, Schmitz P et al (1997) Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proc Natl Acad Sci USA 94:7041–7046
Bethus I, Tse D, Morris RG (2010) Dopamine and memory: modulation of the persistence of memory for novel hippocampal NMDA receptor-dependent paired associates. J Neurosci 30:1610–1618
Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39
Borgkvist A, Malmlof T, Feltmann K, Lindskog M, Schilstrom B (2012) Dopamine in the hippocampus is cleared by the norepinephrine transporter. Int J Neuropsychopharmacol 15:531–540
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 82:444–459
Brigidi GS, Hayes MGB, Delos Santos NP, Hartzell AL, Texari L et al (2019) Genomic decoding of neuronal depolarization by stimulus-specific NPAS4 heterodimers. Cell 179:373–391 e327
Broadbent N, Lumeij LB, Corcoles M, Ayres AI, Bin Ibrahim MZ et al (2020) A stable home-base promotes allocentric memory representations of episodic-like everyday spatial memory. Eur J Neurosci 51:1539–1558
Brodt S, Inostroza M, Niethard N, Born J (2023) Sleep-A brain-state serving systems memory consolidation. Neuron 111:1050–1075
Broussard JI, Yang K, Levine AT, Tsetsenis T, Jenson D et al (2016) Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the hippocampus. Cell Rep 14:1930–1939
Brown R, Kulik J (1977) Flashbulb memories. Cognition 5:73–99
Buonarati OR, Hammes EA, Watson JF, Greger IH, Hell JW (2019) Mechanisms of postsynaptic localization of AMPA-type glutamate receptors and their regulation during long-term potentiation. Sci Signal 12
Caille I, Dumartin B, Bloch B (1996) Ultrastructural localization of D1 dopamine receptor immunoreactivity in rat striatonigral neurons and its relation with dopaminergic innervation. Brain Res 730:17–31
Camps M, Kelly PH, Palacios JM (1990) Autoradiographic localization of dopamine D 1 and D 2 receptors in the brain of several mammalian species. J Neural Transm Gen Sect 80:105–127
Chowdhury A, Luchetti A, Fernandes G, Filho DA, Kastellakis G et al (2022) A locus coeruleus-dorsal CA1 dopaminergic circuit modulates memory linking. Neuron 110:3374–3388 e3378
Christensen DZ, Thomsen MS, Mikkelsen JD (2013) Reduced basal and novelty-induced levels of activity-regulated cytoskeleton associated protein (Arc) and c-Fos mRNA in the cerebral cortex and hippocampus of APPswe/PS1DeltaE9 transgenic mice. Neurochem Int 63:54–60
Ciliax BJ, Heilman C, Demchyshyn LL, Pristupa ZB, Ince E et al (1995) The dopamine transporter: immunochemical characterization and localization in brain. J Neurosci 15:1714–1723
Clifton NE, Cameron D, Trent S, Sykes LH, Thomas KL, Hall J (2017) Hippocampal regulation of postsynaptic density Homer1 by associative learning. Neural Plast 2017:5959182
Coulter CL, Happe HK, Bergman DA, Murrin LC (1995) Localization and quantification of the dopamine transporter: comparison of [3H]WIN 35,428 and [125I]RTI-55. Brain Res 690:217–224
Cragg SJ, Rice ME (2004) DAncing past the DAT at a DA synapse. Trends Neurosci 27:270–277
Curet O, Dennis T, Scatton B (1985) The formation of deaminated metabolites of dopamine in the locus coeruleus depends upon noradrenergic neuronal activity. Brain Res 335:297–301
da Silva WC, Kohler CC, Radiske A, Cammarota M (2012) D1/D5 dopamine receptors modulate spatial memory formation. Neurobiol Learn Mem 97:271–275
Dawson TM, Barone P, Sidhu A, Wamsley JK, Chase TN (1986a) Quantitative autoradiographic localization of D-1 dopamine receptors in the rat brain: use of the iodinated ligand [125I]SCH 23982. Neurosci Lett 68:261–266
Dawson TM, Gehlert DR, McCabe RT, Barnett A, Wamsley JK (1986b) D-1 dopamine receptors in the rat brain: a quantitative autoradiographic analysis. J Neurosci 6:2352–2365
Devoto P, Flore G (2006) On the origin of cortical dopamine: is it a co-transmitter in noradrenergic neurons? Curr Neuropharmacol 4:115–125
Devoto P, Flore G, Pani L, Gessa GL (2001) Evidence for co-release of noradrenaline and dopamine from noradrenergic neurons in the cerebral cortex. Mol Psychiatry 6:657–664
Devoto P, Flore G, Saba P, Fa M, Gessa GL (2005a) Co-release of noradrenaline and dopamine in the cerebral cortex elicited by single train and repeated train stimulation of the locus coeruleus. BMC Neurosci 6:31
Devoto P, Flore G, Saba P, Fa M, Gessa GL (2005b) Stimulation of the locus coeruleus elicits noradrenaline and dopamine release in the medial prefrontal and parietal cortex. J Neurochem 92:368–374
Diering GH, Huganir RL (2018) The AMPA receptor code of synaptic plasticity. Neuron 100:314–329
Droogers WJ, MacGillavry HD (2023) Plasticity of postsynaptic nanostructure. Mol Cell Neurosci 124:103819
Dudai Y, Morris RGM (2001) To consolidate or not to consolidate: what are the questions? In: Bolhuis J (ed) Brain, perception and memory: advances in cognitive sciences. OUP, Oxford, pp 147–162
Dunsmoor JE, Murty VP, Davachi L, Phelps EA (2015) Emotional learning selectively and retroactively strengthens memories for related events. Nature 520:345–348
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 26:782–795
Duszkiewicz AJ, McNamara CG, Takeuchi T, Genzel L (2019) Novelty and dopaminergic modulation of memory persistence: a tale of two systems. Trends Neurosci 42:102–114
Ebbinghaus H (1913) Memory: a contribution to experimental psychology. Teachers College, Columbia University
Ego-Stengel V, Wilson MA (2010) Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20:1–10
El-Ghundi M, Fletcher PJ, Drago J, Sibley DR, O’Dowd BF, George SR (1999) Spatial learning deficit in dopamine D(1) receptor knockout mice. Eur J Pharmacol 383:95–106
Feng J, Zhang C, Lischinsky JE, **g M, Zhou J et al (2019) A genetically encoded fluorescent sensor for rapid and specific in vivo detection of norepinephrine. Neuron 102:745–761 e748
Florian C, Mons N, Roullet P (2006) CREB antisense oligodeoxynucleotide administration into the dorsal hippocampal CA3 region impairs long- but not short-term spatial memory in mice. Learn Mem 13:465–472
Fremeau RT Jr, Duncan GE, Fornaretto MG, Dearry A, Gingrich JA et al (1991) Localization of D1 dopamine receptor mRNA in brain supports a role in cognitive, affective, and neuroendocrine aspects of dopaminergic neurotransmission. Proc Natl Acad Sci USA 88:3772–3776
Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533–536
Frey U, Morris RG (1998) Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci 21:181–188
Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57–65
Frey U, Schroeder H, Matthies H (1990) Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices. Brain Res 522:69–75
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 129:111–114
Frotscher M, Leranth C (1988) Catecholaminergic innervation of pyramidal and GABAergic nonpyramidal neurons in the rat hippocampus. Double label immunostaining with antibodies against tyrosine hydroxylase and glutamate decarboxylase. Histochemistry 88:313–319
Furini CR, Myskiw JC, Schmidt BE, Marcondes LA, Izquierdo I (2014) D1 and D5 dopamine receptors participate on the consolidation of two different memories. Behav Brain Res 271:212–217
Gálvez-Márquez DK, Salgado-Ménez M, Moreno-Castilla P, Rodríguez-Durán L, Escobar ML et al (2022) Spatial contextual recognition memory updating is modulated by dopamine release in the dorsal hippocampus from the locus coeruleus. Proc Natl Acad Sci USA 119:e2208254119
Gangarossa G, Longueville S, De Bundel D, Perroy J, Herve D et al (2012) Characterization of dopamine D1 and D2 receptor-expressing neurons in the mouse hippocampus. Hippocampus 22:2199–2207
Gasbarri A, Packard MG, Campana E, Pacitti C (1994a) Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat. Brain Res Bull 33:445–452
Gasbarri A, Verney C, Innocenzi R, Campana E, Pacitti C (1994b) Mesolimbic dopaminergic neurons innervating the hippocampal formation in the rat: a combined retrograde tracing and immunohistochemical study. Brain Res 668:71–79
Genzel L, Kroes MC, Dresler M, Battaglia FP (2014) Light sleep versus slow wave sleep in memory consolidation: a question of global versus local processes? Trends Neurosci 37:10–19
Genzel L, Rossato JI, Jacobse J, Grieves RM, Spooner PA et al (2017) The Yin and Yang of memory consolidation: hippocampal and neocortical. PLoS Biol 15:e2000531
Getz AM, Ducros M, Breillat C, Lampin-Saint-Amaux A, Daburon S et al (2022) High-resolution imaging and manipulation of endogenous AMPA receptor surface mobility during synaptic plasticity and learning. Sci Adv 8:eabm5298
Gilboa A, Moscovitch M (2021) No consolidation without representation: correspondence between neural and psychological representations in recent and remote memory. Neuron 109:2239–2255
Girardeau G, Zugaro M (2011) Hippocampal ripples and memory consolidation. Curr Opin Neurobiol 21:452–459
Girardeau G, Benchenane K, Wiener SI, Buzsaki G, Zugaro MB (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12:1222–1223
Govindarajan A, Israely I, Huang SY, Tonegawa S (2011) The dendritic branch is the preferred integrative unit for protein synthesis-dependent LTP. Neuron 69:132–146
Granado N, Ortiz O, Suarez LM, Martin ED, Cena V et al (2008) D1 but not D5 dopamine receptors are critical for LTP, spatial learning, and LTP-induced arc and zif268 expression in the hippocampus. Cereb Cortex 18:1–12
Groc L, Choquet D (2020) Linking glutamate receptor movements and synapse function. Science 368:eaay4631
Guzowski JF, McGaugh JL (1997) Antisense oligodeoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc Natl Acad Sci USA 94:2693–2698
Guzowski JF, McNaughton BL, Barnes CA, Worley PF (1999) Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2:1120–1124
Hansen N, Manahan-Vaughan D (2014) Dopamine D1/D5 receptors mediate informational saliency that promotes persistent hippocampal long-term plasticity. Cereb Cortex 24:845–858
Hiester BG, Becker MI, Bowen AB, Schwartz SL, Kennedy MJ (2018) Mechanisms and role of dendritic membrane trafficking for long-term potentiation. Front Cell Neurosci 12:391
Hirst W, Phelps EA, Buckner RL, Budson AE, Cuc A et al (2009) Long-term memory for the terrorist attack of September 11: flashbulb memories, event memories, and the factors that influence their retention. J Exp Psychol Gen 138:161–176
Hjorth-Simonsen A, Jeune B (1972) Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J Comp Neurol 144:215–232
Højgaard K, Szöllősi B, Henningsen K, Minami N, Nakanishi N et al (2023) Novelty-induced memory consolidation is accompanied by increased Agap3 transcription: a cross-species study. Research Square
Horn AS (1973) Structure-activity relations for the inhibition of catecholamine uptake into synaptosomes from noradrenaline and dopaminergic neurons in rat brain homogenates. Br J Pharmacol 47:332–338
Huang YY, Kandel ER (1995) D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc Natl Acad Sci USA 92:2446–2450
Karunakaran S, Chowdhury A, Donato F, Quairiaux C, Michel CM, Caroni P (2016) PV plasticity sustained through D1/5 dopamine signaling required for long-term memory consolidation. Nat Neurosci 19:454–464
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 USA 113:14835–14840
Kentros CG, Agnihotri NT, Streater S, Hawkins RD, Kandel ER (2004) Increased attention to spatial context increases both place field stability and spatial memory. Neuron 42:283–295
Kern A, Mavrikaki M, Ullrich C, Albarran-Zeckler R, Brantley AF, Smith RG (2015) Hippocampal dopamine/DRD1 signaling dependent on the ghrelin receptor. Cell 163:1176–1190
Khan ZU, Gutierrez A, Martin R, Penafiel A, Rivera A, de la Calle A (2000) Dopamine D5 receptors of rat and human brain. Neuroscience 100:689–699
Kramar CP, Castillo-Diaz F, Gigante ED, Medina JH, Barbano MF (2021) The late consolidation of an aversive memory is promoted by VTA dopamine release in the dorsal hippocampus. Eur J Neurosci 53:841–851
Kruijssen DLH, Wierenga CJ (2019) Single synapse LTP: a matter of context? Front Cell Neurosci 13:496
Kwon OB, Paredes D, Gonzalez CM, Neddens J, Hernandez L et al (2008) Neuregulin-1 regulates LTP at CA1 hippocampal synapses through activation of dopamine D4 receptors. Proc Natl Acad Sci USA 105:15587–15592
Ladepeche L, Dupuis JP, Bouchet D, Doudnikoff E, Yang L et al (2013) Single-molecule imaging of the functional crosstalk between surface NMDA and dopamine D1 receptors. Proc Natl Acad Sci USA 110:18005–18010
Laplante F, Sibley DR, Quirion R (2004) Reduction in acetylcholine release in the hippocampus of dopamine D5 receptor-deficient mice. Neuropsychopharmacology 29:1620–1627
Lee FJ, Xue S, Pei L, Vukusic B, Chery N et al (2002) Dual regulation of NMDA receptor functions by direct protein-protein interactions with the dopamine D1 receptor. Cell 111:219–230
Lee H, GoodSmith D, Knierim JJ (2020) Parallel processing streams in the hippocampus. Curr Opin Neurobiol 64:127–134
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 26:7723–7729
Lemon N, Manahan-Vaughan D (2012) Dopamine D1/D5 receptors contribute to de novo hippocampal LTD mediated by novel spatial exploration or locus coeruleus activity. Cereb Cortex 22:2131–2138
Lima KR, da Rosa ACS, Picua SS, SS ES, Soares NM, Mello-Carpes PB. (2022) Novelty promotes recognition memory persistence by D1 dopamine receptor and protein kinase A signalling in rat hippocampus. Eur J Neurosci 55:78–90
Lisman JE, Grace AA (2005) The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46:703–713
Liu F, Wan Q, Pristupa ZB, Yu XM, Wang YT, Niznik HB (2000) Direct protein-protein coupling enables cross-talk between dopamine D5 and gamma-aminobutyric acid A receptors. Nature 403:274–280
Liu C, Goel P, Kaeser PS (2021) Spatial and temporal scales of dopamine transmission. Nat Rev Neurosci 22:345–358
Lorents A, Ruitenberg MFL, Schomaker J (2023) Novelty-induced memory boosts in humans: the when and how. Heliyon 9:e14410
Loy R, Koziell DA, Lindsey JD, Moore RY (1980) Noradrenergic innervation of the adult rat hippocampal formation. J Comp Neurol 189:699–710
Lu Y, Ji Y, Ganesan S, Schloesser R, Martinowich K et al (2011) TrkB as a potential synaptic and behavioral tag. J Neurosci 31:11762–11771
Maingret F, Groc L (2021) Characterization of the functional cross-talk between surface GABA(A) and dopamine D5 receptors. Int J Mol Sci 22
Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5–21
Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103–126
Mansour A, Meador-Woodruff JH, Zhou Q, Civelli O, Akil H, Watson SJ (1992) A comparison of D1 receptor binding and mRNA in rat brain using receptor autoradiographic and in situ hybridization techniques. Neuroscience 46:959–971
Marr D (1971) Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262:23–81
Matthies H, Becker A, Schroeder H, Kraus J, Hollt V, Krug M (1997) Dopamine D1-deficient mutant mice do not express the late phase of hippocampal long-term potentiation. Neuroreport 8:3533–3535
McNamara CG, Tejero-Cantero A, Trouche S, Campo-Urriza N, Dupret D (2014) Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence. Nat Neurosci 17:1658–1660
Meador-Woodruff JH, Mansour A, Grandy DK, Damask SP, Civelli O, Watson SJ Jr (1992) Distribution of D5 dopamine receptor mRNA in rat brain. Neurosci Lett 145:209–212
Merhav M, Rosenblum K (2008) Facilitation of taste memory acquisition by experiencing previous novel taste is protein-synthesis dependent. Learn Mem 15:501–507
Meyer D, Bonhoeffer T, Scheuss V (2014) Balance and stability of synaptic structures during synaptic plasticity. Neuron 82:430–443
Milner TA, Bacon CE (1989) GABAergic neurons in the rat hippocampal formation: ultrastructure and synaptic relationships with catecholaminergic terminals. J Neurosci 9:3410–3427
Missale C, Nash SR, Robinson SW, Jaber M, Caron MG (1998) Dopamine receptors: from structure to function. Physiol Rev 78:189–225
Moncada D, Viola H (2006) Phosphorylation state of CREB in the rat hippocampus: a molecular switch between spatial novelty and spatial familiarity? Neurobiol Learn Mem 86:9–18
Moncada D, Viola H (2007) Induction of long-term memory by exposure to novelty requires protein synthesis: evidence for a behavioral tagging. J Neurosci 27:7476–7481
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 USA 108:12931–12936
Moraga-Amaro R, Gonzalez H, Ugalde V, Donoso-Ramos JP, Quintana-Donoso D et al (2016) Dopamine receptor D5 deficiency results in a selective reduction of hippocampal NMDA receptor subunit NR2B expression and impaired memory. Neuropharmacology 103:222–235
Moron JA, Brockington A, Wise RA, Rocha BA, Hope BT (2002) Dopamine uptake through the norepinephrine transporter in brain regions with low levels of the dopamine transporter: evidence from knock-out mouse lines. J Neurosci 22:389–395
Morris RG (2006) Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 23:2829–2846
Moscovitch M (1995) Recovered consciousness: a hypothesis concerning modularity and episodic memory. J Clin Exp Neuropsychol 17:276–290
Moscovitch M, Cabeza R, Winocur G, Nadel L (2016) Episodic memory and beyond: the hippocampus and neocortex in transformation. Annu Rev Psychol 67:105–134
Mu Y, Zhao C, Gage FH (2011) Dopaminergic modulation of cortical inputs during maturation of adult-born dentate granule cells. J Neurosci 31:4113–4123
Murata Y, Chiba T, Brundin P, Bjorklund A, Lindvall O (1990) Formation of synaptic graft-host connections by noradrenergic locus coeruleus neurons transplanted into the adult rat hippocampus. Exp Neurol 110:258–267
Nair D, Hosy E, Petersen JD, Constals A, Giannone G et al (2013) Super-resolution imaging reveals that AMPA receptors inside synapses are dynamically organized in nanodomains regulated by PSD95. J Neurosci 33:13204–13224
Nakamoto C, Goto Y, Tomizawa Y, Fukata Y, Fukata M et al (2021) A novel red fluorescence dopamine biosensor selectively detects dopamine in the presence of norepinephrine in vitro. Mol Brain 14:173
Navakkode S, Sajikumar S, Frey JU (2007) Synergistic requirements for the induction of dopaminergic D1/D5-receptor-mediated LTP in hippocampal slices of rat CA1 in vitro. Neuropharmacology 52:1547–1554
Navarro-Lobato I, Genzel L (2019) The up and down of sleep: from molecules to electrophysiology. Neurobiol Learn Mem 160:3–10
Nicoll RA (2017) A brief history of long-term potentiation. Neuron 93:281–290
Nomoto M, Ohkawa N, Nishizono H, Yokose J, Suzuki A et al (2016) Cellular tagging as a neural network mechanism for behavioural tagging. Nat Commun 7:12319
O’Carroll CM, Morris RG (2004) Heterosynaptic co-activation of glutamatergic and dopaminergic afferents is required to induce persistent long-term potentiation. Neuropharmacology 47:324–332
O’Carroll CM, Martin SJ, Sandin J, Frenguelli B, Morris RG (2006) Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memory. Learn Mem 13:760–769
Okada D, Ozawa F, Inokuchi K (2009) Input-specific spine entry of soma-derived Vesl-1S protein conforms to synaptic tagging. Science 324:904–909
Oku Y, Huganir RL (2013) AGAP3 and Arf6 regulate trafficking of AMPA receptors and synaptic plasticity. J Neurosci 33:12586–12598
Okuda K, Hojgaard K, Privitera L, Bayraktar G, Takeuchi T (2021) Initial memory consolidation and the synaptic tagging and capture hypothesis. Eur J Neurosci 54:6826–6849
Oleskevich S, Descarries L, Lacaille JC (1989) Quantified distribution of the noradrenaline innervation in the hippocampus of adult rat. J Neurosci 9:3803–3815
Ortiz O, Delgado-Garcia JM, Espadas I, Bahi A, Trullas R et al (2010) Associative learning and CA3-CA1 synaptic plasticity are impaired in D1R null, Drd1a−/− mice and in hippocampal siRNA silenced Drd1a mice. J Neurosci 30:12288–12300
Pacholczyk T, Blakely RD, Amara SG (1991) Expression cloning of a cocaine- and antidepressant-sensitive human noradrenaline transporter. Nature 350:350–354
Park AJ, Havekes R, Fu X, Hansen R, Tudor JC et al (2017) Learning induces the translin/trax RNase complex to express activin receptors for persistent memory. elife 6
Patriarchi T, Mohebi A, Sun J, Marley A, Liang R et al (2020) An expanded palette of dopamine sensors for multiplex imaging in vivo. Nat Methods 17:1147–1155
Patterson SL, Pittenger C, Morozov A, Martin KC, Scanlin H et al (2001) Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase. Neuron 32:123–140
Pei L, Lee FJ, Moszczynska A, Vukusic B, Liu F (2004) Regulation of dopamine D1 receptor function by physical interaction with the NMDA receptors. J Neurosci 24:1149–1158
Perreault ML, Hasbi A, O’Dowd BF, George SR (2014) Heteromeric dopamine receptor signaling complexes: emerging neurobiology and disease relevance. Neuropsychopharmacology 39:156–168
Peters M, Bletsch M, Catapano R, Zhang X, Tully T, Bourtchouladze R (2009) RNA interference in hippocampus demonstrates opposing roles for CREB and PP1α in contextual and temporal long-term memory. Genes Brain Behav 8:320–329
Peyrache A, Khamassi M, Benchenane K, Wiener SI, Battaglia FP (2009) Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat Neurosci 12:919–926
Pezze M, Bast T (2012) Dopaminergic modulation of hippocampus-dependent learning: blockade of hippocampal D1-class receptors during learning impairs 1-trial place memory at a 30-min retention delay. Neuropharmacology 63:710–718
Pinho J, Marcut C, Fonseca R (2020) Actin remodeling, the synaptic tag and the maintenance of synaptic plasticity. IUBMB Life 72:577–589
Prokopiou PC, Engels-Dominguez N, Papp KV, Scott MR, Schultz AP et al (2022) Lower novelty-related locus coeruleus function is associated with Abeta-related cognitive decline in clinically healthy individuals. Nat Commun 13:1571
Puighermanal E, Cutando L, Boubaker-Vitre J, Honore E, Longueville S et al (2016) Anatomical and molecular characterization of dopamine D1 receptor-expressing neurons of the mouse CA1 dorsal hippocampus. Brain Struct Funct 222:1897
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 11:48
Rao-Ruiz P, Couey JJ, Marcelo IM, Bouwkamp CG, Slump DE et al (2019) Engram-specific transcriptome profiling of contextual memory consolidation. Nat Commun 10:2232
Redondo RL, Morris RG (2011) Making memories last: the synaptic tagging and capture hypothesis. Nat Rev Neurosci 12:17–30
Redondo RL, Okuno H, Spooner PA, Frenguelli BG, Bito H, Morris RG (2010) Synaptic tagging and capture: differential role of distinct calcium/calmodulin kinases in protein synthesis-dependent long-term potentiation. J Neurosci 30:4981–4989
Roberson ED, English JD, Adams JP, Selcher JC, Kondratick C, Sweatt JD (1999) The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J Neurosci 19:4337–4348
Rogerson T, Cai DJ, Frank A, Sano Y, Shobe J et al (2014) Synaptic tagging during memory allocation. Nat Rev Neurosci 15:157–169
Rosen ZB, Cheung S, Siegelbaum SA (2015) Midbrain dopamine neurons bidirectionally regulate CA3-CA1 synaptic drive. Nat Neurosci 18:1763–1771
Rossato JI, Bevilaqua LR, Izquierdo I, Medina JH, Cammarota M (2009) Dopamine controls persistence of long-term memory storage. Science 325:1017–1020
Sarinana J, Kitamura T, Kunzler P, Sultzman L, Tonegawa S (2014) Differential roles of the dopamine 1-class receptors, D1R and D5R, in hippocampal dependent memory. Proc Natl Acad Sci USA 111:8245–8250
Scatton B, Simon H, Le Moal M, Bischoff S (1980) Origin of dopaminergic innervation of the rat hippocampal formation. Neurosci Lett 18:125–131
Schott BH, Seidenbecher CI, Fenker DB, Lauer CJ, Bunzeck N et al (2006) The dopaminergic midbrain participates in human episodic memory formation: evidence from genetic imaging. J Neurosci 26:1407–1417
Schroeter S, Apparsundaram S, Wiley RG, Miner LH, Sesack SR, Blakely RD (2000) Immunolocalization of the cocaine- and antidepressant-sensitive l-norepinephrine transporter. J Comp Neurol 420:211–232
Schultz W (2007) Behavioral dopamine signals. Trends Neurosci 30:203–210
Seong J, Lin MZ (2021) Optobiochemistry: genetically encoded control of protein activity by light. Annu Rev Biochem 90:475–501
Sesack SR, Hawrylak VA, Matus C, Guido MA, Levey AI (1998) Dopamine axon varicosities in the prelimbic division of the rat prefrontal cortex exhibit sparse immunoreactivity for the dopamine transporter. J Neurosci 18:2697–2708
Shires KL, Da Silva BM, Hawthorne JP, Morris RG, Martin SJ (2012) Synaptic tagging and capture in the living rat. Nat Commun 3:1246
Smith CC, Greene RW (2012) CNS dopamine transmission mediated by noradrenergic innervation. J Neurosci 32:6072–6080
Smith DR, Striplin CD, Geller AM, Mailman RB, Drago J et al (1998) Behavioural assessment of mice lacking D1A dopamine receptors. Neuroscience 86:135–146
Smith WB, Starck SR, Roberts RW, Schuman EM (2005) Dopaminergic stimulation of local protein synthesis enhances surface expression of GluR1 and synaptic transmission in hippocampal neurons. Neuron 45:765–779
Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195–231
Squire LR, Genzel L, Wixted JT, Morris RG (2015) Memory consolidation. Cold Spring Harb Perspect Biol 7:a021766
Sun F, Zhou J, Dai B, Qian T, Zeng J et al (2020) Next-generation GRAB sensors for monitoring dopaminergic activity in vivo. Nat Methods 17:1156–1166
Sunahara RK, Guan HC, O’Dowd BF, Seeman P, Laurier LG et al (1991) Cloning of the gene for a human dopamine D5 receptor with higher affinity for dopamine than D1. Nature 350:614–619
Swanson LW, Cowan WM (1977) An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 172:49–84
Swanson LW, Hartman BK (1975) The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta-hydroxylase as a marker. J Comp Neurol 163:467–505
Swanson-Park JL, Coussens CM, Mason-Parker SE, Raymond CR, Hargreaves EL et al (1999) A double dissociation within the hippocampus of dopamine D1/D5 receptor and beta-adrenergic receptor contributions to the persistence of long-term potentiation. Neuroscience 92:485–497
Takeuchi T, Duszkiewicz AJ, Morris RGM (2013) The synaptic plasticity and memory hypothesis: encoding, storage and persistence. Philos Trans R Soc Lond B Biol Sci 369:20130288
Takeuchi T, Duszkiewicz AJ, Sonneborn A, Spooner PA, Yamasaki M et al (2016) Locus coeruleus and dopaminergic consolidation of everyday memory. Nature 537:357–362
Takeuchi T, Tamura M, Tse D, Kajii Y, Fernandez G, Morris RGM (2022) Brain region networks for the assimilation of new associative memory into a schema. Mol Brain 15:24
Tanaka J, Horiike Y, Matsuzaki M, Miyazaki T, Ellis-Davies GC, Kasai H (2008) Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 319:1683–1687
Tiberi M, Jarvie KR, Silvia C, Falardeau P, Gingrich JA et al (1991) Cloning, molecular characterization, and chromosomal assignment of a gene encoding a second D1 dopamine receptor subtype: differential expression pattern in rat brain compared with the D1A receptor. Proc Natl Acad Sci USA 88:7491–7495
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 2015:603672
Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA et al (2007) Schemas and memory consolidation. Science 316:76–82
Tse D, Takeuchi T, Kakeyama M, Kajii Y, Okuno H et al (2011) Schema-dependent gene activation. Science 333:891–895
Tsetsenis T, Badyna JK, Wilson JA, Zhang X, Krizman EN et al (2021) Midbrain dopaminergic innervation of the hippocampus is sufficient to modulate formation of aversive memories. Proc Natl Acad Sci USA 118
Tsetsenis T, Broussard JI, Dani JA (2022) Dopaminergic regulation of hippocampal plasticity, learning, and memory. Front Behav Neurosci 16:1092420
Uchigashima M, Ohtsuka T, Kobayashi K, Watanabe M (2016) Dopamine synapse is a neuroligin-2-mediated contact between dopaminergic presynaptic and GABAergic postsynaptic structures. Proc Natl Acad Sci USA 113:4206–4211
Umbriaco D, Garcia S, Beaulieu C, Descarries L (1995) Relational features of acetylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus (CA1). Hippocampus 5:605–620
van de Ven GM, Trouche S, McNamara CG, Allen K, Dupret D (2016) Hippocampal offline reactivation consolidates recently formed cell assembly patterns during sharp wave-ripples. Neuron 92:968–974
Vazdarjanova A, Guzowski JF (2004) Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J Neurosci 24:6489–6496
Vazdarjanova A, McNaughton BL, Barnes CA, Worley PF, Guzowski JF (2002) Experience-dependent coincident expression of the effector immediate-early genes arc and Homer 1a in hippocampal and neocortical neuronal networks. J Neurosci 22:10067–10071
Vianna MR, Alonso M, Viola H, Quevedo J, de Paris F et al (2000) Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat. Learn Mem 7:333–340
Wagatsuma A, Okuyama T, Sun C, Smith LM, Abe K, Tonegawa S (2018) Locus coeruleus input to hippocampal CA3 drives single-trial learning of a novel context. Proc Natl Acad Sci USA 115:E310–E316
Wang SH, Redondo RL, Morris RG (2010) Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory. Proc Natl Acad Sci USA 107:19537–19542
Weitemier AZ, McHugh TJ (2017) Noradrenergic modulation of evoked dopamine release and pH shift in the mouse dorsal hippocampus and ventral striatum. Brain Res 1657:74–86
**ng B, Kong H, Meng X, Wei SG, Xu M, Li SB (2010) Dopamine D1 but not D3 receptor is critical for spatial learning and related signaling in the hippocampus. Neuroscience 169:1511–1519
Xu ZQ, Shi TJ, Hokfelt T (1998) Galanin/GMAP- and NPY-like immunoreactivities in locus coeruleus and noradrenergic nerve terminals in the hippocampal formation and cortex with notes on the galanin-R1 and -R2 receptors. J Comp Neurol 392:227–251
Yamasaki M, Takeuchi T (2017) Locus coeruleus and dopamine-dependent memory consolidation. Neural Plast 2017:8602690
Yang Y, Liu JJ (2022) Structural LTP: signal transduction, actin cytoskeleton reorganization, and membrane remodeling of dendritic spines. Curr Opin Neurobiol 74:102534
Yoshioka W, Endo N, Kurashige A, Haijima A, Endo T et al (2012) Fluorescence laser microdissection reveals a distinct pattern of gene activation in the mouse hippocampal region. Sci Rep 2:783
Yung KK, Bolam JP, Smith AD, Hersch SM, Ciliax BJ, Levey AI (1995) Immunocytochemical localization of D1 and D2 dopamine receptors in the basal ganglia of the rat: light and electron microscopy. Neuroscience 65:709–730
Acknowledgments
This study was supported by grants from the Novo Nordisk Foundation Young Investigator Award 2017 (NNF17OC0026774), Lundbeckfonden (DANDRITE-R248-2016-2518), and the PROMEMO Center for Proteins in Memory, a Center of Excellence funded by the Danish National Research Foundation (DNRF133). I would like to thank Kristoffer Højgaard and Taichi Hiraga for their contributions to the scientific discussion. I am grateful for the support from Yasunari Koyama (KOYAMA Medical and Welfare Group), Daisaku Sawada (Sugamo Sougou Chiryoin), Shinji Adachi (DAIWA KIKO CO. LTD.), and the Tokyo Future Lions Club.
Competing Interests
No competing interests exist.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2024 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Takeuchi, T. (2024). Unlocking the Memory Vault: Dopamine, Novelty, and Memory Consolidation in the Hippocampus. In: Sajikumar, S., Abel, T. (eds) Synaptic Tagging and Capture. Springer, Cham. https://doi.org/10.1007/978-3-031-54864-2_14
Download citation
DOI: https://doi.org/10.1007/978-3-031-54864-2_14
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-54863-5
Online ISBN: 978-3-031-54864-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)