Learning, Neurogenesis and Effects of Flavonoids on Learning

Page: [355 - 364] Pages: 10

  • * (Excluding Mailing and Handling)

Abstract

Abstract: Learning and memory are two of our mind's most magical abilities. Different brain regions have roles to process and store different types of memories. The hippocampus is the part of the brain responsible for receiving information and storing it in the neocortex. One of the most impressive characteristics of the hippocampus is its capacity for neurogenesis which is a process, new neurons are produced and then transformed into mature neurons and integrated into neural circuits. The neurogenesis process in the hippocampus, an example of neuroplasticity in the adult brain, is believed to aid hippocampal-dependent learning and memory. New neurons are constantly produced in the hippocampus and integrated into the pre-existing neuronal network, this allows old memories already stored in the neocortex to be removed from the hippocampus and replaced with new ones. Factors affecting neurogenesis in the hippocampus may also affect hippocampal-dependent learning and memory. The flavonoids can exert particularly powerful actions in mammalian cognition and improve hippocampaldependent learning and memory by positively affecting hippocampal neurogenesis.

Keywords: Learning, neurogenesis, flavonoids, hippocampus, LTP, memory.

Graphical Abstract

[1]
Preston, A.R.; Eichenbaum, H. Interplay of hippocampus and prefrontal cortex in memory. Curr. Biol., 2013, 23(17), R764-R773.
[http://dx.doi.org/10.1016/j.cub.2013.05.041] [PMID: 24028960]
[2]
Lechner, H.A.; Squire, L.R.; Byrne, J.H. 100 years of consolidation remembering Müller and Pilzecker. Learn. Mem., 1999, 6(2), 77-87.
[PMID: 10327233]
[3]
Tulving, E. Episodic and Semantic Memory; Tulving, E.; Donaldson, W., Eds.; NY: Academic Press,. , 1972, pp. 381-403.
[4]
Squire, L.R.; Zola, S.M. Structure and function of declarative and nondeclarative memory systems. Proc. Natl. Acad. Sci. USA, 1996, 93(24), 13515-13522.
[http://dx.doi.org/10.1073/pnas.93.24.13515] [PMID: 8942965]
[5]
Squire, L.R.; Wixted, J.T. The cognitive neuroscience of human memory since H.M. Annu. Rev. Neurosci., 2011, 34, 259-288.
[http://dx.doi.org/10.1146/annurev-neuro-061010-113720] [PMID: 21456960]
[6]
Squire, L.R. Memory systems of the brain: A brief history and current perspective. Neurobiol. Learn. Mem., 2004, 82(3), 171-177.
[http://dx.doi.org/10.1016/j.nlm.2004.06.005] [PMID: 15464402]
[7]
Kitamura, T.; Inokuchi, K. Role of adult neurogenesis in hippocampal-cortical memory consolidation. Mol. Brain, 2014, 7, 13.
[http://dx.doi.org/10.1186/1756-6606-7-13] [PMID: 24552281]
[8]
Baram, T.Z.; Donato, F.; Holmes, G.L. Construction and disruption of spatial memory networks during development. Learn. Mem., 2019, 26(7), 206-218.
[http://dx.doi.org/10.1101/lm.049239.118] [PMID: 31209115]
[9]
D’Hooge, R.; De Deyn, P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res. Brain Res. Rev., 2001, 36(1), 60-90.
[http://dx.doi.org/10.1016/S0165-0173(01)00067-4] [PMID: 11516773]
[10]
Yau, S.Y.; So, K.F. Adult neurogenesis and dendritic remodeling in hippocampal plasticity: which one is more important? Cell Transplant., 2014, 23(4-5), 471-479.
[http://dx.doi.org/10.3727/096368914X678283] [PMID: 24636187]
[11]
McGaugh, J.L. Memory-a century of consolidation. Science, 2000, 287(5451), 248-251.
[http://dx.doi.org/10.1126/science.287.5451.248] [PMID: 10634773]
[12]
Muller, D.; Nikonenko, I.; Jourdain, P.; Alberi, S. LTP, memory and structural plasticity. Curr. Mol. Med., 2002, 2(7), 605-611.
[http://dx.doi.org/10.2174/1566524023362041] [PMID: 12420800]
[13]
Lamprecht, R.; LeDoux, J. Structural plasticity and memory. Nat. Rev. Neurosci., 2004, 5(1), 45-54.
[http://dx.doi.org/10.1038/nrn1301] [PMID: 14708003]
[14]
Malenka, R.C.; Nicoll, R.A. Long-term potentiation-a decade of progress? Science, 1999, 285(5435), 1870-1874.
[http://dx.doi.org/10.1126/science.285.5435.1870] [PMID: 10489359]
[15]
Bliss, T.V.; Collingridge, G.L. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature, 1993, 361(6407), 31-39.
[http://dx.doi.org/10.1038/361031a0] [PMID: 8421494]
[16]
Rendeiro, C.; Guerreiro, J.D.; Williams, C.M.; Spencer, J.P. Flavonoids as modulators of memory and learning: molecular interactions resulting in behavioural effects. Proc. Nutr. Soc., 2012, 71(2), 246-262.
[http://dx.doi.org/10.1017/S0029665112000146] [PMID: 22414320]
[17]
Malenka, R.C.; Bear, M.F. LTP and LTD: A n embarrassment of riches. Neuron, 2004, 44(1), 5-21.
[http://dx.doi.org/10.1016/j.neuron.2004.09.012] [PMID: 15450156]
[18]
Kandel, E.R.; Dudai, Y.; Mayford, M.R. The molecular and systems biology of memory. Cell, 2014, 157(1), 163-186.
[http://dx.doi.org/10.1016/j.cell.2014.03.001] [PMID: 24679534]
[19]
Kandel, E.R. The molecular biology of memory storage: A dialogue between genes and synapses. Science, 2001, 294(5544), 1030-1038.
[http://dx.doi.org/10.1126/science.1067020] [PMID: 11691980]
[20]
Squire, L.; Berg, D.; Bloom, F.E.; Du Lac, S.; Ghosh, A.; Spitzer, N.C. Fundamental neuroscience; Academic Press, 2012.
[21]
Kessels, H.W.; Malinow, R. Synaptic AMPA receptor plasticity and behavior. Neuron, 2009, 61(3), 340-350.
[http://dx.doi.org/10.1016/j.neuron.2009.01.015] [PMID: 19217372]
[22]
Lisman, J.; Yasuda, R.; Raghavachari, S. Mechanisms of CaMKII action in long-term potentiation. Nat. Rev. Neurosci., 2012, 13(3), 169-182.
[http://dx.doi.org/10.1038/nrn3192] [PMID: 22334212]
[23]
Granger, A.J.; Shi, Y.; Lu, W.; Cerpas, M.; Nicoll, R.A. LTP requires a reserve pool of glutamate receptors independent of subunit type. Nature, 2013, 493(7433), 495-500.
[http://dx.doi.org/10.1038/nature11775] [PMID: 23235828]
[24]
Alkon, D.L.; Sun, M.K.; Nelson, T.J. PKC signaling deficits: A mechanistic hypothesis for the origins of Alzheimer’s disease. Trends Pharmacol. Sci., 2007, 28(2), 51-60.
[http://dx.doi.org/10.1016/j.tips.2006.12.002] [PMID: 17218018]
[25]
Sweatt, J.D. The neuronal MAP kinase cascade: A biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem., 2001, 76(1), 1-10.
[http://dx.doi.org/10.1046/j.1471-4159.2001.00054.x] [PMID: 11145972]
[26]
Arnsten, A.F.; Ramos, B.P.; Birnbaum, S.G.; Taylor, J.R. Protein kinase A as a therapeutic target for memory disorders: rationale and challenges. Trends Mol. Med., 2005, 11(3), 121-128.
[http://dx.doi.org/10.1016/j.molmed.2005.01.006] [PMID: 15760770]
[27]
Impey, S.; McCorkle, S.R.; Cha-Molstad, H.; Dwyer, J.M.; Yochum, G.S.; Boss, J.M.; McWeeney, S.; Dunn, J.J.; Mandel, G.; Goodman, R.H. Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell, 2004, 119(7), 1041-1054.
[PMID: 15620361]
[28]
Kandel, E.R. The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Mol. Brain, 2012, 5, 14.
[http://dx.doi.org/10.1186/1756-6606-5-14] [PMID: 22583753]
[29]
Spencer, J.P. The impact of flavonoids on memory: physiological and molecular considerations. Chem. Soc. Rev., 2009, 38(4), 1152-1161.
[http://dx.doi.org/10.1039/b800422f] [PMID: 19421586]
[30]
Grover, L.M.; Teyler, T.J. Two components of long-term potentiation induced by different patterns of afferent activation. Nature, 1990, 347(6292), 477-479.
[http://dx.doi.org/10.1038/347477a0] [PMID: 1977084]
[31]
Mellor, J.; Nicoll, R.A. Hippocampal mossy fiber LTP is independent of postsynaptic calcium. Nat. Neurosci., 2001, 4(2), 125-126.
[http://dx.doi.org/10.1038/83941] [PMID: 11175870]
[32]
Mellor, J.; Nicoll, R.A.; Schmitz, D. Mediation of hippocampal mossy fiber long-term potentiation by presynaptic Ih channels. Science, 2002, 295(5552), 143-147.
[http://dx.doi.org/10.1126/science.1064285] [PMID: 11778053]
[33]
Suh, H.; Deng, W.; Gage, F.H. Signaling in adult neurogenesis. Annu. Rev. Cell Dev. Biol., 2009, 25, 253-275.
[http://dx.doi.org/10.1146/annurev.cellbio.042308.113256] [PMID: 19575663]
[34]
Zhao, C.; Deng, W.; Gage, F.H. Mechanisms and functional implications of adult neurogenesis. Cell, 2008, 132(4), 645-660.
[http://dx.doi.org/10.1016/j.cell.2008.01.033] [PMID: 18295581]
[35]
Spalding, K.L.; Bergmann, O.; Alkass, K.; Bernard, S.; Salehpour, M.; Huttner, H.B.; Boström, E.; Westerlund, I.; Vial, C.; Buchholz, B.A.; Possnert, G.; Mash, D.C.; Druid, H.; Frisén, J. Dynamics of hippocampal neurogenesis in adult humans. Cell, 2013, 153(6), 1219-1227.
[http://dx.doi.org/10.1016/j.cell.2013.05.002] [PMID: 23746839]
[36]
van Praag, H.; Schinder, A.F.; Christie, B.R.; Toni, N.; Palmer, T.D.; Gage, F.H. Functional neurogenesis in the adult hippocampus. Nature, 2002, 415(6875), 1030-1034.
[http://dx.doi.org/10.1038/4151030a] [PMID: 11875571]
[37]
Toni, N.; Teng, E.M.; Bushong, E.A.; Aimone, J.B.; Zhao, C.; Consiglio, A.; van Praag, H.; Martone, M.E.; Ellisman, M.H.; Gage, F.H. Synapse formation on neurons born in the adult hippocampus. Nat. Neurosci., 2007, 10(6), 727-734.
[http://dx.doi.org/10.1038/nn1908] [PMID: 17486101]
[38]
Toni, N.; Laplagne, D.A.; Zhao, C.; Lombardi, G.; Ribak, C.E.; Gage, F.H.; Schinder, A.F. Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat. Neurosci., 2008, 11(8), 901-907.
[http://dx.doi.org/10.1038/nn.2156] [PMID: 18622400]
[39]
Faulkner, R.L.; Jang, M-H.; Liu, X-B.; Duan, X.; Sailor, K.A.; Kim, J.Y.; Ge, S.; Jones, E.G.; Ming, G.L.; Song, H.; Cheng, H.J. Development of hippocampal mossy fiber synaptic outputs by new neurons in the adult brain. Proc. Natl. Acad. Sci. USA, 2008, 105(37), 14157-14162.
[http://dx.doi.org/10.1073/pnas.0806658105] [PMID: 18780780]
[40]
Li, G.; Pleasure, S.J. Ongoing interplay between the neural network and neurogenesis in the adult hippocampus. Curr. Opin. Neurobiol., 2010, 20(1), 126-133.
[http://dx.doi.org/10.1016/j.conb.2009.12.008] [PMID: 20079627]
[41]
Masiulis, I.; Yun, S.; Eisch, A.J. The interesting interplay between interneurons and adult hippocampal neurogenesis. Mol. Neurobiol., 2011, 44(3), 287-302.
[http://dx.doi.org/10.1007/s12035-011-8207-z] [PMID: 21956642]
[42]
Giachino, C.; Barz, M.; Tchorz, J.S.; Tome, M.; Gassmann, M.; Bischofberger, J.; Bettler, B.; Taylor, V. GABA suppresses neurogenesis in the adult hippocampus through GABAB receptors. Development, 2014, 141(1), 83-90.
[http://dx.doi.org/10.1242/dev.102608] [PMID: 24284211]
[43]
Overstreet Wadiche, L.; Bromberg, D.A.; Bensen, A.L.; Westbrook, G.L. GABAergic signaling to newborn neurons in dentate gyrus. J. Neurophysiol., 2005, 94(6), 4528-4532.
[http://dx.doi.org/10.1152/jn.00633.2005] [PMID: 16033936]
[44]
Ge, S.; Goh, E.L.; Sailor, K.A.; Kitabatake, Y.; Ming, G.L.; Song, H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature, 2006, 439(7076), 589-593.
[http://dx.doi.org/10.1038/nature04404] [PMID: 16341203]
[45]
Tashiro, A.; Sandler, V.M.; Toni, N.; Zhao, C.; Gage, F.H. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature, 2006, 442(7105), 929-933.
[http://dx.doi.org/10.1038/nature05028] [PMID: 16906136]
[46]
Tashiro, A.; Makino, H.; Gage, F.H. Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J. Neurosci., 2007, 27(12), 3252-3259.
[http://dx.doi.org/10.1523/JNEUROSCI.4941-06.2007] [PMID: 17376985]
[47]
Brown, J.; Cooper-Kuhn, C.M.; Kempermann, G.; Van Praag, H.; Winkler, J.; Gage, F.H.; Kuhn, H.G. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci., 2003, 17(10), 2042-2046.
[http://dx.doi.org/10.1046/j.1460-9568.2003.02647.x] [PMID: 12786970]
[48]
Stranahan, A.M.; Khalil, D.; Gould, E. Running induces widespread structural alterations in the hippocampus and entorhinal cortex. Hippocampus, 2007, 17(11), 1017-1022.
[http://dx.doi.org/10.1002/hipo.20348] [PMID: 17636549]
[49]
Redila, V.A.; Christie, B.R. Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus. Neuroscience, 2006, 137(4), 1299-1307.
[http://dx.doi.org/10.1016/j.neuroscience.2005.10.050] [PMID: 16338077]
[50]
Cameron, H.A.; McKay, R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol., 2001, 435(4), 406-417.
[http://dx.doi.org/10.1002/cne.1040] [PMID: 11406822]
[51]
Ramirez-Amaya, V.; Marrone, D.F.; Gage, F.H.; Worley, P.F.; Barnes, C.A. Integration of new neurons into functional neural networks. J. Neurosci., 2006, 26(47), 12237-12241.
[http://dx.doi.org/10.1523/JNEUROSCI.2195-06.2006] [PMID: 17122048]
[52]
Leuner, B.; Gould, E.; Shors, T.J. Is there a link between adult neurogenesis and learning? Hippocampus, 2006, 16(3), 216-224.
[http://dx.doi.org/10.1002/hipo.20153] [PMID: 16421862]
[53]
Marín-Burgin, A.; Schinder, A.F. Requirement of adult-born neurons for hippocampus-dependent learning. Behav. Brain Res., 2012, 227(2), 391-399.
[http://dx.doi.org/10.1016/j.bbr.2011.07.001] [PMID: 21763727]
[54]
Deng, W.; Aimone, J.B.; Gage, F.H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci., 2010, 11(5), 339-350.
[http://dx.doi.org/10.1038/nrn2822] [PMID: 20354534]
[55]
Kuhn, H.G.; Dickinson-Anson, H.; Gage, F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci., 1996, 16(6), 2027-2033.
[http://dx.doi.org/10.1523/JNEUROSCI.16-06-02027.1996] [PMID: 8604047]
[56]
Anacker, C.; Hen, R. Adult hippocampal neurogenesis and cognitive flexibility - linking memory and mood. Nat. Rev. Neurosci., 2017, 18(6), 335-346.
[http://dx.doi.org/10.1038/nrn.2017.45] [PMID: 28469276]
[57]
Atallah, H.E.; Frank, M.J.; O’Reilly, R.C. Hippocampus, cortex, and basal ganglia: insights from computational models of complementary learning systems. Neurobiol. Learn. Mem., 2004, 82(3), 253-267.
[http://dx.doi.org/10.1016/j.nlm.2004.06.004] [PMID: 15464408]
[58]
Bakker, A.; Kirwan, C.B.; Miller, M.; Stark, C.E. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science, 2008, 319(5870), 1640-1642.
[http://dx.doi.org/10.1126/science.1152882] [PMID: 18356518]
[59]
Clelland, C.D.; Choi, M.; Romberg, C.; Clemenson, G.D., Jr; Fragniere, A.; Tyers, P.; Jessberger, S.; Saksida, L.M.; Barker, R.A.; Gage, F.H.; Bussey, T.J. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science, 2009, 325(5937), 210-213.
[http://dx.doi.org/10.1126/science.1173215] [PMID: 19590004]
[60]
Gilbert, P.E.; Kesner, R.P.; Lee, I. Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1. Hippocampus, 2001, 11(6), 626-636.
[http://dx.doi.org/10.1002/hipo.1077] [PMID: 11811656]
[61]
Nakashiba, T.; Young, J.Z.; McHugh, T.J.; Buhl, D.L.; Tonegawa, S. Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning. Science, 2008, 319(5867), 1260-1264.
[http://dx.doi.org/10.1126/science.1151120] [PMID: 18218862]
[62]
Aimone, J.B.; Wiles, J.; Gage, F.H. Computational influence of adult neurogenesis on memory encoding. Neuron, 2009, 61(2), 187-202.
[http://dx.doi.org/10.1016/j.neuron.2008.11.026] [PMID: 19186162]
[63]
Lin, C.C.; Huang, T.L. Brain-derived neurotrophic factor and mental disorders. Biomed. J., 2020, 43(2), 134-142.
[http://dx.doi.org/10.1016/j.bj.2020.01.001] [PMID: 32386841]
[64]
Barde, Y-A. Trophic factors and neuronal survival. Neuron, 1989, 2(6), 1525-1534.
[http://dx.doi.org/10.1016/0896-6273(89)90040-8] [PMID: 2697237]
[65]
Egan, M.F.; Kojima, M.; Callicott, J.H.; Goldberg, T.E.; Kolachana, B.S.; Bertolino, A.; Zaitsev, E.; Gold, B.; Goldman, D.; Dean, M.; Lu, B.; Weinberger, D.R. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell, 2003, 112(2), 257-269.
[http://dx.doi.org/10.1016/S0092-8674(03)00035-7] [PMID: 12553913]
[66]
Nagahara, A.H.; Merrill, D.A.; Coppola, G.; Tsukada, S.; Schroeder, B.E.; Shaked, G.M.; Wang, L.; Blesch, A.; Kim, A.; Conner, J.M.; Rockenstein, E.; Chao, M.V.; Koo, E.H.; Geschwind, D.; Masliah, E.; Chiba, A.A.; Tuszynski, M.H. Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer’s disease. Nat. Med., 2009, 15(3), 331-337.
[http://dx.doi.org/10.1038/nm.1912] [PMID: 19198615]
[67]
Vilar, M.; Mira, H. Regulation of neurogenesis by neurotrophins during adulthood: expected and unexpected roles. Front. Neurosci., 2016, 10, 26.
[http://dx.doi.org/10.3389/fnins.2016.00026] [PMID: 26903794]
[68]
Nagahara, A.H.; Mateling, M.; Kovacs, I.; Wang, L.; Eggert, S.; Rockenstein, E.; Koo, E.H.; Masliah, E.; Tuszynski, M.H. Early BDNF treatment ameliorates cell loss in the entorhinal cortex of APP transgenic mice. J. Neurosci., 2013, 33(39), 15596-15602.
[http://dx.doi.org/10.1523/JNEUROSCI.5195-12.2013] [PMID: 24068826]
[69]
Scharfman, H.; Goodman, J.; Macleod, A.; Phani, S.; Antonelli, C.; Croll, S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol., 2005, 192(2), 348-356.
[http://dx.doi.org/10.1016/j.expneurol.2004.11.016] [PMID: 15755552]
[70]
Kaptan, Z.; Akgün-Dar, K.; Kapucu, A.; Dedeakayoğulları, H.; Batu, Ş.; Üzüm, G. Long term consequences on spatial learning-memory of low-calorie diet during adolescence in female rats; hippocampal and prefrontal cortex BDNF level, expression of NeuN and cell proliferation in dentate gyrus. Brain Res., 2015, 1618, 194-204.
[http://dx.doi.org/10.1016/j.brainres.2015.05.041] [PMID: 26072462]
[71]
Russo-Neustadt, A.A.; Alejandre, H.; Garcia, C.; Ivy, A.S.; Chen, M.J. Hippocampal brain-derived neurotrophic factor expression following treatment with reboxetine, citalopram, and physical exercise. Neuropsychopharmacology, 2004, 29(12), 2189-2199.
[http://dx.doi.org/10.1038/sj.npp.1300514] [PMID: 15199375]
[72]
Rossi, C.; Angelucci, A.; Costantin, L.; Braschi, C.; Mazzantini, M.; Babbini, F.; Fabbri, M.E.; Tessarollo, L.; Maffei, L.; Berardi, N.; Caleo, M. Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur. J. Neurosci., 2006, 24(7), 1850-1856.
[http://dx.doi.org/10.1111/j.1460-9568.2006.05059.x] [PMID: 17040481]
[73]
Erickson, K.I.; Miller, D.L.; Roecklein, K.A. The aging hippocampus: interactions between exercise, depression, and BDNF. Neuroscientist, 2012, 18(1), 82-97.
[http://dx.doi.org/10.1177/1073858410397054] [PMID: 21531985]
[74]
Duman, R.S. Role of neurotrophic factors in the etiology and treatment of mood disorders. Neuromolecular Med., 2004, 5(1), 11-25.
[http://dx.doi.org/10.1385/NMM:5:1:011] [PMID: 15001809]
[75]
Kaplan, D.R.; Miller, F.D. Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol., 2000, 10(3), 381-391.
[http://dx.doi.org/10.1016/S0959-4388(00)00092-1] [PMID: 10851172]
[76]
Huang, E.J.; Reichardt, L.F. Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem., 2003, 72(1), 609-642.
[http://dx.doi.org/10.1146/annurev.biochem.72.121801.161629] [PMID: 12676795]
[77]
Bekinschtein, P.; Cammarota, M.; Katche, C.; Slipczuk, L.; Rossato, J.I.; Goldin, A.; Izquierdo, I.; Medina, J.H. BDNF is essential to promote persistence of long-term memory storage. Proc. Natl. Acad. Sci. USA, 2008, 105(7), 2711-2716.
[http://dx.doi.org/10.1073/pnas.0711863105] [PMID: 18263738]
[78]
Wu, H.; Lu, D.; Jiang, H.; Xiong, Y.; Qu, C.; Li, B.; Mahmood, A.; Zhou, D.; Chopp, M. Simvastatin-mediated upregulation of VEGF and BDNF, activation of the PI3K/Akt pathway, and increase of neurogenesis are associated with therapeutic improvement after traumatic brain injury. J. Neurotrauma, 2008, 25(2), 130-139.
[http://dx.doi.org/10.1089/neu.2007.0369] [PMID: 18260796]
[79]
Kelly, A.; Laroche, S.; Davis, S. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory. J. Neurosci., 2003, 23(12), 5354-5360.
[http://dx.doi.org/10.1523/JNEUROSCI.23-12-05354.2003] [PMID: 12832561]
[80]
Riccio, A.; Alvania, R.S.; Lonze, B.E.; Ramanan, N.; Kim, T.; Huang, Y.; Dawson, T.M.; Snyder, S.H.; Ginty, D.D. A nitric oxide signaling pathway controls CREB-mediated gene expression in neurons. Mol. Cell, 2006, 21(2), 283-294.
[http://dx.doi.org/10.1016/j.molcel.2005.12.006] [PMID: 16427017]
[81]
Callaghan, C.K.; Kelly, Á.M. Differential BDNF signaling in dentate gyrus and perirhinal cortex during consolidation of recognition memory in the rat. Hippocampus, 2012, 22(11), 2127-2135.
[http://dx.doi.org/10.1002/hipo.22033] [PMID: 22573708]
[82]
Schratt, G.M.; Nigh, E.A.; Chen, W.G.; Hu, L.; Greenberg, M.E. BDNF regulates the translation of a select group of mRNAs by a mammalian target of rapamycin-phosphatidylinositol 3-kinase-dependent pathway during neuronal development. J. Neurosci., 2004, 24(33), 7366-7377.
[http://dx.doi.org/10.1523/JNEUROSCI.1739-04.2004] [PMID: 15317862]
[83]
Jiao, J.; Huang, X.; Feit-Leithman, R.A.; Neve, R.L.; Snider, W.; Dartt, D.A.; Chen, D.F. Bcl-2 enhances Ca(2+) signaling to support the intrinsic regenerative capacity of CNS axons. EMBO J., 2005, 24(5), 1068-1078.
[http://dx.doi.org/10.1038/sj.emboj.7600589] [PMID: 15719013]
[84]
Manach, C.; Scalbert, A.; Morand, C.; Rémésy, C.; Jiménez, L. Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr., 2004, 79(5), 727-747.
[http://dx.doi.org/10.1093/ajcn/79.5.727] [PMID: 15113710]
[85]
Spencer, J.P. Food for thought: the role of dietary flavonoids in enhancing human memory, learning and neuro-cognitive performance. Proc. Nutr. Soc., 2008, 67(2), 238-252.
[http://dx.doi.org/10.1017/S0029665108007088] [PMID: 18412998]
[86]
Vauzour, D.; Vafeiadou, K.; Rodriguez-Mateos, A.; Rendeiro, C.; Spencer, J.P. The neuroprotective potential of flavonoids: a multiplicity of effects. Genes Nutr., 2008, 3(3-4), 115-126.
[http://dx.doi.org/10.1007/s12263-008-0091-4] [PMID: 18937002]
[87]
Spencer, J.P. Flavonoids and brain health: multiple effects underpinned by common mechanisms. Genes Nutr., 2009, 4(4), 243-250.
[http://dx.doi.org/10.1007/s12263-009-0136-3] [PMID: 19685255]
[88]
Spencer, J.P.; Vauzour, D.; Rendeiro, C. Flavonoids and cognition: the molecular mechanisms underlying their behavioural effects. Arch. Biochem. Biophys., 2009, 492(1-2), 1-9.
[http://dx.doi.org/10.1016/j.abb.2009.10.003] [PMID: 19822127]
[89]
Mandel, S.; Weinreb, O.; Amit, T.; Youdim, M.B. Cell signaling pathways in the neuroprotective actions of the green tea polyphenol (-)-epigallocatechin-3-gallate: implications for neurodegenerative diseases. J. Neurochem., 2004, 88(6), 1555-1569.
[http://dx.doi.org/10.1046/j.1471-4159.2003.02291.x] [PMID: 15009657]
[90]
An, L.; Zhang, Y-Z.; Yu, N-J.; Liu, X-M.; Zhao, N.; Yuan, L.; Chen, H-X.; Li, Y-F. The total flavonoids extracted from Xiaobuxin-Tang up-regulate the decreased hippocampal neurogenesis and neurotrophic molecules expression in chronically stressed rats. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2008, 32(6), 1484-1490.
[http://dx.doi.org/10.1016/j.pnpbp.2008.05.005] [PMID: 18547700]
[91]
Yao, R.; Zhang, L.; Li, X.; Li, L. Effects of Epimedium flavonoids on proliferation and differentiation of neural stem cells in vitro. Neurol. Res., 2010, 32(7), 736-742.
[http://dx.doi.org/10.1179/174313209X459183] [PMID: 19703337]
[92]
Schneider, C.; Segre, T. Green tea: potential health benefits. Am. Fam. Physician, 2009, 79(7), 591-594.
[PMID: 19378876]
[93]
Pervin, M.; Unno, K.; Takagaki, A.; Isemura, M.; Nakamura, Y. Function of green tea catechins in the brain: Epigallocatechin gallate and its metabolites. Int. J. Mol. Sci., 2019, 20(15), 3630.
[http://dx.doi.org/10.3390/ijms20153630] [PMID: 31349535]
[94]
Kim, H-S.; Quon, M.J.; Kim, J.A. New insights into the mechanisms of polyphenols beyond antioxidant properties; lessons from the green tea polyphenol, epigallocatechin 3-gallate. Redox Biol., 2014, 2, 187-195.
[http://dx.doi.org/10.1016/j.redox.2013.12.022] [PMID: 24494192]
[95]
Levites, Y.; Amit, T.; Youdim, M.B.; Mandel, S. Involvement of protein kinase C activation and cell survival/cell cycle genes in green tea polyphenol (-)-epigallocatechin 3-gallate neuroprotective action. J. Biol. Chem., 2002, 277(34), 30574-30580.
[http://dx.doi.org/10.1074/jbc.M202832200] [PMID: 12058035]
[96]
Levites, Y.; Amit, T.; Mandel, S.; Youdim, M.B. Neuroprotection and neurorescue against Abeta toxicity and PKC-dependent release of nonamyloidogenic soluble precursor protein by green tea polyphenol (-)-epigallocatechin-3-gallate. FASEB J., 2003, 17(8), 952-954.
[http://dx.doi.org/10.1096/fj.02-0881fje] [PMID: 12670874]
[97]
Menard, C.; Bastianetto, S.; Quirion, R. Neuroprotective effects of resveratrol and epigallocatechin gallate polyphenols are mediated by the activation of protein kinase C gamma. Front. Cell. Neurosci., 2013, 7, 281.
[http://dx.doi.org/10.3389/fncel.2013.00281] [PMID: 24421757]
[98]
Seong, K-J.; Lee, H-G.; Kook, M.S.; Ko, H-M.; Jung, J-Y.; Kim, W-J. Epigallocatechin-3-gallate rescues LPS-impaired adult hippocampal neurogenesis through suppressing the TLR4-NF-κB signaling pathway in mice. Korean J. Physiol. Pharmacol., 2016, 20(1), 41-51.
[http://dx.doi.org/10.4196/kjpp.2016.20.1.41] [PMID: 26807022]
[99]
Yoo, K.Y.; Choi, J.H.; Hwang, I.K.; Lee, C.H.; Lee, S.O.; Han, S.M.; Shin, H.C.; Kang, I.J.; Won, M.H. (-)-Epigallocatechin-3-gallate increases cell proliferation and neuroblasts in the subgranular zone of the dentate gyrus in adult mice. Phytother. Res., 2010, 24(7), 1065-1070.
[http://dx.doi.org/10.1002/ptr.3083] [PMID: 20013823]
[100]
Guedj, F.; Sébrié, C.; Rivals, I.; Ledru, A.; Paly, E.; Bizot, J.C.; Smith, D.; Rubin, E.; Gillet, B.; Arbones, M.; Delabar, J.M. Green tea polyphenols rescue of brain defects induced by overexpression of DYRK1A. PLoS One, 2009, 4(2)e4606
[http://dx.doi.org/10.1371/journal.pone.0004606] [PMID: 19242551]
[101]
Ortiz-López, L.; Márquez-Valadez, B.; Gómez-Sánchez, A.; Silva-Lucero, M.D.; Torres-Pérez, M.; Téllez-Ballesteros, R.I.; Ichwan, M.; Meraz-Ríos, M.A.; Kempermann, G.; Ramírez-Rodríguez, G.B. Green tea compound epigallo-catechin-3-gallate (EGCG) increases neuronal survival in adult hippocampal neurogenesis in vivo and in vitro. Neuroscience, 2016, 322, 208-220.
[http://dx.doi.org/10.1016/j.neuroscience.2016.02.040] [PMID: 26917271]
[102]
Lee, M.J.; Maliakal, P.; Chen, L.; Meng, X.; Bondoc, F.Y.; Prabhu, S.; Lambert, G.; Mohr, S.; Yang, C.S. Pharmacokinetics of tea catechins after ingestion of green tea and (-)-epigallocatechin-3-gallate by humans: formation of different metabolites and individual variability. Cancer Epidemiol. Biomarkers Prev., 2002, 11(10 Pt 1), 1025-1032.
[PMID: 12376503]
[103]
Stagni, F.; Giacomini, A.; Emili, M.; Trazzi, S.; Guidi, S.; Sassi, M.; Ciani, E.; Rimondini, R.; Bartesaghi, R. Short- and long-term effects of neonatal pharmacotherapy with epigallocatechin-3-gallate on hippocampal development in the Ts65Dn mouse model of Down syndrome. Neuroscience, 2016, 333, 277-301.
[http://dx.doi.org/10.1016/j.neuroscience.2016.07.031] [PMID: 27457036]
[104]
Li, Q.; Zhao, H.F.; Zhang, Z.F.; Liu, Z.G.; Pei, X.R.; Wang, J.B.; Cai, M.Y.; Li, Y. Long-term administration of green tea catechins prevents age-related spatial learning and memory decline in C57BL/6 J mice by regulating hippocampal cyclic amp-response element binding protein signaling cascade. Neuroscience, 2009, 159(4), 1208-1215.
[http://dx.doi.org/10.1016/j.neuroscience.2009.02.008] [PMID: 19409206]
[105]
Jang, S-W.; Liu, X.; Yepes, M.; Shepherd, K.R.; Miller, G.W.; Liu, Y.; Wilson, W.D.; Xiao, G.; Blanchi, B.; Sun, Y.E.; Ye, K. A selective TrkB agonist with potent neurotrophic activities by 7,8-dihydroxyflavone. Proc. Natl. Acad. Sci. USA, 2010, 107(6), 2687-2692.
[http://dx.doi.org/10.1073/pnas.0913572107] [PMID: 20133810]
[106]
Liu, X.; Obianyo, O.; Chan, C.B.; Huang, J.; Xue, S.; Yang, J.J.; Zeng, F.; Goodman, M.; Ye, K. Biochemical and biophysical investigation of the brain-derived neurotrophic factor mimetic 7,8-dihydroxyflavone in the binding and activation of the TrkB receptor. J. Biol. Chem., 2014, 289(40), 27571-27584.
[http://dx.doi.org/10.1074/jbc.M114.562561] [PMID: 25143381]
[107]
Liu, X.; Qi, Q.; Xiao, G.; Li, J.; Luo, H.R.; Ye, K. O-methylated metabolite of 7,8-dihydroxyflavone activates TrkB receptor and displays antidepressant activity. Pharmacology, 2013, 91(3-4), 185-200.
[http://dx.doi.org/10.1159/000346920] [PMID: 23445871]
[108]
Liu, X.; Chan, C-B.; Jang, S-W.; Pradoldej, S.; Huang, J.; He, K.; Phun, L.H.; France, S.; Xiao, G.; Jia, Y.; Luo, H.R.; Ye, K. A synthetic 7,8-dihydroxyflavone derivative promotes neurogenesis and exhibits potent antidepressant effect. J. Med. Chem., 2010, 53(23), 8274-8286.
[http://dx.doi.org/10.1021/jm101206p] [PMID: 21073191]
[109]
Stagni, F.; Giacomini, A.; Guidi, S.; Emili, M.; Uguagliati, B.; Salvalai, M.E.; Bortolotto, V.; Grilli, M.; Rimondini, R.; Bartesaghi, R. A flavonoid agonist of the TrkB receptor for BDNF improves hippocampal neurogenesis and hippocampus-dependent memory in the Ts65Dn mouse model of DS.. Exp. Neurol., 2017,298(Pt A), 79-96.,
[http://dx.doi.org/10.1016/j.expneurol.2017.08.018] [PMID: 28882412]
[110]
Giacomini, A.; Stagni, F.; Emili, M.; Uguagliati, B.; Rimondini, R.; Bartesaghi, R.; Guidi, S. Timing of treatment with the flavonoid 7, 8-DHF critically impacts on its effects on learning and memory in the Ts65Dn mouse. Antioxidants, 2019, 8(6), 163.
[http://dx.doi.org/10.3390/antiox8060163] [PMID: 31174258]
[111]
Lu, L.; Guo, Q.; Zhao, L. Overview of Oroxylin A: A Promising Flavonoid Compound. Phytother. Res., 2016, 30(11), 1765-1774.
[http://dx.doi.org/10.1002/ptr.5694] [PMID: 27539056]
[112]
Lee, S.; Kim, D.H.; Lee, D.H.; Jeon, S.J.; Lee, C.H.; Son, K.H.; Jung, J.W.; Shin, C.Y.; Ryu, J.H.; Oroxylin, A. Oroxylin A, a flavonoid, stimulates adult neurogenesis in the hippocampal dentate gyrus region of mice. Neurochem. Res., 2010, 35(11), 1725-1732.
[http://dx.doi.org/10.1007/s11064-010-0235-y] [PMID: 20680459]
[113]
Jeon, S.J.; Rhee, S.Y.; Seo, J.E.; Bak, H.R.; Lee, S.H.; Ryu, J.H.; Cheong, J.H.; Shin, C.Y.; Kim, G-H.; Lee, Y.S.; Ko, K.H. Oroxylin A increases BDNF production by activation of MAPK-CREB pathway in rat primary cortical neuronal culture. Neurosci. Res., 2011, 69(3), 214-222.
[http://dx.doi.org/10.1016/j.neures.2010.11.008] [PMID: 21145362]
[114]
Balamurugan, K.; Karthikeyan, J. Evaluation of the antioxidant and anti-inflammatory nature of luteolin in experimentally induced hepatocellular carcinoma. Biomedicine & Preventive Nutrition, 2012, 2(2), 86-90.
[http://dx.doi.org/10.1016/j.bionut.2012.01.002]
[115]
Yoo, D.Y.; Choi, J.H.; Kim, W.; Nam, S.M.; Jung, H.Y.; Kim, J.H.; Won, M-H.; Yoon, Y.S.; Hwang, I.K. Effects of luteolin on spatial memory, cell proliferation, and neuroblast differentiation in the hippocampal dentate gyrus in a scopolamine-induced amnesia model. Neurol. Res., 2013, 35(8), 813-820.
[http://dx.doi.org/10.1179/1743132813Y.0000000217] [PMID: 23651687]
[116]
Zhou, W-B.; Miao, Z-N.; Zhang, B.; Long, W.; Zheng, F-X.; Kong, J.; Yu, B. Luteolin induces hippocampal neurogenesis in the Ts65Dn mouse model of Down syndrome. Neural Regen. Res., 2019, 14(4), 613-620.
[http://dx.doi.org/10.4103/1673-5374.248519] [PMID: 30632501]
[117]
Zhuang, P.W.; Cui, G.Z.; Zhang, Y.J.; Zhang, M.X.; Guo, H.; Zhang, J.B.; Lu, Z.Q.; Isaiah, A.O.; Lin, Y.X. Baicalin regulates neuronal fate decision in neural stem/progenitor cells and stimulates hippocampal neurogenesis in adult rats. CNS Neurosci. Ther., 2013, 19(3), 154-162.
[http://dx.doi.org/10.1111/cns.12050] [PMID: 23302221]
[118]
Maher, P.; Akaishi, T.; Abe, K. Flavonoid fisetin promotes ERK-dependent long-term potentiation and enhances memory. Proc. Natl. Acad. Sci. USA, 2006, 103(44), 16568-16573.
[http://dx.doi.org/10.1073/pnas.0607822103] [PMID: 17050681]
[119]
Perez-Rando, M.; Castillo-Gomez, E.; Bueno-Fernandez, C.; Nacher, J. The TrkB agonist 7,8-dihydroxyflavone changes the structural dynamics of neocortical pyramidal neurons and improves object recognition in mice. Brain Struct. Funct., 2018, 223(5), 2393-2408.
[http://dx.doi.org/10.1007/s00429-018-1637-x] [PMID: 29500536]
[120]
Pu, F.; Mishima, K.; Irie, K.; Motohashi, K.; Tanaka, Y.; Orito, K.; Egawa, T.; Kitamura, Y.; Egashira, N.; Iwasaki, K.; Fujiwara, M. Neuroprotective effects of quercetin and rutin on spatial memory impairment in an 8-arm radial maze task and neuronal death induced by repeated cerebral ischemia in rats. J. Pharmacol. Sci., 2007, 104(4), 329-334.
[http://dx.doi.org/10.1254/jphs.FP0070247] [PMID: 17666865]
[121]
Akaishi, T.; Morimoto, T.; Shibao, M.; Watanabe, S.; Sakai-Kato, K.; Utsunomiya-Tate, N.; Abe, K. Structural requirements for the flavonoid fisetin in inhibiting fibril formation of amyloid β protein. Neurosci. Lett., 2008, 444(3), 280-285.
[http://dx.doi.org/10.1016/j.neulet.2008.08.052] [PMID: 18761054]
[122]
Qiu, T.; Wu, D.; Yang, L.; Ye, H.; Wang, Q.; Cao, Z.; Tang, K. Exploring the mechanism of flavonoids through systematic bioinformatics analysis. Front. Pharmacol., 2018, 9, 918.
[http://dx.doi.org/10.3389/fphar.2018.00918] [PMID: 30158870]