Cited by 281Neurogenesis and neuroplasticity mechanismsNeuroscience and Neuropharmacology ResearchNeuroinflammation and Neurodegeneration Mechanisms

Exploring the Role of Neuroplasticity in Development, Aging, and Neurodegeneration

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Marzola, Patrícia, Melzer, Thayza, Pavesi, Eloisa, Gil-Mohapel, Joana, Brocardo, Patricia S.·2023·Brain Sciences

Abstract

Neuroplasticity refers to the ability of the brain to reorganize and modify its neural connections in response to environmental stimuli, experience, learning, injury, and disease processes. It encompasses a range of mechanisms, including changes in synaptic strength and connectivity, the formation of new synapses, alterations in the structure and function of neurons, and the generation of new neurons. Neuroplasticity plays a crucial role in developing and maintaining brain function, including learning and memory, as well as in recovery from brain injury and adaptation to environmental changes. In this review, we explore the vast potential of neuroplasticity in various aspects of brain function across the lifespan and in the context of disease. Changes in the aging brain and the significance of neuroplasticity in maintaining cognitive function later in life will also be reviewed. Finally, we will discuss common mechanisms associated with age-related neurodegenerative processes (including protein aggregation and accumulation, mitochondrial dysfunction, oxidative stress, and neuroinflammation) and how these processes can be mitigated, at least partially, by non-invasive and non-pharmacologic lifestyle interventions aimed at promoting and harnessing neuroplasticity.

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  • Brain regions critically involved in cognition, such as the hippocampus, amygdala, and prefrontal cortex, are especially vulnerable in AD.

    “Brain regions critically involved in cognition, such as the hippocampus, amygdala, and prefrontal cortex, are especially vulnerable [84].”

    From Toward a Unified Framework in Molecular Neurobiology of Alzheimer’s Disease: Revisiting the Pathophysiological Hypotheses (2026) · cites this paper as [84]

    Section 4.3 says the hippocampus is particularly affected by aging, and Section 4.1 says aging particularly affects the hippocampus and cerebral cortex while increasing the risk of AD. Neither passage establishes that the hippocampus, amygdala, and prefrontal cortex are all especially vulnerable in AD; the discussion of the amygdala and prefrontal cortex in Section 3.3 concerns adolescence. (LLM, conf=0.82)

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  1. [2]Konorski J. Conditioned Reflexes and Neuron Organization, Facsimile Reprint of the 1948 Cambridge University Press Cambridge, UK 1968
  2. [3]Voss P. Thomas M.E. Cisneros-Franco J.M. de Villers-Sidani É. Dynamic Brains and the Changing Rules of Neuroplasticity: Implications for Learning and Recovery Front. Psychol. 2017 8 1657 10.3389/fpsyg.2017.01657 29085312 PMC5649212 · DOI
  3. [5]Frizzell T.O. Phull E. Khan M. Song X. Grajauskas L.A. Gawryluk J. D’Arcy R.C.N. Imaging Functional Neuroplasticity in Human White Matter Tracts Brain Struct. Funct. 2022 227 381 392 10.1007/s00429-021-02407-4 34812936 PMC8741691 · DOI
  4. [6]Leuner B. Gould E. Structural Plasticity and Hippocampal Function Annu. Rev. Psychol. 2010 61 111 140 10.1146/annurev.psych.093008.100359 19575621 PMC3012424 · DOI
  5. [7]Chen X. Zhou X. Yang L. Miao X. Lu D.-H. Yang X.-Y. Zhou Z.-B. Kang W.-B. Chen K.-Y. Zhou L.-H. Neonatal Exposure to Low-Dose (1.2%) Sevoflurane Increases Rats’ Hippocampal Neurogenesis and Synaptic Plasticity in Later Life Neurotox. Res. 2018 34 188 197 10.1007/s12640-018-9877-3 29427282 · DOI
  6. [8]Garthe A. Roeder I. Kempermann G. Mice in an Enriched Environment Learn More Flexibly Because of Adult Hippocampal Neurogenesis Hippocampus 2016 26 261 271 10.1002/hipo.22520 26311488 PMC5049654 · DOI
  7. [9]Kempermann G. Song H. Gage F.H. Neurogenesis in the Adult Hippocampus Cold Spring Harb. Perspect. Biol. 2015 7 a018812 10.1101/cshperspect.a018812 26330519 PMC4563705 · DOI · Paper page
  8. [10]Takeuchi N. Izumi S.-I. Rehabilitation with Poststroke Motor Recovery: A Review with a Focus on Neural Plasticity Stroke Res. Treat. 2013 2013 128641 10.1155/2013/128641 23738231 PMC3659508 · DOI
  9. [12]Jurkowski M.P. Bettio L. Woo E.K. Patten A. Yau S.-Y. Gil-Mohapel J. Beyond the Hippocampus and the SVZ: Adult Neurogenesis Throughout the Brain Front. Cell. Neurosci. 2020 14 576444 10.3389/fncel.2020.576444 33132848 PMC7550688 · DOI
  10. [13]Zhao C. Deng W. Gage F.H. Mechanisms and Functional Implications of Adult Neurogenesis Cell 2008 132 645 660 10.1016/j.cell.2008.01.033 18295581 · DOI · Paper page
  11. [14]Kempermann G. Kuhn H.G. Gage F.H. More Hippocampal Neurons in Adult Mice Living in an Enriched Environment Nature 1997 386 493 495 10.1038/386493a0 9087407 · DOI
  12. [15]Lazarov O. Mattson M.P. Peterson D.A. Pimplikar S.W. van Praag H. When Neurogenesis Encounters Aging and Disease Trends Neurosci. 2010 33 569 579 10.1016/j.tins.2010.09.003 20961627 PMC2981641 · DOI
  13. [18]Yang G. Pan F. Gan W.-B. Stably Maintained Dendritic Spines Are Associated with Lifelong Memories Nature 2009 462 920 924 10.1038/nature08577 19946265 PMC4724802 · DOI · Paper page
  14. [19]Bliss T.V.P. Collingridge G.L. A Synaptic Model of Memory: Long-Term Potentiation in the Hippocampus Nature 1993 361 31 39 10.1038/361031a0 8421494 · DOI · Paper page
  15. [20]Bear M.F. Malenka R.C. Synaptic Plasticity: LTP and LTD Curr. Opin. Neurobiol. 1994 4 389 399 10.1016/0959-4388(94)90101-5 7919934 · DOI · Paper page
  16. [21]Pinar C. Fontaine C.J. Triviño-Paredes J. Lottenberg C.P. Gil-Mohapel J. Christie B.R. Revisiting the Flip Side: Long-Term Depression of Synaptic Efficacy in the Hippocampus Neurosci. Biobehav. Rev. 2017 80 394 413 10.1016/j.neubiorev.2017.06.001 28624435 · DOI
  17. [24]Monday H.R. Younts T.J. Castillo P.E. Long-Term Plasticity of Neurotransmitter Release: Emerging Mechanisms and Contributions to Brain Function and Disease Annu. Rev. Neurosci. 2018 41 299 322 10.1146/annurev-neuro-080317-062155 29709205 PMC6238218 · DOI · Paper page
  18. [25]Zuo Y. Lin A. Chang P. Gan W.-B. Development of Long-Term Dendritic Spine Stability in Diverse Regions of Cerebral Cortex Neuron 2005 46 181 189 10.1016/j.neuron.2005.04.001 15848798 · DOI · Paper page
  19. [26]Kourosh-Arami M. Hosseini N. Komaki A. Brain Is Modulated by Neuronal Plasticity during Postnatal Development J. Physiol. Sci. 2021 71 34 10.1186/s12576-021-00819-9 34789147 PMC10716960 · DOI
  20. [27]Johnston M.V. Ishida A. Ishida W.N. Matsushita H.B. Nishimura A. Tsuji M. Plasticity and Injury in the Developing Brain Brain Dev. 2009 31 1 10 10.1016/j.braindev.2008.03.014 18490122 PMC2660856 · DOI
  21. [29]Ming G. Song H. Adult Neurogenesis in the Mammalian Brain: Significant Answers and Significant Questions Neuron 2011 70 687 702 10.1016/j.neuron.2011.05.001 21609825 PMC3106107 · DOI · Paper page
  22. [30]Budday S. Steinmann P. Kuhl E. Physical Biology of Human Brain Development Front. Cell. Neurosci. 2015 9 257 10.3389/fncel.2015.00257 26217183 PMC4495345 · DOI
  23. [31]Gage F.H. Structural Plasticity of the Adult Brain Dialogues Clin. Neurosci. 2004 6 135 141 10.31887/DCNS.2004.6.2/fgage 22034393 PMC3181802 · DOI
  24. [32]Bhatt S. Diaz R. Trainor P.A. Signals and Switches in Mammalian Neural Crest Cell Differentiation Cold Spring Harb. Perspect. Biol. 2013 5 a008326 10.1101/cshperspect.a008326 23378583 PMC3552505 · DOI · Paper page
  25. [33]Kosodo Y. Röper K. Haubensak W. Marzesco A.-M. Corbeil D. Huttner W.B. Asymmetric Distribution of the Apical Plasma Membrane during Neurogenic Divisions of Mammalian Neuroepithelial Cells EMBO J. 2004 23 2314 2324 10.1038/sj.emboj.7600223 15141162 PMC419905 · DOI
  26. [34]Stiles J. Jernigan T.L. The Basics of Brain Development Neuropsychol. Rev. 2010 20 327 348 10.1007/s11065-010-9148-4 21042938 PMC2989000 · DOI · Paper page
  27. [35]Gil-Sanz C. Franco S.J. Martinez-Garay I. Espinosa A. Harkins-Perry S. Müller U. Cajal-Retzius Cells Instruct Neuronal Migration by Coincidence Signaling between Secreted and Contact-Dependent Guidance Cues Neuron 2013 79 461 477 10.1016/j.neuron.2013.06.040 23931996 PMC3774067 · DOI
  28. [36]Patton M.H. Blundon J.A. Zakharenko S.S. Rejuvenation of Plasticity in the Brain: Opening the Critical Period Curr. Opin. Neurobiol. 2019 54 83 89 10.1016/j.conb.2018.09.003 30286407 PMC6361689 · DOI
  29. [37]Huttenlocher P.R. Dabholkar A.S. Regional Differences in Synaptogenesis in Human Cerebral Cortex J. Comp. Neurol. 1997 387 167 178 10.1002/(SICI)1096-9861(19971020)387:2<167::AID-CNE1>3.0.CO;2-Z 9336221 · DOI
  30. [38]Ismail F.Y. Fatemi A. Johnston M.V. Cerebral Plasticity: Windows of Opportunity in the Developing Brain Eur. J. Paediatr. Neurol. 2017 21 23 48 10.1016/j.ejpn.2016.07.007 27567276 · DOI · Paper page
  31. [39]Faust T.E. Gunner G. Schafer D.P. Mechanisms Governing Activity-Dependent Synaptic Pruning in the Developing Mammalian CNS Nat. Rev. Neurosci. 2021 22 657 673 10.1038/s41583-021-00507-y 34545240 PMC8541743 · DOI
  32. [40]Fares J. Bou Diab Z. Nabha S. Fares Y. Neurogenesis in the Adult Hippocampus: History, Regulation, and Prospective Roles Int. J. Neurosci. 2019 129 598 611 10.1080/00207454.2018.1545771 30433866 · DOI
  33. [41]Eriksson P.S. Perfilieva E. Björk-Eriksson T. Alborn A.-M. Nordborg C. Peterson D.A. Gage F.H. Neurogenesis in the Adult Human Hippocampus Nat. Med. 1998 4 1313 1317 10.1038/3305 9809557 · DOI · Paper page
  34. [42]Merkle F.T. Tramontin A.D. García-Verdugo J.M. Alvarez-Buylla A. Radial Glia Give Rise to Adult Neural Stem Cells in the Subventricular Zone Proc. Natl. Acad. Sci. USA 2004 101 17528 17532 10.1073/pnas.0407893101 15574494 PMC536036 · DOI
  35. [43]Kuhn H. Dickinson-Anson H. Gage F. Neurogenesis in the Dentate Gyrus of the Adult Rat: Age-Related Decrease of Neuronal Progenitor Proliferation J. Neurosci. 1996 16 2027 2033 10.1523/JNEUROSCI.16-06-02027.1996 8604047 PMC6578509 · DOI · Paper page
  36. [44]Lois C. Alvarez-Buylla A. Long-Distance Neuronal Migration in the Adult Mammalian Brain Science 1994 264 1145 1148 10.1126/science.8178174 8178174 · DOI
  37. [45]Maggi R. Zasso J. Conti L. Neurodevelopmental Origin and Adult Neurogenesis of the Neuroendocrine Hypothalamus Front. Cell. Neurosci. 2015 8 440 10.3389/fncel.2014.00440 25610370 PMC4285089 · DOI
  38. [46]Kokoeva M.V. Yin H. Flier J.S. Neurogenesis in the Hypothalamus of Adult Mice: Potential Role in Energy Balance Science 2005 310 679 683 10.1126/science.1115360 16254185 · DOI
  39. [47]Villalba A. Götz M. Borrell V. The Regulation of Cortical Neurogenesis Curr. Top. Dev. Biol. 2021 142 1 66 10.1016/bs.ctdb.2020.10.003 33706916 · DOI
  40. [48]Gould E. Reeves A.J. Graziano M.S.A. Gross C.G. Neurogenesis in the Neocortex of Adult Primates Science 1999 286 548 552 10.1126/science.286.5439.548 10521353 · DOI
  41. [49]Roeder S.S. Burkardt P. Rost F. Rode J. Brusch L. Coras R. Englund E. Håkansson K. Possnert G. Salehpour M. Evidence for Postnatal Neurogenesis in the Human Amygdala Commun. Biol. 2022 5 366 10.1038/s42003-022-03299-8 35440676 PMC9018740 · DOI
  42. [50]Ponti G. Peretto P. Bonfanti L. Genesis of Neuronal and Glial Progenitors in the Cerebellar Cortex of Peripuberal and Adult Rabbits PLoS ONE 2008 3 e2366 10.1371/journal.pone.0002366 18523645 PMC2396292 · DOI
  43. [51]Andreotti J.P. Prazeres P.H.D.M. Magno L.A.V. Romano-Silva M.A. Mintz A. Birbrair A. Neurogenesis in the Postnatal Cerebellum after Injury Int. J. Dev. Neurosci. 2018 67 33 36 10.1016/j.ijdevneu.2018.03.002 29555564 PMC6069997 · DOI
  44. [52]Ernst A. Alkass K. Bernard S. Salehpour M. Perl S. Tisdale J. Possnert G. Druid H. Frisén J. Neurogenesis in the Striatum of the Adult Human Brain Cell 2014 156 1072 1083 10.1016/j.cell.2014.01.044 24561062 · DOI · Paper page
  45. [53]Bruel-Jungerman E. Rampon C. Laroche S. Adult Hippocampal Neurogenesis, Synaptic Plasticity and Memory: Facts and Hypotheses Rev. Neurosci. 2007 18 93 114 10.1515/REVNEURO.2007.18.2.93 17593874 · DOI
  46. [54]Koehl M. Abrous D.N. A New Chapter in the Field of Memory: Adult Hippocampal Neurogenesis Eur. J. Neurosci. 2011 33 1101 1114 10.1111/j.1460-9568.2011.07609.x 21395854 · DOI
  47. [55]Samuels B.A. Hen R. Neurogenesis and Affective Disorders Eur. J. Neurosci. 2011 33 1152 1159 10.1111/j.1460-9568.2011.07614.x 21395859 · DOI
  48. [56]Åberg M.A.I. Åberg N.D. Hedbäcker H. Oscarsson J. Eriksson P.S. Peripheral Infusion of IGF-I Selectively Induces Neurogenesis in the Adult Rat Hippocampus J. Neurosci. 2000 20 2896 2903 10.1523/JNEUROSCI.20-08-02896.2000 10751442 PMC6772218 · DOI · Paper page
  49. [57]Zigova T. Pencea V. Wiegand S.J. Luskin M.B. Intraventricular Administration of BDNF Increases the Number of Newly Generated Neurons in the Adult Olfactory Bulb Mol. Cell. Neurosci. 1998 11 234 245 10.1006/mcne.1998.0684 9675054 · DOI
  50. [58]Yao B. Christian K.M. He C. Jin P. Ming G. Song H. Epigenetic Mechanisms in Neurogenesis Nat. Rev. Neurosci. 2016 17 537 549 10.1038/nrn.2016.70 27334043 PMC5610421 · DOI
  51. [59]Du Preez A. Onorato D. Eiben I. Musaelyan K. Egeland M. Zunszain P.A. Fernandes C. Thuret S. Pariante C.M. Chronic Stress Followed by Social Isolation Promotes Depressive-like Behaviour, Alters Microglial and Astrocyte Biology and Reduces Hippocampal Neurogenesis in Male Mice Brain. Behav. Immun. 2021 91 24 47 10.1016/j.bbi.2020.07.015 32755644 · DOI · Paper page
  52. [60]Malberg J.E. Eisch A.J. Nestler E.J. Duman R.S. Chronic Antidepressant Treatment Increases Neurogenesis in Adult Rat Hippocampus J. Neurosci. 2000 20 9104 9110 10.1523/JNEUROSCI.20-24-09104.2000 11124987 PMC6773038 · DOI · Paper page
  53. [61]Manev H. Uz T. Smalheiser N.R. Manev R. Antidepressants Alter Cell Proliferation in the Adult Brain in Vivo and in Neural Cultures in Vitro Eur. J. Pharmacol. 2001 411 67 70 10.1016/S0014-2999(00)00904-3 11137860 · DOI
  54. [63]Bettio L.E.B. Rajendran L. Gil-Mohapel J. The Effects of Aging in the Hippocampus and Cognitive Decline Neurosci. Biobehav. Rev. 2017 79 66 86 10.1016/j.neubiorev.2017.04.030 28476525 · DOI
  55. [65]Isaev N.K. Stelmashook E.V. Genrikhs E.E. Neurogenesis and Brain Aging Rev. Neurosci. 2019 30 573 580 10.1515/revneuro-2018-0084 30763272 · DOI
  56. [66]Gipson C.D. Kupchik Y.M. Kalivas P.W. Rapid, Transient Synaptic Plasticity in Addiction Neuropharmacology 2014 76 276 286 10.1016/j.neuropharm.2013.04.032 23639436 PMC3762905 · DOI
  57. [67]Bicker F. Nardi L. Maier J. Vasic V. Schmeisser M.J. Criss-crossing Autism Spectrum Disorder and Adult Neurogenesis J. Neurochem. 2021 159 452 478 10.1111/jnc.15501 34478569 · DOI
  58. [68]Hansel C. Deregulation of Synaptic Plasticity in Autism Neurosci. Lett. 2019 688 58 61 10.1016/j.neulet.2018.02.003 29421544 · DOI
  59. [71]Babcock K.R. Page J.S. Fallon J.R. Webb A.E. Adult Hippocampal Neurogenesis in Aging and Alzheimer’s Disease Stem Cell Rep. 2021 16 681 693 10.1016/j.stemcr.2021.01.019 PMC8072031 33636114 · DOI
  60. [72]Magee J.C. Grienberger C. Synaptic Plasticity Forms and Functions Annu. Rev. Neurosci. 2020 43 95 117 10.1146/annurev-neuro-090919-022842 32075520 · DOI · Paper page
  61. [73]Baltaci S.B. Mogulkoc R. Baltaci A.K. Molecular Mechanisms of Early and Late LTP Neurochem. Res. 2019 44 281 296 10.1007/s11064-018-2695-4 30523578 · DOI · Paper page
  62. [74]Mainberger F. Langer S. Mall V. Jung N.H. Impaired Synaptic Plasticity in RASopathies: A Mini-Review J. Neural Transm. 2016 123 1133 1138 10.1007/s00702-016-1609-3 27565148 · DOI
  63. [75]Bliss T.V.P. Lømo T. Long-Lasting Potentiation of Synaptic Transmission in the Dentate Area of the Anaesthetized Rabbit Following Stimulation of the Perforant Path J. Physiol. 1973 232 331 356 10.1113/jphysiol.1973.sp010273 4727084 PMC1350458 · DOI · Paper page
  64. [76]Gall C.M. Le A.A. Lynch G. Sex Differences in Synaptic Plasticity Underlying Learning J. Neurosci. Res. 2023 101 764 782 10.1002/jnr.24844 33847004 PMC10337639 · DOI
  65. [77]Lynch M.A. Long-Term Potentiation and Memory Physiol. Rev. 2004 84 87 136 10.1152/physrev.00014.2003 14715912 · DOI
  66. [78]Johnson M.H. Functional Brain Development in Humans Nat. Rev. Neurosci. 2001 2 475 483 10.1038/35081509 11433372 · DOI · Paper page
  67. [80]Pascual-Leone A. Amedi A. Fregni F. Merabet L.B. THE PLASTIC HUMAN BRAIN CORTEX Annu. Rev. Neurosci. 2005 28 377 401 10.1146/annurev.neuro.27.070203.144216 16022601 · DOI · Paper page
  68. [81]Draganski B. Gaser C. Busch V. Schuierer G. Bogdahn U. May A. Changes in Grey Matter Induced by Training Nature 2004 427 311 312 10.1038/427311a 14737157 · DOI · Paper page
  69. [82]Boyke J. Driemeyer J. Gaser C. Büchel C. May A. Training-Induced Brain Structure Changes in the Elderly J. Neurosci. 2008 28 7031 7035 10.1523/JNEUROSCI.0742-08.2008 18614670 PMC6670504 · DOI · Paper page
  70. [83]Castrén E. Hen R. Neuronal Plasticity and Antidepressant Actions Trends Neurosci. 2013 36 259 267 10.1016/j.tins.2012.12.010 23380665 PMC3648595 · DOI · Paper page
  71. [84]Kleim J.A. Barbay S. Cooper N.R. Hogg T.M. Reidel C.N. Remple M.S. Nudo R.J. Motor Learning-Dependent Synaptogenesis Is Localized to Functionally Reorganized Motor Cortex Neurobiol. Learn. Mem. 2002 77 63 77 10.1006/nlme.2000.4004 11749086 · DOI
  72. [85]Gil-Mohapel J. Boehme F. Kainer L. Christie B.R. Hippocampal Cell Loss and Neurogenesis after Fetal Alcohol Exposure: Insights from Different Rodent Models Brain Res. Rev. 2010 64 283 303 10.1016/j.brainresrev.2010.04.011 20471420 · DOI
  73. [87]McEwen B.S. Bowles N.P. Gray J.D. Hill M.N. Hunter R.G. Karatsoreos I.N. Nasca C. Mechanisms of Stress in the Brain Nat. Neurosci. 2015 18 1353 1363 10.1038/nn.4086 26404710 PMC4933289 · DOI · Paper page
  74. [88]Catala M. Embryonic Development of the Central Nervous System Encyclopedia of Neuroscience Springer Berlin/Heidelberg, Germany 2021 196 202
  75. [89]Copp A.J. Greene N.D.E. Neural Tube Defects-Disorders of Neurulation and Related Embryonic Processes Wiley Interdiscip. Rev. Dev. Biol. 2013 2 213 227 10.1002/wdev.71 24009034 PMC4023228 · DOI
  76. [94]Miller F.D. Gauthier-Fisher A. Home at Last: Neural Stem Cell Niches Defined Cell Stem Cell 2009 4 507 510 10.1016/j.stem.2009.05.008 19497279 · DOI
  77. [95]Paus T. Growth of White Matter in the Adolescent Brain: Myelin or Axon? Brain Cogn. 2010 72 26 35 10.1016/j.bandc.2009.06.002 19595493 · DOI · Paper page
  78. [96]Kuan C.-Y. Roth K.A. Flavell R.A. Rakic P. Mechanisms of Programmed Cell Death in the Developing Brain Trends Neurosci. 2000 23 291 297 10.1016/S0166-2236(00)01581-2 10856938 · DOI
  79. [97]Bourgeois J. Synaptogenesis, Heterochrony and Epigenesis in the Mammalian Neocortex Acta Paediatr. 1997 86 27 33 10.1111/j.1651-2227.1997.tb18340.x 9298788 · DOI
  80. [99]Hultman C.M. Sparen P. Takei N. Murray R.M. Cnattingius S. Geddes J. Prenatal and Perinatal Risk Factors for Schizophrenia, Affective Psychosis, and Reactive Psychosis of Early Onset: Case-Control Study Prenatal and Perinatal Risk Factors for Early Onset Schizophrenia, Affective Psychosis, and Reactive Psychosis BMJ 1999 318 421 426 10.1136/bmj.318.7181.421 9974454 PMC27730 · DOI
  81. [101]Wadhwa P. Buss C. Entringer S. Swanson J. Developmental Origins of Health and Disease: Brief History of the Approach and Current Focus on Epigenetic Mechanisms Semin. Reprod. Med. 2009 27 358 368 10.1055/s-0029-1237424 19711246 PMC2862635 · DOI
  82. [102]de Juan Romero C. Borrell V. Genetic Maps and Patterns of Cerebral Cortex Folding Curr. Opin. Cell Biol. 2017 49 31 37 10.1016/j.ceb.2017.11.009 29227862 · DOI
  83. [103]Toso L. Poggi S.H. Roberson R. Woodard J. Park J. Abebe D. Spong C.Y. Prevention of Alcohol-Induced Learning Deficits in Fetal Alcohol Syndrome Mediated through NMDA and GABA Receptors Am. J. Obstet. Gynecol. 2006 194 681 686 10.1016/j.ajog.2006.01.003 16522397 · DOI
  84. [104]Olney J.W. Wozniak D.F. Jevtovic-Todorovic V. Farber N.B. Bittigau P. Ikonomidou C. Glutamate and GABA Receptor Dysfunction in the Fetal Alcohol Syndrome Neurotox. Res. 2002 4 315 325 10.1080/1029842021000010875 12829421 · DOI
  85. [105]Buss C. Entringer S. Wadhwa P.D. Fetal Programming of Brain Development: Intrauterine Stress and Susceptibility to Psychopathology Sci. Signal. 2012 5 pt7 10.1126/scisignal.2003406 23047922 PMC3837231 · DOI
  86. [107]Partanen E. Kujala T. Tervaniemi M. Huotilainen M. Prenatal Music Exposure Induces Long-Term Neural Effects PLoS ONE 2013 8 e78946 10.1371/journal.pone.0078946 24205353 PMC3813619 · DOI
  87. [108]Golub M.D. Sadtler P.T. Oby E.R. Quick K.M. Ryu S.I. Tyler-Kabara E.C. Batista A.P. Chase S.M. Yu B.M. Learning by Neural Reassociation Nat. Neurosci. 2018 21 607 616 10.1038/s41593-018-0095-3 29531364 PMC5876156 · DOI
  88. [109]Giedd J.N. Structural Magnetic Resonance Imaging of the Adolescent Brain Ann. N. Y. Acad. Sci. 2004 1021 77 85 10.1196/annals.1308.009 15251877 · DOI · Paper page
  89. [110]Bishop D.V.M. Snowling M.J. Developmental Dyslexia and Specific Language Impairment: Same or Different? Psychol. Bull. 2004 130 858 886 10.1037/0033-2909.130.6.858 15535741 · DOI · Paper page
  90. [112]Werker J.F. Hensch T.K. Critical Periods in Speech Perception: New Directions Annu. Rev. Psychol. 2015 66 173 196 10.1146/annurev-psych-010814-015104 25251488 · DOI · Paper page
  91. [113]Diamond A. Executive Functions Annu. Rev. Psychol. 2013 64 135 168 10.1146/annurev-psych-113011-143750 23020641 PMC4084861 · DOI · Paper page
  92. [114]Hackman D.A. Farah M.J. Socioeconomic Status and the Developing Brain Trends Cogn. Sci. 2009 13 65 73 10.1016/j.tics.2008.11.003 19135405 PMC3575682 · DOI
  93. [115]Bowlby J. Attachment and Loss: Retrospect and Prospect Am. J. Orthopsychiatry 1982 52 664 678 10.1111/j.1939-0025.1982.tb01456.x 7148988 · DOI · Paper page
  94. [118]Russell G. Lightman S. The Human Stress Response Nat. Rev. Endocrinol. 2019 15 525 534 10.1038/s41574-019-0228-0 31249398 · DOI · Paper page
  95. [120]Oomen C.A. Mayer J.L. De Kloet E.R. Joëls M. Lucassen P.J. Brief Treatment with the Glucocorticoid Receptor Antagonist Mifepristone Normalizes the Reduction in Neurogenesis after Chronic Stress Eur. J. Neurosci. 2007 26 3395 3401 10.1111/j.1460-9568.2007.05972.x 18052970 · DOI
  96. [121]Liu R. Yang X.D. Liao X.M. Xie X.M. Su Y.A. Li J.T. Wang X.D. Si T.M. Early Postnatal Stress Suppresses the Developmental Trajectory of Hippocampal Pyramidal Neurons: The Role of CRHR1 Brain Struct. Funct. 2016 221 4525 4536 10.1007/s00429-016-1182-4 26792004 · DOI
  97. [122]Fabricius K. Wörtwein G. Pakkenberg B. The Impact of Maternal Separation on Adult Mouse Behaviour and on the Total Neuron Number in the Mouse Hippocampus Brain Struct. Funct. 2008 212 403 416 10.1007/s00429-007-0169-6 18200448 PMC2226080 · DOI
  98. [124]Herzberg M.P. Gunnar M.R. Early Life Stress and Brain Function: Activity and Connectivity Associated with Processing Emotion and Reward Neuroimage 2020 209 116493 10.1016/j.neuroimage.2019.116493 31884055 PMC7056544 · DOI
  99. [126]Hair N.L. Hanson J.L. Wolfe B.L. Pollak S.D. Association of Child Poverty, Brain Development, and Academic Achievement JAMA Pediatr. 2015 169 822 829 10.1001/jamapediatrics.2015.1475 26192216 PMC4687959 · DOI
  100. [129]Pilowsky D.J. Keyes K.M. Hasin D.S. Adverse Childhood Events and Lifetime Alcohol Dependence Am. J. Public Health 2009 99 258 263 10.2105/AJPH.2008.139006 19059847 PMC2622772 · DOI
  101. [130]Hyman S.M. Paliwal P. Chaplin T.M. Mazure C.M. Rounsaville B.J. Sinha R. Severity of Childhood Trauma Is Predictive of Cocaine Relapse Outcomes in Women but Not Men Drug Alcohol Depend. 2008 92 208 216 10.1016/j.drugalcdep.2007.08.006 17900822 PMC2233653 · DOI · Paper page
  102. [133]Gee D.G. Humphreys K.L. Flannery J. Goff B. Telzer E.H. Shapiro M. Hare T.A. Bookheimer S.Y. Tottenham N. A Developmental Shift from Positive to Negative Connectivity in Human Amygdala–Prefrontal Circuitry J. Neurosci. 2013 33 4584 4593 10.1523/JNEUROSCI.3446-12.2013 23467374 PMC3670947 · DOI · Paper page
  103. [134]Blakemore S.-J. Development of the Social Brain in Adolescence J. R. Soc. Med. 2012 105 111 116 10.1258/jrsm.2011.110221 22434810 PMC3308644 · DOI
  104. [136]Sowell E.R. Peterson B.S. Thompson P.M. Welcome S.E. Henkenius A.L. Toga A.W. Mapping Cortical Change across the Human Life Span Nat. Neurosci. 2003 6 309 315 10.1038/nn1008 12548289 · DOI · Paper page
  105. [137]Evans J. Sumners C. Moore J. Huentelman M.J. Deng J. Gelband C.H. Shaw G. Characterization of Mitotic Neurons Derived From Adult Rat Hypothalamus and Brain Stem J. Neurophysiol. 2002 87 1076 1085 10.1152/jn.00088.2001 11826071 · DOI
  106. [138]Parent A. Côté P.Y. Lavoie B. Chemical Anatomy of Primate Basal Ganglia Prog. Neurobiol. 1995 46 131 197 10.1016/0301-0082(95)80010-6 7568912 · DOI
  107. [139]Suzuki S.O. Goldman J.E. Multiple Cell Populations in the Early Postnatal Subventricular Zone Take Distinct Migratory Pathways: A Dynamic Study of Glial and Neuronal Progenitor Migration J. Neurosci. 2003 23 4240 4250 10.1523/JNEUROSCI.23-10-04240.2003 12764112 PMC6741090 · DOI
  108. [140]Shapiro L.A. Ng K. Zhou Q.-Y. Ribak C.E. Subventricular Zone-Derived, Newly Generated Neurons Populate Several Olfactory and Limbic Forebrain Regions Epilepsy Behav. 2009 14 74 80 10.1016/j.yebeh.2008.09.011 18849007 PMC2677571 · DOI
  109. [141]Zhao M. Momma S. Delfani K. Carlén M. Cassidy R.M. Johansson C.B. Brismar H. Shupliakov O. Frisén J. Janson A.M. Evidence for Neurogenesis in the Adult Mammalian Substantia Nigra Proc. Natl. Acad. Sci. USA 2003 100 7925 7930 10.1073/pnas.1131955100 12792021 PMC164689 · DOI
  110. [142]Magavi S.S. Leavitt B.R. Macklis J.D. Induction of Neurogenesis in the Neocortex of Adult Mice Nature 2000 405 951 955 10.1038/35016083 10879536 · DOI
  111. [143]Bernier P.J. Bédard A. Vinet J. Lévesque M. Parent A. Newly Generated Neurons in the Amygdala and Adjoining Cortex of Adult Primates Proc. Natl. Acad. Sci. USA 2002 99 11464 11469 10.1073/pnas.172403999 12177450 PMC123279 · DOI
  112. [144]Cao Q.-L. Howard R.M. Dennison J.B. Whittemore S.R. Differentiation of Engrafted Neuronal-Restricted Precursor Cells Is Inhibited in the Traumatically Injured Spinal Cord Exp. Neurol. 2002 177 349 359 10.1006/exnr.2002.7981 12429182 · DOI
  113. [145]Dayer A.G. Cleaver K.M. Abouantoun T. Cameron H.A. New GABAergic Interneurons in the Adult Neocortex and Striatum Are Generated from Different Precursors J. Cell Biol. 2005 168 415 427 10.1083/jcb.200407053 15684031 PMC2171716 · DOI
  114. [146]Inta D. Alfonso J. von Engelhardt J. Kreuzberg M.M. Meyer A.H. van Hooft J.A. Monyer H. Neurogenesis and Widespread Forebrain Migration of Distinct GABAergic Neurons from the Postnatal Subventricular Zone Proc. Natl. Acad. Sci. USA 2008 105 20994 20999 10.1073/pnas.0807059105 19095802 PMC2605417 · DOI
  115. [147]Florio M. Huttner W.B. Neural Progenitors, Neurogenesis and the Evolution of the Neocortex Development 2014 141 2182 2194 10.1242/dev.090571 24866113 · DOI
  116. [148]Zecevic N. Rakic P. Development of Layer I Neurons in the Primate Cerebral Cortex J. Neurosci. 2001 21 5607 5619 10.1523/JNEUROSCI.21-15-05607.2001 11466432 PMC6762645 · DOI
  117. [149]Jhaveri D.J. Tedoldi A. Hunt S. Sullivan R. Watts N.R. Power J.M. Bartlett P.F. Sah P. Evidence for Newly Generated Interneurons in the Basolateral Amygdala of Adult Mice Mol. Psychiatry 2018 23 521 532 10.1038/mp.2017.134 28809399 PMC5822453 · DOI
  118. [150]Lee D.A. Bedont J.L. Pak T. Wang H. Song J. Miranda-Angulo A. Takiar V. Charubhumi V. Balordi F. Takebayashi H. Tanycytes of the Hypothalamic Median Eminence Form a Diet-Responsive Neurogenic Niche Nat. Neurosci. 2012 15 700 702 10.1038/nn.3079 22446882 PMC3380241 · DOI · Paper page
  119. [151]Li J. Tang Y. Cai D. IKKβ/NF-ΚB Disrupts Adult Hypothalamic Neural Stem Cells to Mediate a Neurodegenerative Mechanism of Dietary Obesity and Pre-Diabetes Nat. Cell Biol. 2012 14 999 1012 10.1038/ncb2562 22940906 PMC3463771 · DOI
  120. [152]Bernstein P.L. Zuo M. Cheng M.-F. Social Condition Affects the Courtship Behavior of Male Ring Doves with Posterior Medial Hypothalamic Lesions Behav. Neural Biol. 1993 59 120 125 10.1016/0163-1047(93)90834-5 8476379 · DOI
  121. [153]Fowler C.D. Liu Y. Ouimet C. Wang Z. The Effects of Social Environment on Adult Neurogenesis in the Female Prairie Vole J. Neurobiol. 2002 51 115 128 10.1002/neu.10042 11932953 · DOI
  122. [154]Cheng M.-F. Peng J.-P. Chen G. Gardner J.P. Bonder E.M. Functional Restoration of Acoustic Units and Adult-Generated Neurons after Hypothalamic Lesion J. Neurobiol. 2004 60 197 213 10.1002/neu.20014 15266651 · DOI
  123. [155]Zhang Y. Kim M.S. Jia B. Yan J. Zuniga-Hertz J.P. Han C. Cai D. Hypothalamic Stem Cells Control Ageing Speed Partly through Exosomal MiRNAs Nature 2017 548 52 57 10.1038/nature23282 28746310 PMC5999038 · DOI · Paper page
  124. [156]Plakkot B. Di Agostino A. Subramanian M. Implications of Hypothalamic Neural Stem Cells on Aging and Obesity-Associated Cardiovascular Diseases Cells 2023 12 769 10.3390/cells12050769 36899905 PMC10000584 · DOI
  125. [157]Duman R.S. Nakagawa S. Malberg J.E. Regulation of Adult Neurogenesis by Antidepressant Treatment Neuropsychopharmacology 2001 25 836 844 10.1016/S0893-133X(01)00358-X 11750177 · DOI · Paper page
  126. [158]Santarelli L. Saxe M. Gross C. Surget A. Battaglia F. Dulawa S. Weisstaub N. Lee J. Duman R. Arancio O. Requirement of Hippocampal Neurogenesis for the Behavioral Effects of Antidepressants Science 2003 301 805 809 10.1126/science.1083328 12907793 · DOI · Paper page
  127. [159]Castello N.A. Nguyen M.H. Tran J.D. Cheng D. Green K.N. LaFerla F.M. Ketamine-Induced Neurogenesis in Prefrontal Cortex Contributes to Antidepressant-like Effects Proc. Natl. Acad. Sci. USA 2020 117 28794 28804
  128. [161]van Praag H. Christie B.R. Sejnowski T.J. Gage F.H. Running Enhances Neurogenesis, Learning, and Long-Term Potentiation in Mice Proc. Natl. Acad. Sci. USA 1999 96 13427 13431 10.1073/pnas.96.23.13427 10557337 PMC23964 · DOI · Paper page
  129. [162]Yau S. Gil-Mohapel J. Christie B.R. So K. Physical Exercise-Induced Adult Neurogenesis: A Good Strategy to Prevent Cognitive Decline in Neurodegenerative Diseases? Biomed Res. Int. 2014 2014 403120 10.1155/2014/403120 24818140 PMC4000963 · DOI
  130. [164]Edlow A.G. Maternal Obesity and Neurodevelopmental and Psychiatric Disorders in Offspring Prenat. Diagn. 2017 37 95 110 10.1002/pd.4932 27684946 PMC5572633 · DOI
  131. [166]Dearden L. Ozanne S.E. Early Life Origins of Metabolic Disease: Developmental Programming of Hypothalamic Pathways Controlling Energy Homeostasis Front. Neuroendocrinol. 2015 39 3 16 10.1016/j.yfrne.2015.08.001 26296796 · DOI
  132. [167]Bae-Gartz I. Janoschek R. Breuer S. Schmitz L. Hoffmann T. Ferrari N. Branik L. Oberthuer A. Kloppe C.-S. Appel S. Maternal Obesity Alters Neurotrophin-Associated MAPK Signaling in the Hypothalamus of Male Mouse Offspring Front. Neurosci. 2019 13 962 10.3389/fnins.2019.00962 31572115 PMC6753176 · DOI
  133. [168]Schmitz L. Kuglin R. Bae-Gartz I. Janoschek R. Appel S. Mesaros A. Jakovcevski I. Vohlen C. Handwerk M. Ensenauer R. Hippocampal Insulin Resistance Links Maternal Obesity with Impaired Neuronal Plasticity in Adult Offspring Psychoneuroendocrinology 2018 89 46 52 10.1016/j.psyneuen.2017.12.023 29324300 · DOI
  134. [169]Van Dam J.M. Garrett A.J. Schneider L.A. Hodyl N.A. Goldsworthy M.R. Coat S. Rowan J.A. Hague W.M. Pitcher J.B. Reduced Cortical Excitability, Neuroplasticity, and Salivary Cortisol in 11–13-Year-Old Children Born to Women with Gestational Diabetes Mellitus EBioMedicine 2018 31 143 149 10.1016/j.ebiom.2018.04.011 29709497 PMC6014572 · DOI
  135. [170]Yu L. Zhong X. He Y. Shi Y. Butyrate, but Not Propionate, Reverses Maternal Diet-Induced Neurocognitive Deficits in Offspring Pharmacol. Res. 2020 160 105082 10.1016/j.phrs.2020.105082 32679183 · DOI
  136. [171]Mendes-da-Silva C. Lemes S.F. Baliani T.d.S. Versutti M.D. Torsoni M.A. Increased Expression of Hes5 Protein in Notch Signaling Pathway in the Hippocampus of Mice Offspring of Dams Fed a High-fat Diet during Pregnancy and Suckling Int. J. Dev. Neurosci. 2015 40 35 42 10.1016/j.ijdevneu.2014.11.005 25450527 · DOI
  137. [172]Ge Q. Hu X. Ma N. Sun M. Zhang L. Cai Z. Tan R. Lu H. Maternal High-salt Diet during Pregnancy Impairs Synaptic Plasticity and Memory in Offspring FASEB J. 2021 35 e21244 10.1096/fj.202001890R 33715195 · DOI
  138. [173]Wasserman G.A. Liu X. Parvez F. Ahsan H. Factor-Litvak P. van Geen A. Slavkovich V. Lolacono N.J. Cheng Z. Hussain I. Water Arsenic Exposure and Children’s Intellectual Function in Araihazar, Bangladesh Environ. Health Perspect. 2004 112 1329 1333 10.1289/ehp.6964 15345348 PMC1247525 · DOI
  139. [174]May P.A. Chambers C.D. Kalberg W.O. Zellner J. Feldman H. Buckley D. Kopald D. Hasken J.M. Xu R. Honerkamp-Smith G. Prevalence of Fetal Alcohol Spectrum Disorders in 4 US Communities JAMA 2018 319 474 10.1001/jama.2017.21896 29411031 PMC5839298 · DOI
  140. [175]Brancato A. Castelli V. Lavanco G. Marino R.A.M. Cannizzaro C. In Utero Δ9-Tetrahydrocannabinol Exposure Confers Vulnerability towards Cognitive Impairments and Alcohol Drinking in the Adolescent Offspring: Is There a Role for Neuropeptide Y? J. Psychopharmacol. 2020 34 663 679 10.1177/0269881120916135 32338122 · DOI
  141. [177]Grandjean P. Landrigan P.J. Neurobehavioural Effects of Developmental Toxicity Lancet Neurol. 2014 13 330 338 10.1016/S1474-4422(13)70278-3 24556010 PMC4418502 · DOI · Paper page
  142. [181]Heidarzadeh M. Taheri M. Mazaheripour Z. Abbasi-Khameneh F. The Incidence of Congenital Anomalies in Newborns before and during the Covid-19 Pandemic Ital. J. Pediatr. 2022 48 174 10.1186/s13052-022-01368-6 36109775 PMC9479418 · DOI
  143. [182]Black M.M. Walker S.P. Fernald L.C.H. Andersen C.T. DiGirolamo A.M. Lu C. McCoy D.C. Fink G. Shawar Y.R. Shiffman J. Early Childhood Development Coming of Age: Science through the Life Course Lancet 2017 389 77 90 10.1016/S0140-6736(16)31389-7 27717614 PMC5884058 · DOI · Paper page
  144. [183]Vinuesa A. Bentivegna M. Calfa G. Filipello F. Pomilio C. Bonaventura M.M. Lux-Lantos V. Matzkin M.E. Gregosa A. Presa J. Early Exposure to a High-Fat Diet Impacts on Hippocampal Plasticity: Implication of Microglia-Derived Exosome-like Extracellular Vesicles Mol. Neurobiol. 2019 56 5075 5094 10.1007/s12035-018-1435-8 30474797 · DOI
  145. [184]Arcego D.M. Olivo L.B. Moraes R.O. Garcia E.d.S. Silveira A.C. Krolow R. Couto-Pereira N.d.S. Lampert C. Toniazzo A.P. Nicola F.d.C. Neurometabolic Effects of Sweetened Solution Intake during Adolescence Related to Depressive-like Phenotype in Rats Nutrition 2020 75–76 110770 10.1016/j.nut.2020.110770 32276242 · DOI
  146. [185]Lee H. Park H. Ha E. Hong Y.-C. Ha M. Park H. Kim B.-N. Lee B. Lee S.-J. Lee K.Y. Effect of Breastfeeding Duration on Cognitive Development in Infants: 3-Year Follow-up Study J. Korean Med. Sci. 2016 31 579 10.3346/jkms.2016.31.4.579 27051242 PMC4810341 · DOI
  147. [186]Abbink M.R. Schipper L. Naninck E.F.G. de Vos C.M.H. Meier R. van der Beek E.M. Lucassen P.J. Korosi A. The Effects of Early Life Stress, Postnatal Diet Modulation, and Long-Term Western-Style Diet on Later-Life Metabolic and Cognitive Outcomes Nutrients 2020 12 570 10.3390/nu12020570 32098348 PMC7071477 · DOI
  148. [187]Ruel M.T. Alderman H. Nutrition-Sensitive Interventions and Programmes: How Can They Help to Accelerate Progress in Improving Maternal and Child Nutrition? Lancet 2013 382 536 551 10.1016/S0140-6736(13)60843-0 23746780 · DOI · Paper page
  149. [188]Victora C.G. Adair L. Fall C. Hallal P.C. Martorell R. Richter L. Sachdev H.S. Maternal and Child Undernutrition: Consequences for Adult Health and Human Capital Lancet 2008 371 340 357 10.1016/S0140-6736(07)61692-4 18206223 PMC2258311 · DOI
  150. [189]Prado E.L. Abbeddou S. Adu-Afarwuah S. Arimond M. Ashorn P. Ashorn U. Brown K.H. Hess S.Y. Lartey A. Maleta K. Linear Growth and Child Development in Burkina Faso, Ghana, and Malawi Pediatrics 2016 138 e20154698 10.1542/peds.2015-4698 27474016 · DOI
  151. [195]Nelson C.A. Thomas K.M. de Haan M. Neural Bases of Cognitive Development Handbook of Child Psychology John Wiley & Sons, Inc. Hoboken, NJ, USA 2007 1 56
  152. [196]Kempermann G. Environmental Enrichment, New Neurons and the Neurobiology of Individuality Nat. Rev. Neurosci. 2019 20 235 245 10.1038/s41583-019-0120-x 30723309 · DOI
  153. [197]Bergami M. Masserdotti G. Temprana S.G. Motori E. Eriksson T.M. Göbel J. Yang S.M. Conzelmann K.-K. Schinder A.F. Götz M. A Critical Period for Experience-Dependent Remodeling of Adult-Born Neuron Connectivity Neuron 2015 85 710 717 10.1016/j.neuron.2015.01.001 25661179 · DOI
  154. [198]Barichello T. Fagundes G.D. Generoso J.S. Dagostin C.S. Simões L.R. Vilela M.C. Comim C.M. Petronilho F. Quevedo J. Teixeira A.L. Environmental Enrichment Restores Cognitive Deficits Induced by Experimental Childhood Meningitis Rev. Bras. Psiquiatr. 2014 36 322 329 10.1590/1516-4446-2014-1443 25076170 · DOI
  155. [200]Vogel Ciernia A. Laufer B.I. Dunaway K.W. Mordaunt C.E. Coulson R.L. Totah T.S. Stolzenberg D.S. Frahm J.C. Singh-Taylor A. Baram T.Z. Experience-Dependent Neuroplasticity of the Developing Hypothalamus: Integrative Epigenomic Approaches Epigenetics 2018 13 318 330 10.1080/15592294.2018.1451720 29613827 PMC5997166 · DOI
  156. [201]Marrocco J. McEwen B.S. Sex in the Brain: Hormones and Sex Differences Dialogues Clin. Neurosci. 2016 18 373 383 10.31887/DCNS.2016.18.4/jmarrocco 28179809 PMC5286723 · DOI
  157. [202]Duarte-Guterman P. Yagi S. Chow C. Galea L.A.M. Hippocampal Learning, Memory, and Neurogenesis: Effects of Sex and Estrogens across the Lifespan in Adults Horm. Behav. 2015 74 37 52 10.1016/j.yhbeh.2015.05.024 26122299 · DOI
  158. [203]Triviño-Paredes J. Patten A.R. Gil-Mohapel J. Christie B.R. The Effects of Hormones and Physical Exercise on Hippocampal Structural Plasticity Front. Neuroendocrinol. 2016 41 23 43 10.1016/j.yfrne.2016.03.001 26989000 · DOI
  159. [204]Hojo Y. Murakami G. Mukai H. Higo S. Hatanaka Y. Ogiue-Ikeda M. Ishii H. Kimoto T. Kawato S. Estrogen Synthesis in the Brain—Role in Synaptic Plasticity and Memory Mol. Cell. Endocrinol. 2008 290 31 43 10.1016/j.mce.2008.04.017 18541362 · DOI · Paper page
  160. [205]Hojo Y. Hattori T. Enami T. Furukawa A. Suzuki K. Ishii H. Mukai H. Morrison J.H. Janssen W.G.M. Kominami S. Adult Male Rat Hippocampus Synthesizes Estradiol from Pregnenolone by Cytochromes P45017α and P450 Aromatase Localized in Neurons Proc. Natl. Acad. Sci. USA 2004 101 865 870 10.1073/pnas.2630225100 14694190 PMC321772 · DOI · Paper page
  161. [206]Kato A. Hojo Y. Higo S. Komatsuzaki Y. Murakami G. Yoshino H. Uebayashi M. Kawato S. Female Hippocampal Estrogens Have a Significant Correlation with Cyclic Fluctuation of Hippocampal Spines Front. Neural Circuits 2013 7 149 10.3389/fncir.2013.00149 24151456 PMC3798982 · DOI
  162. [207]Okamoto M. Hojo Y. Inoue K. Matsui T. Kawato S. McEwen B.S. Soya H. Mild Exercise Increases Dihydrotestosterone in Hippocampus Providing Evidence for Androgenic Mediation of Neurogenesis Proc. Natl. Acad. Sci. USA 2012 109 13100 13105 10.1073/pnas.1210023109 22807478 PMC3420174 · DOI
  163. [208]Prange-Kiel J. Wehrenberg U. Jarry H. Rune G.M. Para/Autocrine Regulation of Estrogen Receptors in Hippocampal Neurons Hippocampus 2003 13 226 234 10.1002/hipo.10075 12699330 · DOI
  164. [209]Camacho-Arroyo I. Piña-Medina A.G. Bello-Alvarez C. Zamora-Sánchez C.J. Sex Hormones and Proteins Involved in Brain Plasticity Vitam. Horm. 2020 114 145 165 10.1016/bs.vh.2020.04.002 32723542 · DOI
  165. [210]Fester L. Rune G.M. Sex Neurosteroids: Hormones Made by the Brain for the Brain Neurosci. Lett. 2021 753 135849 10.1016/j.neulet.2021.135849 33775739 · DOI
  166. [211]Brunne B. Rune G.M. Sex Neurosteroidogenesis and Hippocampal Network Maintenance Curr. Opin. Endocr. Metab. Res. 2022 23 100316 10.1016/j.coemr.2022.100316 · DOI
  167. [212]McEwen B.S. Akama K.T. Spencer-Segal J.L. Milner T.A. Waters E.M. Estrogen Effects on the Brain: Actions beyond the Hypothalamus via Novel Mechanisms Behav. Neurosci. 2012 126 4 16 10.1037/a0026708 22289042 PMC3480182 · DOI
  168. [213]Brann D.W. Lu Y. Wang J. Zhang Q. Thakkar R. Sareddy G.R. Pratap U.P. Tekmal R.R. Vadlamudi R.K. Brain-Derived Estrogen and Neural Function Neurosci. Biobehav. Rev. 2022 132 793 817 10.1016/j.neubiorev.2021.11.014 34823913 PMC8816863 · DOI
  169. [214]Lu Y. Sareddy G.R. Wang J. Wang R. Li Y. Dong Y. Zhang Q. Liu J. O’Connor J.C. Xu J. Neuron-Derived Estrogen Regulates Synaptic Plasticity and Memory J. Neurosci. 2019 39 2792 2809 10.1523/JNEUROSCI.1970-18.2019 30728170 PMC6462452 · DOI
  170. [215]Bettio L.E.B. Thacker J.S. Rodgers S.P. Brocardo P.S. Christie B.R. Gil-Mohapel J. Interplay between Hormones and Exercise on Hippocampal Plasticity across the Lifespan Biochim. Biophys. Acta-Mol. Basis Dis. 2020 1866 165821 10.1016/j.bbadis.2020.165821 32376385 · DOI · Paper page
  171. [224]Navarro A. Boveris A. The Mitochondrial Energy Transduction System and the Aging Process Am. J. Physiol. Physiol. 2007 292 C670 C686 10.1152/ajpcell.00213.2006 17020935 · DOI · Paper page
  172. [225]Muñoz-Espín D. Serrano M. Cellular Senescence: From Physiology to Pathology Nat. Rev. Mol. Cell Biol. 2014 15 482 496 10.1038/nrm3823 24954210 · DOI · Paper page
  173. [227]Stern Y. Arenaza-Urquijo E.M. Bartrés-Faz D. Belleville S. Cantilon M. Chetelat G. Ewers M. Franzmeier N. Kempermann G. Kremen W.S. Whitepaper: Defining and Investigating Cognitive Reserve, Brain Reserve, and Brain Maintenance Alzheimers Dement. 2020 16 1305 1311 10.1016/j.jalz.2018.07.219 30222945 PMC6417987 · DOI · Paper page
  174. [228]McQuail J.A. Dunn A.R. Stern Y. Barnes C.A. Kempermann G. Rapp P.R. Kaczorowski C.C. Foster T.C. Cognitive Reserve in Model Systems for Mechanistic Discovery: The Importance of Longitudinal Studies Front. Aging Neurosci. 2021 12 607685 10.3389/fnagi.2020.607685 33551788 PMC7859530 · DOI
  175. [229]Ionescu-Tucker A. Cotman C.W. Emerging Roles of Oxidative Stress in Brain Aging and Alzheimer’s Disease Neurobiol. Aging 2021 107 86 95 10.1016/j.neurobiolaging.2021.07.014 34416493 · DOI · Paper page
  176. [230]Baracaldo-Santamaría D. Avendaño-Lopez S.S. Ariza-Salamanca D.F. Rodriguez-Giraldo M. Calderon-Ospina C.A. González-Reyes R.E. Nava-Mesa M.O. Role of Calcium Modulation in the Pathophysiology and Treatment of Alzheimer’s Disease Int. J. Mol. Sci. 2023 24 9067 10.3390/ijms24109067 37240413 PMC10218981 · DOI
  177. [231]Lesuis S.L. Hoeijmakers L. Korosi A. de Rooij S.R. Swaab D.F. Kessels H.W. Lucassen P.J. Krugers H.J. Vulnerability and Resilience to Alzheimer’s Disease: Early Life Conditions Modulate Neuropathology and Determine Cognitive Reserve Alzheimers. Res. Ther. 2018 10 95 10.1186/s13195-018-0422-7 30227888 PMC6145191 · DOI
  178. [232]Jellinger K.A. Attems J. Neuropathological Approaches to Cerebral Aging and Neuroplasticity Dialogues Clin. Neurosci. 2013 15 29 43 10.31887/DCNS.2013.15.1/kjellinger 23576887 PMC3622466 · DOI
  179. [233]Hy L.X. Keller D.M. Prevalence of AD among Whites Neurology 2000 55 198 204 10.1212/WNL.55.2.198 10908890 · DOI
  180. [234]Niu H. Álvarez-Álvarez I. Guillén-Grima F. Aguinaga-Ontoso I. Prevalence and Incidence of Alzheimer’s Disease in Europe: A Meta-Analysis Neurologia 2017 32 523 532 10.1016/j.nrl.2016.02.016 27130306 · DOI
  181. [236]Guo J. Huang X. Dou L. Yan M. Shen T. Tang W. Li J. Aging and Aging-Related Diseases: From Molecular Mechanisms to Interventions and Treatments Signal Transduct. Target. Ther. 2022 7 391 10.1038/s41392-022-01251-0 36522308 PMC9755275 · DOI
  182. [237]Verkhratsky A. Lazareva N. Semyanov A. Glial Decline and Loss of Homeostatic Support Rather than Inflammation Defines Cognitive Aging Neural Regen. Res. 2022 17 565 10.4103/1673-5374.320979 34380892 PMC8504371 · DOI
  183. [238]Barrientos R.M. Kitt M.M. Watkins L.R. Maier S.F. Neuroinflammation in the Normal Aging Hippocampus Neuroscience 2015 309 84 99 10.1016/j.neuroscience.2015.03.007 25772789 PMC4567963 · DOI
  184. [239]Wang X. Michaelis E.K. Selective Neuronal Vulnerability to Oxidative Stress in the Brain Front. Aging Neurosci. 2010 2 12 10.3389/fnagi.2010.00012 20552050 PMC2874397 · DOI
  185. [240]Grimm A. Eckert A. Brain Aging and Neurodegeneration: From a Mitochondrial Point of View J. Neurochem. 2017 143 418 431 10.1111/jnc.14037 28397282 PMC5724505 · DOI
  186. [241]Johnson F.B. Sinclair D.A. Guarente L. Molecular Biology of Aging Cell 1999 96 291 302 10.1016/S0092-8674(00)80567-X 9988222 · DOI
  187. [242]Khachaturian Z.S. The Role of Calcium Regulation in Brain Aging: Reexamination of a Hypothesis Aging Clin. Exp. Res. 1989 1 17 34 10.1007/BF03323872 2488296 · DOI
  188. [243]Foster T.C. Calcium Homeostasis and Modulation of Synaptic Plasticity in the Aged Brain Aging Cell 2007 6 319 325 10.1111/j.1474-9726.2007.00283.x 17517041 · DOI
  189. [244]Gant J.C. Chen K.-C. Kadish I. Blalock E.M. Thibault O. Porter N.M. Landfield P.W. Reversal of Aging-Related Neuronal Ca2+ Dysregulation and Cognitive Impairment by Delivery of a Transgene Encoding FK506-Binding Protein 12.6/1b to the Hippocampus J. Neurosci. 2015 35 10878 10887 10.1523/JNEUROSCI.1248-15.2015 26224869 PMC4518058 · DOI
  190. [245]Kumar A. Foster T.C. Alteration in NMDA Receptor Mediated Glutamatergic Neurotransmission in the Hippocampus During Senescence Neurochem. Res. 2019 44 38 48 10.1007/s11064-018-2634-4 30209673 PMC6374185 · DOI
  191. [246]Santos-Parker J.R. LaRocca T.J. Seals D.R. Aerobic Exercise and Other Healthy Lifestyle Factors That Influence Vascular Aging Adv. Physiol. Educ. 2014 38 296 307 10.1152/advan.00088.2014 25434012 PMC4315444 · DOI
  192. [247]Simpson R.J. Kunz H. Agha N. Graff R. Exercise and the Regulation of Immune Functions Prog. Mol. Biol. Transl. Sci. 2015 135 355 380 10.1016/bs.pmbts.2015.08.001 26477922 · DOI
  193. [248]Fjell A.M. Walhovd K.B. Structural Brain Changes in Aging: Courses, Causes and Cognitive Consequences Rev. Neurosci. 2010 21 187 222 10.1515/REVNEURO.2010.21.3.187 20879692 · DOI
  194. [249]Beyer K. Domingo-Sàbat M. Ariza A. Guillazo-Blanch G. Molecular Anatomy of the Nigrostriatal Pathway in the Rat: A Review Neuroscience 2012 227 70 83
  195. [250]Gil J.M. Rego A.C. Mechanisms of Neurodegeneration in Huntington’s Disease Eur. J. Neurosci. 2008 27 2803 2820 10.1111/j.1460-9568.2008.06310.x 18588526 · DOI
  196. [251]Li Y. Liu W. Oo T.F. Wang L. Tang Y. Jackson-Lewis V. Zhou C. Geghman K. Bogdanov M. Przedborski S. Mutant LRRK2R1441G BAC Transgenic Mice Recapitulate Cardinal Features of Parkinson’s Disease Nat. Neurosci. 2009 12 826 828 10.1038/nn.2349 19503083 PMC2845930 · DOI
  197. [255]Bhat A.H. Dar K.B. Anees S. Zargar M.A. Masood A. Sofi M.A. Ganie S.A. Oxidative Stress, Mitochondrial Dysfunction and Neurodegenerative Diseases; a Mechanistic Insight Biomed. Pharmacother. 2015 74 101 110 10.1016/j.biopha.2015.07.025 26349970 · DOI
  198. [256]Sweeney P. Park H. Baumann M. Dunlop J. Frydman J. Kopito R. McCampbell A. Leblanc G. Venkateswaran A. Nurmi A. Protein misfolding in neurodegenerative diseases: Implications and strategies Transl Neurodegener. 2017 6 1 13 10.1186/s40035-017-0077-5 28293421 PMC5348787 · DOI · Paper page
  199. [257]DiFiglia M. Sapp E. Chase K.O. Davies S.W. Bates G.P. Vonsattel J.P. Aronin N. Aggregation of Huntingtin in Neuronal Intranuclear Inclusions and Dystrophic Neurites in Brain Science 1997 277 1990 1993 10.1126/science.277.5334.1990 9302293 · DOI
  200. [260]Hroudová J. Singh N. Fišar Z. Mitochondrial Dysfunctions in Neurodegenerative Diseases: Relevance to Alzheimer’s Disease Biomed Res. Int. 2014 2014 175062 10.1155/2014/175062 24900954 PMC4036420 · DOI

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Authors
Marzola, P., Melzer, T., Pavesi, E., Gil-Mohapel, J., & Brocardo, P. S.
Affiliations
  • Universidade Federal de Santa Catarina (BR)
  • Department of Morphological Sciences and Graduate Neuroscience Program, Center of Biological Sciences, Federal University of Santa Catarina, Florianopolis 88040-900, SC, Brazil
  • Division of Medical Sciences, University of Victoria, Victoria, BC V8P 5C2, Canada
Venue
Brain Sciences
Publisher
MDPI AG
Published
2023-11-21
Volume
13
Issue
12
Pages
1610
ISSN
2076-3425 (ISSN-L)
OpenAlex
W4388867239
Cited by
281
References
52
Citations by year
2026: 121 · 2025: 141 · 2024: 19
FWCI
10.72
Type
journal article
Language
en
Open access
Locations
  • Brain Sciences (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Fundação de Amparo à Pesquisa e Inovação do Estado de Santa Catarina (2021TR1523, UVic-FAPESP SPRINT 1/2018)
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; Brazil) Research Productivity Fellowship (2021TR1523, UVic-FAPESP SPRINT 1/2018)
  • University of Victoria (UVic, Victoria, BC, Canada) – São Paulo Research Foundation (FAPESP, São Paulo, SP, Brazil) SPRINT partnership (2021TR1523, UVic-FAPESP SPRINT 1/2018)
Topics
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords
neuroplasticity, brain development, brain aging, neurodegeneration, synaptic plasticity, neurogenesis, learning and memory, brain injury recovery, protein aggregation, mitochondrial dysfunction, oxidative stress, neuroinflammation, lifestyle intervention

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