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Current Pharmaceutical Biotechnology

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ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

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Mini-Review Article

The Impact of Physical Exercise on the Hippocampus in Physiological Condition and Ageing-Related Decline: Current Evidence from Animal and Human Studies

Author(s): Giovanni Lauretta, Silvia Ravalli, Grazia Maugeri, Velia D’Agata, Michelino Di Rosa and Giuseppe Musumeci*

Volume 23, Issue 2, 2022

Published on: 05 April, 2021

Page: [180 - 189] Pages: 10

DOI: 10.2174/1389201022666210405142611

Price: $65

Abstract

Physical exercise (PE), notoriously, promotes a state of general well-being, throughout the entire human lifespan. Moreover, maintaining an adequate and regular PE habit results in a powerful preventive factor towards many diseases and may also help in managing existing pathological conditions. PE induces structural and functional changes in various parts of the body, determining biological and psychological benefits. Additionally, in the elderly, PE might represent a remarkable tool reducing cognitive impairments related to the normal aging processes and it has also been found to have an impact on neurodegenerative diseases such as Alzheimer’s disease. The present review aims to provide an overview of PE effects on the hippocampus, since it is one of the brain regions most susceptible to aging and, therefore, involved in diseases characterized by cognitive impairment.

Keywords: Physical exercise, cognitive impairment, cognitive decline, aging, hippocampus, neurogenesis, neurotrophic factors.

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[1]
Di Liegro, C.M.; Schiera, G.; Proia, P.; Di Liegro, I. Physical Activity and Brain Health. Genes (Basel), 2019, 10(9), 720.
[http://dx.doi.org/10.3390/genes10090720] [PMID: 31533339]
[2]
Tremblay, M.S.; Colley, R.C.; Saunders, T.J.; Healy, G.N.; Owen, N. Physiological and health implications of a sedentary lifestyle. Appl. Physiol. Nutr. Metab., 2010, 35(6), 725-740.
[http://dx.doi.org/10.1139/H10-079] [PMID: 21164543]
[3]
Vina, J.; Sanchis-Gomar, F.; Martinez-Bello, V.; Gomez-Cabrera, M.C. Exercise acts as a drug; the pharmacological benefits of exercise. Br. J. Pharmacol., 2012, 167(1), 1-12.
[http://dx.doi.org/10.1111/j.1476-5381.2012.01970.x] [PMID: 22486393]
[4]
Toledo, A.C.; Magalhaes, R.M.; Hizume, D.C.; Vieira, R.P.; Biselli, P.J.; Moriya, H.T.; Mauad, T.; Lopes, F.D.; Martins, M.A. Aerobic exercise attenuates pulmonary injury induced by exposure to cigarette smoke. Eur. Respir. J., 2012, 39(2), 254-264.
[http://dx.doi.org/10.1183/09031936.00003411] [PMID: 21700603]
[5]
Nystoriak, M.A.; Bhatnagar, A. Cardiovascular Effects and Benefits of Exercise. Front. Cardiovasc. Med., 2018, 5, 135.
[http://dx.doi.org/10.3389/fcvm.2018.00135] [PMID: 30324108]
[6]
Castrogiovanni, P.; Di Rosa, M.; Ravalli, S.; Castorina, A.; Guglielmino, C.; Imbesi, R.; Vecchio, M.; Drago, F.; Szychlinska, M.A.; Musumeci, G. Moderate physical activity as a prevention method for knee osteoarthritis and the role of synoviocytes as biological key. Int. J. Mol. Sci., 2019, 20(3), 511.
[http://dx.doi.org/10.3390/ijms20030511] [PMID: 30691048]
[7]
Musumeci, G. Effects of exercise on physical limitations and fatigue in rheumatic diseases. World J. Orthop., 2015, 6(10), 762-769.
[http://dx.doi.org/10.5312/wjo.v6.i10.762] [PMID: 26601057]
[8]
Beavers, K.M.; Brinkley, T.E.; Nicklas, B.J. Effect of exercise training on chronic inflammation. Clin. Chim. Acta, 2010, 411(11-12), 785-793.
[http://dx.doi.org/10.1016/j.cca.2010.02.069] [PMID: 20188719]
[9]
Eckstein, M.L.; Williams, D.M.; O’Neil, L.K.; Hayes, J.; Stephens, J.W.; Bracken, R.M. Physical exercise and non-insulin glucose-lowering therapies in the management of Type 2 diabetes mellitus: a clinical review. Diabet. Med., 2019, 36(3), 349-358.
[PMID: 30536728]
[10]
Wang, Q.; Zhou, W. Roles and molecular mechanisms of physical exercise in cancer prevention and treatment. J. Sport Health Sci., 2020, 2095-2546(20), 30095-8.,
[11]
Young, D.R.; Hivert, M.F.; Alhassan, S.; Camhi, S.M.; Ferguson, J.F.; Katzmarzyk, P.T.; Lewis, C.E.; Owen, N.; Perry, C.K.; Siddique, J.; Yong, C.M. Physical activity committee of the council on lifestyle and cardiometabolic health; council on clinical cardiology; council on epidemiology and prevention; council on functional genomics and translational biology; and stroke council. sedentary behavior and cardiovascular morbidity and mortality: a science advisory from the american heart association. Circulation, 2016, 134(13), e262-e279.
[http://dx.doi.org/10.1161/CIR.0000000000000440] [PMID: 27528691]
[12]
Maugeri, G.; D'Agata, V. Effects of physical activity on amyotrophic lateral sclerosis. J.F.M.K., 2020, , 5.(2) 5020029.,
[13]
Ma, Q. Beneficial effects of moderate voluntary physical exercise and its biological mechanisms on brain health. Neurosci. Bull., 2008, 24(4), 265-270.
[http://dx.doi.org/10.1007/s12264-008-0402-1] [PMID: 18668156]
[14]
Esteban-Cornejo, I.; Martinez-Gomez, D.; Tejero-González, C.M.; Izquierdo-Gomez, R.; Carbonell-Baeza, A.; Castro-Piñero, J.; Sallis, J.F.; Veiga, O.L.U.P. UP & DOWN Study Group.Maternal physical activity before and during the prenatal period and the offspring’s academic performance in youth. The UP&DOWN study. J. Matern. Fetal Neonatal Med., 2016, 29(9), 1414-1420.
[http://dx.doi.org/10.3109/14767058.2015.1049525] [PMID: 26135457]
[15]
Chaddock, L.; Erickson, K.I.; Prakash, R.S.; Kim, J.S.; Voss, M.W.; Vanpatter, M.; Pontifex, M.B.; Raine, L.B.; Konkel, A.; Hillman, C.H.; Cohen, N.J.; Kramer, A.F. A neuroimaging investigation of the association between aerobic fitness, hippocampal volume, and memory performance in preadolescent children. Brain Res., 2010, 1358, 172-183.
[http://dx.doi.org/10.1016/j.brainres.2010.08.049] [PMID: 20735996]
[16]
Chaddock-Heyman, L.; Erickson, K.I.; Kienzler, C.; Drollette, E.S.; Raine, L.B.; Kao, S.C.; Bensken, J.; Weisshappel, R.; Castelli, D.M.; Hillman, C.H.; Kramer, A.F. Physical activity increases white matter microstructure in children. Front. Neurosci., 2018, 12, 950.
[http://dx.doi.org/10.3389/fnins.2018.00950] [PMID: 30618578]
[17]
Thomas, A.G.; Dennis, A.; Bandettini, P.A.; Johansen-Berg, H. The effects of aerobic activity on brain structure. Front. Psychol., 2012, 3, 86.
[http://dx.doi.org/10.3389/fpsyg.2012.00086] [PMID: 22470361]
[18]
van Praag, H.; Shubert, T.; Zhao, C.; Gage, F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci., 2005, 25(38), 8680-8685.
[http://dx.doi.org/10.1523/JNEUROSCI.1731-05.2005] [PMID: 16177036]
[19]
Erickson, K.I.; Prakash, R.S.; Voss, M.W.; Chaddock, L.; Hu, L.; Morris, K.S.; White, S.M.; Wójcicki, T.R.; McAuley, E.; Kramer, A.F. Aerobic fitness is associated with hippocampal volume in elderly humans. Hippocampus, 2009, 19(10), 1030-1039.
[http://dx.doi.org/10.1002/hipo.20547] [PMID: 19123237]
[20]
Fleiner, T.; Dauth, H.; Gersie, M.; Zijlstra, W.; Haussermann, P. Structured physical exercise improves neuropsychiatric symptoms in acute dementia care: a hospital-based RCT. Alzheimers Res. Ther., 2017, 9(1), 68.
[http://dx.doi.org/10.1186/s13195-017-0289-z] [PMID: 28851451]
[21]
Vreugdenhil, A.; Cannell, J.; Davies, A.; Razay, G. A community-based exercise programme to improve functional ability in people with Alzheimer’s disease: a randomized controlled trial. Scand. J. Caring Sci., 2012, 26(1), 12-19.
[http://dx.doi.org/10.1111/j.1471-6712.2011.00895.x] [PMID: 21564154]
[22]
Small, G.W. Detection and prevention of cognitive decline. Am. J. Geriatr. Psychiatry, 2016, 24(12), 1142-1150.
[http://dx.doi.org/10.1016/j.jagp.2016.08.013] [PMID: 27745823]
[23]
WHO Guidelines Risk Reduction of Cognitive Decline and Dementia; World Health Organization: Geneva, 2019.
[24]
Crous-Bou, M.; Minguillón, C.; Gramunt, N.; Molinuevo, J.L. Alzheimer’s disease prevention: from risk factors to early intervention. Alzheimers Res. Ther., 2017, 9(1), 71.
[http://dx.doi.org/10.1186/s13195-017-0297-z] [PMID: 28899416]
[25]
Knierim, J.J. The hippocampus. Curr. Biol., 2015, 25(23), R1116-R1121.
[http://dx.doi.org/10.1016/j.cub.2015.10.049] [PMID: 26654366]
[26]
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.
[http://dx.doi.org/10.1016/j.neubiorev.2017.04.030] [PMID: 28476525]
[27]
Grundman, M.; Sencakova, D.; Jack, C.R., Jr; Petersen, R.C.; Kim, H.T.; Schultz, A.; Weiner, M.F.; DeCarli, C.; DeKosky, S.T.; van Dyck, C.; Thomas, R.G.; Thal, L.J. Alzheimer’s Disease Cooperative Study. Brain MRI hippocampal volume and prediction of clinical status in a mild cognitive impairment trial. J. Mol. Neurosci., 2002, 19(1-2), 23-27.
[http://dx.doi.org/10.1007/s12031-002-0006-6] [PMID: 12212787]
[28]
Dawe, R.J.; Yu, L.; Arfanakis, K.; Schneider, J.A.; Bennett, D.A.; Boyle, P.A. Late-life cognitive decline is associated with hippocampal volume, above and beyond its associations with traditional neuropathologic indices. Alzheimers Dement., 2020, 16(1), 209-218.
[http://dx.doi.org/10.1002/alz.12009] [PMID: 31914231]
[29]
Bruno, D.; Ciarleglio, A.; Grothe, M.J.; Nierenberg, J.; Bachman, A.H.; Teipel, S.J.; Petkova, E.; Ardekani, B.A.; Pomara, N. Hippocampal volume and integrity as predictors of cognitive decline in intact elderly. Neuroreport, 2016, 27(11), 869-873.
[http://dx.doi.org/10.1097/WNR.0000000000000629] [PMID: 27306593]
[30]
Peng, G.P.; Feng, Z.; He, F.P.; Chen, Z.Q.; Liu, X.Y.; Liu, P.; Luo, B.Y. Correlation of hippocampal volume and cognitive performances in patients with either mild cognitive impairment or Alzheimer’s disease. CNS Neurosci. Ther., 2015, 21(1), 15-22.
[http://dx.doi.org/10.1111/cns.12317] [PMID: 25146658]
[31]
Suwabe, K.; Hyodo, K.; Byun, K.; Ochi, G.; Yassa, M.A.; Soya, H. Acute moderate exercise improves mnemonic discrimination in young adults. Hippocampus, 2017, 27(3), 229-234.
[http://dx.doi.org/10.1002/hipo.22695] [PMID: 27997992]
[32]
Frodl, T.; Strehl, K.; Carballedo, A.; Tozzi, L.; Doyle, M.; Amico, F.; Gormley, J.; Lavelle, G.; O’Keane, V. Aerobic exercise increases hippocampal subfield volumes in younger adults and prevents volume decline in the elderly. Brain Imaging Behav., 2020, 14(5), 1577-1587.
[http://dx.doi.org/10.1007/s11682-019-00088-6] [PMID: 30927200]
[33]
Du, Z.; Li, Y.; Li, J.; Zhou, C.; Li, F.; Yang, X. Physical activity can improve cognition in patients with Alzheimer’s disease: a systematic review and meta-analysis of randomized controlled trials. Clin. Interv. Aging, 2018, 13, 1593-1603.
[http://dx.doi.org/10.2147/CIA.S169565] [PMID: 30233156]
[34]
Northey, J.M.; Cherbuin, N.; Pumpa, K.L.; Smee, D.J.; Rattray, B. Exercise interventions for cognitive function in adults older than 50: a systematic review with meta-analysis. Br. J. Sports Med., 2018, 52(3), 154-160.
[http://dx.doi.org/10.1136/bjsports-2016-096587] [PMID: 28438770]
[35]
Den Ouden, L.; Kandola, A.; Suo, C.; Hendrikse, J.; Costa, R.J.S.; Watt, M.J.; Lorenzetti, V.; Chye, Y.; Parkes, L.; Sabaroedin, K.; Yücel, M. The influence of aerobic exercise on hippocampal integrity and function: preliminary findings of a multi-modal imaging analysis. Brain Plast., 2018, 4(2), 211-216.
[http://dx.doi.org/10.3233/BPL-170053] [PMID: 30598871]
[36]
Erickson, K.I.; Voss, M.W.; Prakash, R.S.; Basak, C.; Szabo, A.; Chaddock, L.; Kim, J.S.; Heo, S.; Alves, H.; White, S.M.; Wojcicki, T.R.; Mailey, E.; Vieira, V.J.; Martin, S.A.; Pence, B.D.; Woods, J.A.; McAuley, E.; Kramer, A.F. Exercise training increases size of hippocampus and improves memory. Proc. Natl. Acad. Sci. USA, 2011, 108(7), 3017-3022.
[http://dx.doi.org/10.1073/pnas.1015950108] [PMID: 21282661]
[37]
Berchtold, N.C.; Prieto, G.A.; Phelan, M.; Gillen, D.L.; Baldi, P.; Bennett, D.A.; Buchman, A.S.; Cotman, C.W. Hippocampal gene expression patterns linked to late-life physical activity oppose age and AD-related transcriptional decline. Neurobiol. Aging, 2019, 78, 142-154.
[http://dx.doi.org/10.1016/j.neurobiolaging.2019.02.012] [PMID: 30927700]
[38]
Musumeci, G.; Castrogiovanni, P.; Castorina, S.; Imbesi, R.; Szychlinska, M.A.; Scuderi, S.; Loreto, C.; Giunta, S. Changes in serotonin (5-HT) and brain-derived neurotrophic factor (BDFN) expression in frontal cortex and hippocampus of aged rat treated with high tryptophan diet. Brain Res. Bull., 2015, 119(Pt A), 12- 18.,
[http://dx.doi.org/10.1016/j.brainresbull.2015.09.010] [PMID: 26444078]
[39]
Intlekofer, K.A.; Berchtold, N.C.; Malvaez, M.; Carlos, A.J.; McQuown, S.C.; Cunningham, M.J.; Wood, M.A.; Cotman, C.W. Exercise and sodium butyrate transform a subthreshold learning event into long-term memory via a brain-derived neurotrophic factor-dependent mechanism. Neuropsychopharmacology, 2013, 38(10), 2027-34.4.,
[40]
Eadie, B.D.; Redila, V.A.; Christie, B.R. Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation, dendritic complexity, and spine density. J. Comp. Neurol., 2005, 486(1), 39-47.
[http://dx.doi.org/10.1002/cne.20493] [PMID: 15834963]
[41]
Farmer, J.; Zhao, X.; van Praag, H.; Wodtke, K.; Gage, F.H.; Christie, B.R. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience, 2004, 124(1), 71-79.
[http://dx.doi.org/10.1016/j.neuroscience.2003.09.029] [PMID: 14960340]
[42]
Van der Borght, K.; Kóbor-Nyakas, D.E.; Klauke, K.; Eggen, B.J.; Nyakas, C.; Van der Zee, E.A.; Meerlo, P. Physical exercise leads to rapid adaptations in hippocampal vasculature: temporal dynamics and relationship to cell proliferation and neurogenesis. Hippocampus, 2009, 19(10), 928-936.
[http://dx.doi.org/10.1002/hipo.20545] [PMID: 19212941]
[43]
Smith, P.J.; Blumenthal, J.A.; Hoffman, B.M.; Cooper, H.; Strauman, T.A.; Welsh-Bohmer, K.; Browndyke, J.N.; Sherwood, A. Aerobic exercise and neurocognitive performance: a meta-analytic review of randomized controlled trials. Psychosom. Med., 2010, 72(3), 239-252.
[http://dx.doi.org/10.1097/PSY.0b013e3181d14633] [PMID: 20223924]
[44]
Burdette, J.H.; Laurienti, P.J.; Espeland, M.A.; Morgan, A.; Telesford, Q.; Vechlekar, C.D.; Hayasaka, S.; Jennings, J.M.; Katula, J.A.; Kraft, R.A.; Rejeski, W.J. Using network science to evaluate exercise-associated brain changes in older adults. Front. Aging Neurosci., 2010, 2, 23.
[http://dx.doi.org/10.3389/fnagi.2010.00023] [PMID: 20589103]
[45]
Maass, A.; Düzel, S.; Goerke, M.; Becke, A.; Sobieray, U.; Neumann, K.; Lövden, M.; Lindenberger, U.; Bäckman, L.; Braun-Dullaeus, R.; Ahrens, D.; Heinze, H.J.; Müller, N.G.; Düzel, E. Vascular hippocampal plasticity after aerobic exercise in older adults. Mol. Psychiatry, 2015, 20(5), 585-593.
[http://dx.doi.org/10.1038/mp.2014.114] [PMID: 25311366]
[46]
Steventon, J.J.; Foster, C.; Furby, H.; Helme, D.; Wise, R.G.; Murphy, K. Hippocampal blood flow is increased after 20 min of moderate-intensity exercise. Cereb. Cortex, 2020, 30(2), 525-533.
[http://dx.doi.org/10.1093/cercor/bhz104] [PMID: 31216005]
[47]
Colucci-D’Amato, L.; Speranza, L.; Volpicelli, F. Neurotrophic factor BDNF, physiological functions and therapeutic potential in depression, neurodegeneration and brain cancer. Int. J. Mol. Sci., 2020, 21(20), 7777.
[http://dx.doi.org/10.3390/ijms21207777] [PMID: 33096634]
[48]
Matthews, V.B.; Aström, M.B.; Chan, M.H.; Bruce, C.R.; Krabbe, K.S.; Prelovsek, O.; Akerström, T.; Yfanti, C.; Broholm, C.; Mortensen, O.H.; Penkowa, M.; Hojman, P.; Zankari, A.; Watt, M.J.; Bruunsgaard, H.; Pedersen, B.K.; Febbraio, M.A. Brain-derived neurotrophic factor is produced by skeletal muscle cells in response to contraction and enhances fat oxidation via activation of AMP-activated protein kinase. Diabetologia, 2009, 52(7), 1409-1418.
[http://dx.doi.org/10.1007/s00125-009-1364-1] [PMID: 19387610]
[49]
Prigent-Tessier, A.; Quirié, A.; Maguin-Gaté, K.; Szostak, J.; Mossiat, C.; Nappey, M.; Devaux, S.; Marie, C.; Demougeot, C. Physical training and hypertension have opposite effects on endothelial brain-derived neurotrophic factor expression. Cardiovasc. Res., 2013, 100(3), 374-382.
[http://dx.doi.org/10.1093/cvr/cvt219] [PMID: 24092446]
[50]
Fujimura, H.; Altar, C.A.; Chen, R.; Nakamura, T.; Nakahashi, T.; Kambayashi, J.; Sun, B.; Tandon, N.N. Brain-derived neurotrophic factor is stored in human platelets and released by agonist stimulation. Thromb. Haemost., 2002, 87(4), 728-734.
[http://dx.doi.org/10.1055/s-0037-1613072] [PMID: 12008958]
[51]
Griffin, E.W.; Bechara, R.G.; Birch, A.M.; Kelly, A.M. Exercise enhances hippocampal-dependent learning in the rat: evidence for a BDNF-related mechanism. Hippocampus, 2009, 19(10), 973-980.
[http://dx.doi.org/10.1002/hipo.20631] [PMID: 19437410]
[52]
Loprinzi, P.D.; Day, S.; Deming, R. Acute exercise intensity and memory function: evaluation of the transient hypofrontality hypothesis. Medicina (Kaunas), 2019, 55(8), 445.
[http://dx.doi.org/10.3390/medicina55080445] [PMID: 31394736]
[53]
Vilela, T.C.; Muller, A.P.; Damiani, A.P.; Macan, T.P.; da Silva, S.; Canteiro, P.B.; de Sena Casagrande, A.; Pedroso, G.D.S.; Nesi, R.T.; de Andrade, V.M.; de Pinho, R.A. Strength and aerobic exercises improve spatial memory in aging rats through stimulating distinct neuroplasticity mechanisms. Mol. Neurobiol., 2017, 54(10), 7928-7937.
[http://dx.doi.org/10.1007/s12035-016-0272-x] [PMID: 27878552]
[54]
Sanfilippo, C.; Musumeci, G.; Castrogiovanni, P.; Fazio, F.; Li Volti, G.; Barbagallo, I.; Maugeri, G.; Ravalli, S.; Imbesi, R.; Di Rosa, M. Hippocampal transcriptome deconvolution reveals differences in cell architecture of not demented elderly subjects underwent late-life physical activity. J. Chem. Neuroanat., 2021, 113101934 Epub ahead of print
[http://dx.doi.org/10.1016/j.jchemneu.2021.101934] [PMID: 33582252]
[55]
Szuhany, K.L.; Bugatti, M.; Otto, M.W. A meta-analytic review of the effects of exercise on brain-derived neurotrophic factor. J. Psychiatr. Res., 2015, 60, 56-64.
[http://dx.doi.org/10.1016/j.jpsychires.2014.10.003] [PMID: 25455510]
[56]
Rasmussen, P.; Brassard, P.; Adser, H.; Pedersen, M.V.; Leick, L.; Hart, E.; Secher, N.H.; Pedersen, B.K.; Pilegaard, H. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp. Physiol., 2009, 94(10), 1062-1069.
[http://dx.doi.org/10.1113/expphysiol.2009.048512] [PMID: 19666694]
[57]
Pan, W.; Banks, W.A.; Fasold, M.B.; Bluth, J.; Kastin, A.J. Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology, 1998, 37(12), 1553-1561.
[http://dx.doi.org/10.1016/S0028-3908(98)00141-5] [PMID: 9886678]
[58]
Cho, H.C.; Kim, J.; Kim, S.; Son, Y.H.; Lee, N.; Jung, S.H. The concentrations of serum, plasma and platelet BDNF are all increased by treadmill VO2max performance in healthy college men. Neurosci. Lett., 2012, 519(1), 78-83.
[http://dx.doi.org/10.1016/j.neulet.2012.05.025] [PMID: 22617010]
[59]
Monnier, A.; Prigent-Tessier, A.; Quirié, A.; Bertrand, N.; Savary, S.; Gondcaille, C.; Garnier, P.; Demougeot, C.; Marie, C. Brain-derived neurotrophic factor of the cerebral microvasculature: a forgotten and nitric oxide-dependent contributor of brain-derived neurotrophic factor in the brain. Acta Physiol. (Oxf.), 2017, 219(4), 790-802.
[http://dx.doi.org/10.1111/apha.12743] [PMID: 27364224]
[60]
Wrann, C.D.; White, J.P.; Salogiannnis, J.; Laznik-Bogoslavski, D.; Wu, J.; Ma, D.; Lin, J.D.; Greenberg, M.E.; Spiegelman, B.M. Exercise induces hippocampal BDNF through a PGC-1α/FNDC5 pathway. Cell Metab., 2013, 18(5), 649-659.
[http://dx.doi.org/10.1016/j.cmet.2013.09.008] [PMID: 24120943]
[61]
Mizoguchi, Y.; Yao, H.; Imamura, Y.; Hashimoto, M.; Monji, A. Lower brain-derived neurotrophic factor levels are associated with age-related memory impairment in community-dwelling older adults: the Sefuri study. Sci. Rep., 2020, 10(1), 16442.
[http://dx.doi.org/10.1038/s41598-020-73576-1] [PMID: 33020545]
[62]
Borba, E.M.; Duarte, J.A.; Bristot, G.; Scotton, E.; Camozzato, A.L.; Chaves, M.L. Brain-derived neurotrophic factor serum levels and hippocampal volume in mild cognitive impairment and dementia due to Alzheimer disease. Dement. Geriatr. Cogn. Disord. Extra, 2016, 6(3), 559-567.
[http://dx.doi.org/10.1159/000450601] [PMID: 28101102]
[63]
Petzold, A.; Psotta, L.; Brigadski, T.; Endres, T.; Lessmann, V. Chronic BDNF deficiency leads to an age-dependent impairment in spatial learning. Neurobiol. Learn. Mem., 2015, 120, 52-60.
[http://dx.doi.org/10.1016/j.nlm.2015.02.009] [PMID: 25724412]
[64]
Salinas, J.; Beiser, A.; Himali, J.J.; Satizabal, C.L.; Aparicio, H.J.; Weinstein, G.; Mateen, F.J.; Berkman, L.F.; Rosand, J.; Seshadri, S. Associations between social relationship measures, serum brain-derived neurotrophic factor, and risk of stroke and dementia. Alzheimers Dement. (N. Y.), 2017, 3(2), 229-237.
[http://dx.doi.org/10.1016/j.trci.2017.03.001] [PMID: 29067329]
[65]
Ng, T.K.S.; Ho, C.S.H.; Tam, W.W.S.; Kua, E.H.; Ho, R.C. Decreased serum brain-derived neurotrophic factor (BDNF) levels in patients with Alzheimer’s disease (AD): A systematic review and meta-analysis. Int. J. Mol. Sci., 2019, 20(2), 257.
[http://dx.doi.org/10.3390/ijms20020257] [PMID: 30634650]
[66]
Dobrucki, L.W.; Tsutsumi, Y.; Kalinowski, L.; Dean, J.; Gavin, M.; Sen, S.; Mendizabal, M.; Sinusas, A.J.; Aikawa, R. Analysis of angiogenesis induced by local IGF-1 expression after myocardial infarction using microSPECT-CT imaging. J. Mol. Cell. Cardiol., 2010, 48(6), 1071-1079.
[http://dx.doi.org/10.1016/j.yjmcc.2009.10.008] [PMID: 19850049]
[67]
Fabel, K.; Fabel, K.; Tam, B.; Kaufer, D.; Baiker, A.; Simmons, N.; Kuo, C.J.; Palmer, T.D. VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur. J. Neurosci., 2003, 18(10), 2803-2812.
[http://dx.doi.org/10.1111/j.1460-9568.2003.03041.x] [PMID: 14656329]
[68]
Ryu, Y.; Maekawa, T.; Yoshino, D.; Sakitani, N.; Takashima, A.; Inoue, T.; Suzurikawa, J.; Toyohara, J.; Tago, T.; Makuuchi, M.; Fujita, N.; Sawada, K.; Murase, S.; Watanave, M.; Hirai, H.; Sakai, T.; Yoshikawa, Y.; Ogata, T.; Shinohara, M.; Nagao, M.; Sawada, Y. Mechanical regulation underlies effects of exercise on serotonin- induced signaling in the prefrontal cortex neurons. iScience, 2020, 23(2), 100874.,
[69]
Zhang, G.; Cinalli, D.; Cohen, S.J.; Knapp, K.D.; Rios, L.M.; Martínez-Hernández, J.; Luján, R.; Stackman, R.W., Jr Examination of the hippocampal contribution to serotonin 5-HT2A receptor-mediated facilitation of object memory in C57BL/6J mice. Neuropharmacology, 2016, 109, 332-340.
[http://dx.doi.org/10.1016/j.neuropharm.2016.04.033] [PMID: 27114257]
[70]
Lois, C.; García-Verdugo, J.M.; Alvarez-Buylla, A. Chain migration of neuronal precursors. Science, 1996, 271(5251), 978-981.
[http://dx.doi.org/10.1126/science.271.5251.978] [PMID: 8584933]
[71]
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(11), 1313-1317.
[http://dx.doi.org/10.1038/3305] [PMID: 9809557]
[72]
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]
[73]
Yu, D.X.; Marchetto, M.C.; Gage, F.H. How to make a hippocampal dentate gyrus granule neuron. Development, 2014, 141(12), 2366-2375.
[http://dx.doi.org/10.1242/dev.096776] [PMID: 24917496]
[74]
Luna, V.M.; Anacker, C.; Burghardt, N.S.; Khandaker, H.; Andreu, V.; Millette, A.; Leary, P.; Ravenelle, R.; Jimenez, J.C.; Mastrodonato, A.; Denny, C.A.; Fenton, A.A.; Scharfman, H.E.; Hen, R. Adult-born hippocampal neurons bidirectionally modulate entorhinal inputs into the dentate gyrus. Science, 2019, 364(6440), 578-583.
[http://dx.doi.org/10.1126/science.aat8789] [PMID: 31073064]
[75]
Dupret, D.; Revest, J.M.; Koehl, M.; Ichas, F.; De Giorgi, F.; Costet, P.; Abrous, D.N.; Piazza, P.V. Spatial relational memory requires hippocampal adult neurogenesis. PLoS One, 2008, 3(4)e1959
[http://dx.doi.org/10.1371/journal.pone.0001959] [PMID: 18509506]
[76]
Alam, M.J.; Kitamura, T.; Saitoh, Y.; Ohkawa, N.; Kondo, T.; Inokuchi, K. Adult neurogenesis conserves hippocampal memory capacity. J. Neurosci., 2018, 38(31), 6854-6863.
[http://dx.doi.org/10.1523/JNEUROSCI.2976-17.2018] [PMID: 29986876]
[77]
Jessberger, S.; Clark, R.E.; Broadbent, N.J.; Clemenson, G.D., Jr; Consiglio, A.; Lie, D.C.; Squire, L.R.; Gage, F.H. Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn. Mem., 2009, 16(2), 147-154.
[http://dx.doi.org/10.1101/lm.1172609] [PMID: 19181621]
[78]
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]
[79]
Berdugo-Vega, G.; Arias-Gil, G.; López-Fernández, A.; Artegiani, B.; Wasielewska, J.M.; Lee, C.C.; Lippert, M.T.; Kempermann, G.; Takagaki, K.; Calegari, F. Author Correction: Increasing neurogenesis refines hippocampal activity rejuvenating navigational learning strategies and contextual memory throughout life. Nat. Commun., 2020, 11(1), 1138.
[http://dx.doi.org/10.1038/s41467-020-14935-4] [PMID: 32098959]
[80]
Musumeci, G.; Castrogiovanni, P.; Szychlinska, M.A.; Imbesi, R.; Loreto, C.; Castorina, S.; Giunta, S. Protective effects of high Tryptophan diet on aging-induced passive avoidance impairment and hippocampal apoptosis. Brain Res. Bull., 2017, 128, 76-82.
[http://dx.doi.org/10.1016/j.brainresbull.2016.11.007] [PMID: 27889579]
[81]
Heine, V.M.; Maslam, S.; Joëls, M.; Lucassen, P.J. Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol. Aging, 2004, 25(3), 361-375.
[http://dx.doi.org/10.1016/S0197-4580(03)00090-3] [PMID: 15123342]
[82]
Rudnitskaya, E.A.; Kozlova, T.A.; Burnyasheva, A.O.; Kolosova, N.G.; Stefanova, N.A. Alterations of hippocampal neurogenesis during development of Alzheimer’s disease-like pathology in OXYS rats. Exp. Gerontol., 2019, 115, 32-45.
[http://dx.doi.org/10.1016/j.exger.2018.11.008] [PMID: 30415068]
[83]
Zhang, C.; McNeil, E.; Dressler, L.; Siman, R. Long-lasting impairment in hippocampal neurogenesis associated with amyloid deposition in a knock-in mouse model of familial Alzheimer’s disease. Exp. Neurol., 2007, 204(1), 77-87.
[http://dx.doi.org/10.1016/j.expneurol.2006.09.018] [PMID: 17070803]
[84]
Boldrini, M.; Fulmore, C.A.; Tartt, A.N.; Simeon, L.R.; Pavlova, I.; Poposka, V.; Rosoklija, G.B.; Stankov, A.; Arango, V.; Dwork, A.J.; Hen, R.; Mann, J.J. Human hippocampal neurogenesis persists throughout aging. Cell Stem Cell, 2018, 22(4), 589-599.e5.
[http://dx.doi.org/10.1016/j.stem.2018.03.015] [PMID: 29625071]
[85]
Moreno-Jiménez, E.P.; Flor-García, M.; Terreros-Roncal, J.; Rábano, A.; Cafini, F.; Pallas-Bazarra, N.; Ávila, J.; Llorens-Martín, M. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease. Nat. Med., 2019, 25(4), 554-560.
[http://dx.doi.org/10.1038/s41591-019-0375-9] [PMID: 30911133]
[86]
Tobin, M.K.; Musaraca, K.; Disouky, A.; Shetti, A.; Bheri, A.; Honer, W.G.; Kim, N.; Dawe, R.J.; Bennett, D.A.; Arfanakis, K.; Lazarov, O. Human hippocampal neurogenesis persists in aged adults and Alzheimer’s disease patients. Cell Stem Cell, 2019, 24(6), 974-982.e3.
[http://dx.doi.org/10.1016/j.stem.2019.05.003] [PMID: 31130513]
[87]
Inoue, K.; Okamoto, M.; Shibato, J.; Lee, M.C.; Matsui, T.; Rakwal, R.; Soya, H. Long-term mild, rather than intense, exercise enhances adult hippocampal neurogenesis and greatly changes the transcriptomic profile of the hippocampus. PLoS One, 2015, 10(6)e0128720
[http://dx.doi.org/10.1371/journal.pone.0128720] [PMID: 26061528]
[88]
Zhao, C.; Teng, E.M.; Summers, R.G., Jr; Ming, G.L.; Gage, F.H. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J. Neurosci., 2006, 26(1), 3-11.
[http://dx.doi.org/10.1523/JNEUROSCI.3648-05.2006] [PMID: 16399667]
[89]
Lin, J.Y.; Kuo, W.W.; Baskaran, R.; Kuo, C.H.; Chen, Y.A.; Chen, W.S.; Ho, T.J.; Day, C.H.; Mahalakshmi, B.; Huang, C.Y. Correction for: Swimming exercise stimulates IGF1/PI3K/Akt and AMPK/SIRT1/PGC1α survival signaling to suppress apoptosis and inflammation in aging hippocampus. Aging (Albany NY), 2020, 12(16), 16663-16664.
[http://dx.doi.org/10.18632/aging.104045] [PMID: 32889802]
[90]
Kim, D.; Cho, J.; Kang, H. Protective effect of exercise training against the progression of Alzheimer’s disease in 3xTg-AD mice. Behav. Brain Res., 2019, 374112105
[http://dx.doi.org/10.1016/j.bbr.2019.112105] [PMID: 31325514]
[91]
e, L.; Burns, J.M.; Swerdlow, R.H. Effect of high-intensity exercise on aged mouse brain mitochondria, neurogenesis, and inflammation. Neurobiol. Aging, 2014, 35(11), 2574-2583..
[http://dx.doi.org/10.1016/j.neurobiolaging.2014.05.033] [PMID: 25002036]
[92]
Ferreira, A.C.; Novais, A.; Sousa, N.; Sousa, J.C.; Marques, F. Voluntary running rescues the defective hippocampal neurogenesis and behaviour observed in lipocalin 2-null mice. Sci. Rep., 2019, 9(1), 1649.
[http://dx.doi.org/10.1038/s41598-018-38140-y] [PMID: 30733506]
[93]
Merritt, J.R.; Rhodes, J.S. Mouse genetic differences in voluntary wheel running, adult hippocampal neurogenesis and learning on the multi-strain-adapted plus water maze. Behav. Brain Res., 2015, 280, 62-71.
[http://dx.doi.org/10.1016/j.bbr.2014.11.030] [PMID: 25435316]
[94]
Mustroph, M.L.; Chen, S.; Desai, S.C.; Cay, E.B.; DeYoung, E.K.; Rhodes, J.S. Aerobic exercise is the critical variable in an enriched environment that increases hippocampal neurogenesis and water maze learning in male C57BL/6J mice. Neuroscience, 2012, 219, 62-71.
[http://dx.doi.org/10.1016/j.neuroscience.2012.06.007] [PMID: 22698691]
[95]
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(23), 13427-13431.
[http://dx.doi.org/10.1073/pnas.96.23.13427] [PMID: 10557337]
[96]
Trinchero, M.F.; Herrero, M.; Schinder, A.F. Rejuvenating the brain with chronic exercise through adult neurogenesis. Front. Neurosci., 2019, 13, 1000.
[http://dx.doi.org/10.3389/fnins.2019.01000] [PMID: 31619959]
[97]
Nokia, M.S.; Lensu, S.; Ahtiainen, J.P.; Johansson, P.P.; Koch, L.G.; Britton, S.L.; Kainulainen, H. Physical exercise increases adult hippocampal neurogenesis in male rats provided it is aerobic and sustained. J. Physiol., 2016, 594(7), 1855-1873.
[http://dx.doi.org/10.1113/JP271552] [PMID: 26844666]
[98]
Cunha, C.; Brambilla, R.; Thomas, K.L. A simple role for BDNF in learning and memory? Front. Mol. Neurosci., 2010, 3, 1.
[http://dx.doi.org/10.3389/neuro.02.001.2010] [PMID: 20162032]
[99]
Dworkin, S.; Mantamadiotis, T. Targeting CREB signalling in neurogenesis. Expert Opin. Ther. Targets, 2010, 14(8), 869-879.
[http://dx.doi.org/10.1517/14728222.2010.501332] [PMID: 20569094]
[100]
Zhu, D.Y.; Lau, L.; Liu, S.H.; Wei, J.S.; Lu, Y.M. Activation of cAMP-response-element-binding protein (CREB) after focal cerebral ischemia stimulates neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. USA, 2004, 101(25), 9453-9457.
[http://dx.doi.org/10.1073/pnas.0401063101] [PMID: 15197280]
[101]
Nam, S.M.; Kim, J.W.; Yoo, D.Y.; Yim, H.S.; Kim, D.W.; Choi, J.H.; Kim, W.; Jung, H.Y.; Won, M.H.; Hwang, I.K.; Seong, J.K.; Yoon, Y.S. Physical exercise ameliorates the reduction of neural stem cell, cell proliferation and neuroblast differentiation in senescent mice induced by D-galactose. BMC Neurosci., 2014, 15, 116.
[http://dx.doi.org/10.1186/s12868-014-0116-4] [PMID: 25359614]
[102]
Stein, A.M.; Silva, T.M.V.; Coelho, F.G.M.; Arantes, F.J.; Costa, J.L.R.; Teodoro, E.; Santos-Galduróz, R.F. Physical exercise, IGF-1 and cognition A systematic review of experimental studies in the elderly. Dement. Neuropsychol., 2018, 12(2), 114-122.
[http://dx.doi.org/10.1590/1980-57642018dn12-020003] [PMID: 29988330]
[103]
Cetinkaya, C.; Sisman, A.R.; Kiray, M.; Camsari, U.M.; Gencoglu, C.; Baykara, B.; Aksu, I.; Uysal, N. Positive effects of aerobic exercise on learning and memory functioning, which correlate with hippocampal IGF-1 increase in adolescent rats. Neurosci. Lett., 2013, 549, 177-181.
[http://dx.doi.org/10.1016/j.neulet.2013.06.012] [PMID: 23792196]
[104]
Yuan, H.; Chen, R.; Wu, L.; Chen, Q.; Hu, A.; Zhang, T.; Wang, Z.; Zhu, X. The regulatory mechanism of neurogenesis by IGF-1 in adult mice. Mol. Neurobiol., 2015, 51(2), 512-522.
[http://dx.doi.org/10.1007/s12035-014-8717-6] [PMID: 24777577]
[105]
Nieto-Estévez, V.; Defterali, Ç.; Vicario-Abejón, C. IGF-I: A key growth factor that regulates neurogenesis and synaptogenesis from embryonic to adult stages of the brain. Front. Neurosci., 2016, 10, 52.
[http://dx.doi.org/10.3389/fnins.2016.00052] [PMID: 26941597]
[106]
Niu, X.; Zhao, Y.; Yang, N.; Zhao, X.; Zhang, W.; Bai, X.; Li, A.; Yang, W.; Lu, L. Proteasome activation by insulin-like growth factor-1/nuclear factor erythroid 2-related factor 2 signaling promotes exercise-induced neurogenesis. Stem Cells, 2020, 38(2), 246-260.
[PMID: 31648402]
[107]
Zhao, Y.; Liu, X.; He, Z.; Niu, X.; Shi, W.; Ding, J.M.; Zhang, L.; Yuan, T.; Li, A.; Yang, W.; Lu, L. Essential role of proteasomes in maintaining self-renewal in neural progenitor cells. Sci. Rep., 2016, 6, 19752.
[http://dx.doi.org/10.1038/srep19752] [PMID: 26804982]
[108]
Cao, L.; Jiao, X.; Zuzga, D.S.; Liu, Y.; Fong, D.M.; Young, D.; During, M.J. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat. Genet., 2004, 36(8), 827-835.
[http://dx.doi.org/10.1038/ng1395] [PMID: 15258583]
[109]
Jin, K.; Zhu, Y.; Sun, Y.; Mao, X.O.; Xie, L.; Greenberg, D.A. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl. Acad. Sci. USA, 2002, 99(18), 11946-11950.
[http://dx.doi.org/10.1073/pnas.182296499] [PMID: 12181492]
[110]
Han, W.; Song, X.; He, R.; Li, T.; Cheng, L.; Xie, L.; Chen, H.; Jiang, L. VEGF regulates hippocampal neurogenesis and reverses cognitive deficits in immature rats after status epilepticus through the VEGF R2 signaling pathway. Epilepsy Behav., 2017, 68, 159-167.
[http://dx.doi.org/10.1016/j.yebeh.2016.12.007] [PMID: 28193596]
[111]
Claesson-Welsh, L. VEGF receptor signal transduction - A brief update. Vascul. Pharmacol., 2016, 86, 14-17.
[http://dx.doi.org/10.1016/j.vph.2016.05.011] [PMID: 27268035]
[112]
Valente, T.; Hidalgo, J.; Bolea, I.; Ramirez, B.; Anglés, N.; Reguant, J.; Morelló, J.R.; Gutiérrez, C.; Boada, M.; Unzeta, M. A diet enriched in polyphenols and polyunsaturated fatty acids, LMN diet, induces neurogenesis in the subventricular zone and hippocampus of adult mouse brain. J. Alzheimers Dis., 2009, 18(4), 849-865.
[http://dx.doi.org/10.3233/JAD-2009-1188] [PMID: 19661617]
[113]
Fernández-Fernández, L.; Comes, G.; Bolea, I.; Valente, T.; Ruiz, J.; Murtra, P.; Ramirez, B.; Anglés, N.; Reguant, J.; Morelló, J.R.; Boada, M.; Hidalgo, J.; Escorihuela, R.M.; Unzeta, M. LMN diet, rich in polyphenols and polyunsaturated fatty acids, improves mouse cognitive decline associated with aging and Alzheimer’s disease. Behav. Brain Res., 2012, 228(2), 261-271.
[http://dx.doi.org/10.1016/j.bbr.2011.11.014] [PMID: 22119712]
[114]
Akbaraly, T.; Sexton, C.; Zsoldos, E.; Mahmood, A.; Filippini, N.; Kerleau, C.; Verdier, J.M.; Virtanen, M.; Gabelle, A.; Ebmeier, K.P.; Kivimaki, M. Association of Long-Term Diet Quality with Hippocampal Volume: Longitudinal Cohort Study. Am. J. Med., 2018, 131(11), 1372-1381.e4.
[http://dx.doi.org/10.1016/j.amjmed.2018.07.001] [PMID: 30056104]
[115]
Maugeri, G.; Castrogiovanni, P.; Battaglia, G.; Pippi, R.; D’Agata, V.; Palma, A.; Di Rosa, M.; Musumeci, G. The impact of physical activity on psychological health during Covid-19 pandemic in Italy. Heliyon, 2020, 6(6)e04315
[http://dx.doi.org/10.1016/j.heliyon.2020.e04315] [PMID: 32613133]
[116]
Ravalli, S.; Musumeci, G. Coronavirus Outbreak in Italy: Physiological Benefits of Home-Based Exercise During Pandemic. J Funct Morphol Kinesiol,, 2020, 5(2), 31.
[http://dx.doi.org/10.3390/jfmk5020031] [PMID: 33467247]

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