Exercise to spot the differences: a framework for the effect of exercise on hippocampal pattern separation in humans

References

Afzal, A., Ahmad, S., Agha, F., Batool, Z., Tabassum, S., Liaquat, L., Sadir, S., Nawaz, A., and Haider, S. (2018). Administration of 5-HT-1B agonist ameliorates pseudodementia induced by depression in rats. Pak. J. Pharm. Sci. 31: 2179–2184.Search in Google Scholar

Ahlskog, J.E., Geda, Y.E., Graff-Radford, N.R., and Petersen, R.C. (2011). Physical exercise as a preventive or disease-modifying treatment of dementia and brain aging. Mayo Clin. Proc. 86: 876–884, https://doi.org/10.4065/mcp.2011.0252.Search in Google Scholar

Aimone, J.B., Li, Y., Lee, S.W., Clemenson, G.D., Deng, W., and Gage, F.H. (2014). Regulation and function of adult neurogenesis: from genes to cognition. Physiol. Rev. 94: 991–1026, https://doi.org/10.1152/physrev.00004.2014.Search in Google Scholar

Ally, B.A., Hussey, E.P., Ko, P.C., and Molitor, R.J. (2013). Pattern separation and pattern completion in Alzheimer’s disease: evidence of rapid forgetting in amnestic mild cognitive impairment. Hippocampus 23: 1246–1258, https://doi.org/10.1002/hipo.22162.Search in Google Scholar

Amaral, D.G. and Witter, M.P. (1989). The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31: 571–591, https://doi.org/10.1016/0306-4522(89)90424-7.Search in Google Scholar

Ambrogini, P., Lattanzi, D., Ciuffoli, S., Betti, M., Fanelli, M., and Cuppini, R. (2013). Physical exercise and environment exploration affect synaptogenesis in adult-generated neurons in the rat dentate gyrus: possible role of BDNF. Brain Res. 1534: 1–12, https://doi.org/10.1016/j.brainres.2013.08.023.Search in Google Scholar PubMed

Ardawi, M.S.M., Rouzi, A.A., and Qari, M.H. (2012). Physical activity in relation to serum sclerostin, insulin-like growth factor-1, and bone turnover markers in healthy premenopausal women: a cross-sectional and a longitudinal study. J. Clin. Endocrinol. Metab. 97: 3691–3699, https://doi.org/10.1210/jc.2011-3361.Search in Google Scholar PubMed

Ashdown-Franks, G., Firth, J., Carney, R., Carvalho, A.F., Hallgren, M., Koyanagi, A., Rosenbaum, S., Schuch, F.B., Smith, L., Solmi, M., et al.. (2020). Exercise as medicine for mental and substance use disorders: a meta-review of the benefits for neuropsychiatric and cognitive outcomes. Sports Med. 50: 151–170, https://doi.org/10.1007/s40279-019-01187-6.Search in Google Scholar PubMed

Avital, A., Goshen, I., Kamsler, A., Segal, M., Iverfeldt, K., Richter-Levin, G., and Yirmiya, R. (2003). Impaired interleukin-1 signaling is associated with deficits in hippocampal memory processes and neural plasticity. Hippocampus 13: 826–834, https://doi.org/10.1002/hipo.10135.Search in Google Scholar PubMed

Barha, C.K., Falck, R.S., Davis, J.C., Nagamatsu, L.S., and Liu-Ambrose, T. (2017). Sex differences in aerobic exercise efficacy to improve cognition: a systematic review and meta-analysis of studies in older rodents. Front. Neuroendocrinol. 46: 86–105, https://doi.org/10.1016/j.yfrne.2017.06.001.Search in Google Scholar PubMed

Barha, C.K. and Galea, L.A.M. (2010). Influence of different estrogens on neuroplasticity and cognition in the hippocampus. Biochim. Biophys. Acta 1800: 1056–1067, https://doi.org/10.1016/j.bbagen.2010.01.006.Search in Google Scholar PubMed

Bekinschtein, P., Kent, B.A., Oomen, C.A., Clemenson, G.D., Gage, F.H., Saksida, L.M., and Bussey, T.J. (2013). BDNF in the dentate gyrus is required for consolidation of “pattern-separated” memories. Cell Rep. 5: 759–768, https://doi.org/10.1016/j.celrep.2013.09.027.Search in Google Scholar PubMed PubMed Central

Bekinschtein, P., Oomen, C.A., Saksida, L.M., and Bussey, T.J. (2011). Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable? Semin. Cell Dev. Biol. 22: 536–542, https://doi.org/10.1016/j.semcdb.2011.07.002.Search in Google Scholar PubMed

Ben-Zeev, T., Hirsh, T., Weiss, I., Gornstein, M., and Okun, E. (2020). The effects of high-intensity functional training (HIFT) on spatial learning, visual pattern separation and attention span in adolescents. Front. Behav. Neurosci. 14: 1–11, https://doi.org/10.3389/fnbeh.2020.577390.Search in Google Scholar PubMed PubMed Central

Bennett, I.J., Huffman, D.J., and Stark, C.E.L. (2015). Limbic tract integrity contributes to pattern separation performance across the lifespan. Cerebr. Cortex 25: 2988–2999, https://doi.org/10.1093/cercor/bhu093.Search in Google Scholar PubMed PubMed Central

Bennett, I.J. and Stark, C.E.L. (2016). Mnemonic discrimination relates to perforant path integrity: an ultra-high resolution diffusion tensor imaging study. Neurobiol. Learn. Mem. 129: 107–112, https://doi.org/10.1016/j.nlm.2015.06.014.Search in Google Scholar PubMed PubMed Central

Bernstein, E.E., Brühl, A., Kley, H., Heinrichs, N., and McNally, R.J. (2020). Mnemonic discrimination in treatment-seeking adults with and without PTSD. Behav. Res. Ther. 131: 103650, https://doi.org/10.1016/j.brat.2020.103650.Search in Google Scholar PubMed

Bernstein, E.E. and McNally, R.J. (2018). Exploring behavioral pattern separation and risk for emotional disorders. J. Anxiety Disord. 59: 27–33, https://doi.org/10.1016/j.janxdis.2018.08.006.Search in Google Scholar PubMed

Bernstein, E.E. and McNally, R.J. (2019). Examining the effects of exercise on pattern separation and the moderating effects of mood symptoms. Behav. Ther. 50: 582–593, https://doi.org/10.1016/j.beth.2018.09.007.Search in Google Scholar PubMed

Bliss, T.V.P. and Collingridge, G.L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31–39, https://doi.org/10.1038/361031a0.Search in Google Scholar PubMed

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., et al.. (2018). Human hippocampal neurogenesis persists throughout aging. Cell Stem Cell 22: 589–599.e5, https://doi.org/10.1016/j.stem.2018.03.015.Search in Google Scholar PubMed PubMed Central

Bolz, L., Heigele, S., and Bischofberger, J. (2016). Running improves pattern separation during novel object recognition. Brain Plast. 1: 129–141, https://doi.org/10.3233/BPL-150010.Search in Google Scholar PubMed PubMed Central

Borsini, A., Zunszain, P.A., Thuret, S., and Pariante, C.M. (2015). The role of inflammatory cytokines as key modulators of neurogenesis. Cell Press 38: 145–157, https://doi.org/10.1016/j.tins.2014.12.006.Search in Google Scholar PubMed

Bouret, S. and Sara, S.J. (2005). Network reset: a simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci. 28: 574–582, https://doi.org/10.1016/j.tins.2005.09.002.Search in Google Scholar PubMed

Bramham, C.R. and Messaoudi, E. (2005). BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog. Neurobiol. 76: 99–125, https://doi.org/10.1016/j.pneurobio.2005.06.003.Search in Google Scholar PubMed

Brolinson, P.G. and Elliott, D. (2007). Exercise and the immune system. Clin. Sports Med. 26: 311–319, https://doi.org/10.1016/j.csm.2007.04.011.Search in Google Scholar PubMed

Broussard, S.R., Mccusker, R.H., Novakofski, J.E., Strle, K., Shen, W.H., Johnson, R.W., Freund, G.G., Dantzer, R., and Kelley, K.W. (2003). Cytokine-hormone interactions: tumor necrosis factor α impairs biologic activity and downstream activation signals of the insulin-like growth factor I receptor in myoblasts. Endocrinology 144: 2988–2996, https://doi.org/10.1210/en.2003-0087.Search in Google Scholar PubMed

Burke, S.N., Turner, S.M., Desrosiers, C.L., Johnson, S.A., and Maurer, A.P. (2018). Perforant path fiber loss results in mnemonic discrimination task deficits in young rats. Front. Syst. Neurosci. 12: 61, https://doi.org/10.3389/fnsys.2018.00061.Search in Google Scholar PubMed PubMed Central

Burzynska, A.Z., Jiao, Y., Knecht, A.M., Fanning, J., Awick, E.A., Chen, T., Gothe, N., Voss, M.W., McAuley, E., and Kramer, A.F. (2017). White matter integrity declined over 6-months, but dance intervention improved integrity of the fornix of older adults. Front. Aging Neurosci. 9: 59, https://doi.org/10.3389/fnagi.2017.00059.Search in Google Scholar PubMed PubMed Central

Calabrese, F., Rossetti, A.C., Racagni, G., Gass, P., Riva, M.A., and Molteni, R. (2014). Brain-derived neurotrophic factor: a bridge between inflammation and neuroplasticity. Front. Cell. Neurosci. 8: 430, https://doi.org/10.3389/fncel.2014.00430.Search in Google Scholar PubMed PubMed Central

Campbell, K.L., Campbell, P.T., Ulrich, C.M., Wener, M., Alfano, C.M., Foster-Schubert, K., Rudolph, R.E., Potter, J.D., and McTiernan, A. (2008). No reduction in C-reactive protein following a 12-month randomized controlled trial of exercise in men and women. Cancer Epidemiol. Biomarkers Prev. 17: 1714–1718, https://doi.org/10.1158/1055-9965.epi-08-0088.Search in Google Scholar PubMed PubMed Central

Campbell, P.T., Campbell, K.L., Wener, M.H., Wood, B.L., Potter, J.D., McTiernan, A., and Ulrich, C.M. (2009). A yearlong exercise intervention decreases CRP among obese postmenopausal women. Med. Sci. Sports Exerc. 41: 1533–1539, https://doi.org/10.1249/mss.0b013e31819c7feb.Search in Google Scholar PubMed PubMed Central

Cappon, J., Brasel, J.A., Mohan, S., and Cooper, D.M. (1994). Effect of brief exercise on circulating insulin-like growth factor I. J. Appl. Physiol. 76: 2490–2496, https://doi.org/10.1152/jappl.1994.76.6.2490.Search in Google Scholar PubMed

Carro, E., Nuñez, A., Busiguina, S., and Torres-Aleman, I. (2000). Circulating insulin-like growth factor I mediates effects of exercise on the brain. J. Neurosci. 20: 2926–2933, https://doi.org/10.1523/jneurosci.20-08-02926.2000.Search in Google Scholar

Caspersen, C., Powell, K., and Christenson, G. (1985). Physical activity, exercise, and physical fitness: definitions and distinctions for health-related research. Public Health Rep. 100: 126–131.Search in Google Scholar

Cassilhas, R.C., Tufik, S., and De Mello, M.T. (2016). Physical exercise, neuroplasticity, spatial learning and memory. Cell. Mol. Life Sci. 73: 975–983, https://doi.org/10.1007/s00018-015-2102-0.Search in Google Scholar PubMed

Castrén, E. (2013). Neuronal plasticity and antidepressant actions. Cell Press 36: 259–267.10.1016/j.tins.2012.12.010Search in Google Scholar PubMed PubMed Central

Castrén, E. and Hen, R. (2013). Neuronal plasticity and antidepressant actions. Cell Press 36: 259–267.10.1016/j.tins.2012.12.010Search in Google Scholar

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., et al.. (2010). A neuroimaging investigation of the association between aerobic fitness, hippocampal volume, and memory performance in preadolescent children. Brain Res. 1358: 172–183, https://doi.org/10.1016/j.brainres.2010.08.049.Search in Google Scholar PubMed PubMed Central

Chang, Y.K., Labban, J.D., Gapin, J.I., and Etnier, J.L. (2012). The effects of acute exercise on cognitive performance: a meta-analysis. Brain Res. 1453: 87–101, https://doi.org/10.1016/j.brainres.2012.02.068.Search in Google Scholar PubMed

Chen, H.I., Lin, L.C., Yu, L., Liu, Y.F., Kuo, Y.M., Huang, A.M., Chuang, J.I., Wu, F. Sen, Liao, P.C., and Jen, C.J. (2008). Treadmill exercise enhances passive avoidance learning in rats: the role of down-regulated serotonin system in the limbic system. Neurobiol. Learn. Mem. 89: 489–496, https://doi.org/10.1016/j.nlm.2007.08.004.Search in Google Scholar PubMed

Chen, M.J., Nguyen, T.V., Pike, C., and Russo-Neustadt, A. (2007). Norepinephrine induces BDNF and activates the PI-3K and MAPK cascades in embryonic hippocampal neurons. Cell. Signal. 19: 114–128, https://doi.org/10.1016/j.cellsig.2006.05.028.Search in Google Scholar PubMed

Chennaoui, M., Drogou, C., and Gomez-Merino, D. (2008). Effects of physical training on IL-1p, IL-6 and IL-lra concentrations in various brain areas of the rat. Eur. Cytokine Netw. 19: 8–14, https://doi.org/10.1684/ecn.2008.0115.Search in Google Scholar PubMed

Chennaoui, M., Grimaldi, B., Fillion, M.P., Bonnin, A., Drogou, C., Fillion, G., and Guezennec, C.Y. (2000). Effects of physical training on functional activity of 5-HT(1B) receptors in rat central nervous system: role of 5-HT-moduline. Naunyn. Schmiedebergs. Arch. Pharmacol. 361: 600–604, https://doi.org/10.1007/s002100000242.Search in Google Scholar PubMed

Choi, S.H., Bylykbashi, E., Chatila, Z.K., Lee, S.W., Pulli, B., Clemenson, G.D., Kim, E., Rompala, A., Oram, M.K., Asselin, C., et al.. (2018). Combined adult neurogenesis and BDNF mimic exercise effects on cognition in an Alzheimer’s mouse model. Science 361: 1–15, https://doi.org/10.1126/science.aan8821.Search in Google Scholar PubMed PubMed Central

Christiansen, T., Paulsen, S.K., Bruun, J.M., Pedersen, S.B., and Richelsen, B. (2010). Exercise training versus diet-induced weight-loss on metabolic risk factors and inflammatory markers in obese subjects: a 12-week randomized intervention study. Am. J. Physiol. Endocrinol. Metab. 298: 824–831, https://doi.org/10.1152/ajpendo.00574.2009.Search in Google Scholar PubMed

Church, D.D., Hoffman, J.R., Mangine, G.T., Jajtner, A.R., Townsend, J.R., Beyer, K.S., Wang, R., La Monica, M.B., Fukuda, D.H., and Stout, J.R. (2016). Comparison of high-intensity vs. high-volume resistance training on the BDNF response to exercise. J. Appl. Physiol. 121: 123–128, https://doi.org/10.1152/japplphysiol.00233.2016.Search in Google Scholar PubMed

Church, T.S., Barlow, C.E., Earnest, C.P., Kampert, J.B., Priest, E.L., and Blair, S.N. (2002). Associations between cardiorespiratory fitness and C-reactive protein in men. Arterioscler. Thromb. Vasc. Biol. 22: 1869–1876, https://doi.org/10.1161/01.atv.0000036611.77940.f8.Search in Google Scholar PubMed

Cirillo, J., Lavender, A.P., Ridding, M.C., and Semmler, J.G. (2009). Motor cortex plasticity induced by paired associative stimulation is enhanced in physically active individuals. J. Physiol. 587: 5831–5842, https://doi.org/10.1113/jphysiol.2009.181834.Search in Google Scholar PubMed PubMed Central

Clark, P.J., Brzezinska, W.J., Puchalski, E.K., Krone, D.A., and Rhodes, J.S. (2009). Functional analysis of neurovascular adaptations to exercise in the dentate gyrus of young adult mice associated with cognitive gain. Hippocampus 19: 937–950, https://doi.org/10.1002/hipo.20543.Search in Google Scholar PubMed PubMed Central

Clelland, C.D., Choi, M., Romberg, C., Clemenson, G.D., Fragniere, A., Tyers, P., Jessberger, S., Saksida, L.M., Barker, R.A., Gage, F.H., et al.. (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325: 210–213, https://doi.org/10.1126/science.1173215.Search in Google Scholar PubMed PubMed Central

Coolen, L.M. and Grattan, D.R. (2019). Geyer, M.A., Ellenbroek, B.A., Marsden, C.A., Barnes, T.R.E., and Andersen, S.L. (Eds.), Neuroendocrine regulation of behavior. Springer, Switzerland.10.1007/978-3-030-38720-4Search in Google Scholar

Cotman, C.W. and Berchtold, N.C. (2002). Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 25: 295–301, https://doi.org/10.1016/s0166-2236(02)02143-4.Search in Google Scholar

Cotman, C.W., Berchtold, N.C., and Christie, L.A. (2007). Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci. 30: 464–472, https://doi.org/10.1016/j.tins.2007.06.011.Search in Google Scholar PubMed

Crawford, L.K., Li, H., Zou, L., Wei, G.X., and Loprinzi, P.D. (2020). Hypothesized mechanisms through which exercise may attenuate memory interference. Medicina (B. Aires) 56: 1–15, https://doi.org/10.3390/medicina56030129.Search in Google Scholar PubMed PubMed Central

Creer, D.J., Romberg, C., Saksida, L.M., Van Praag, H., and Bussey, T.J. (2010). Running enhances spatial pattern separation in mice. Proc. Natl. Acad. Sci. U. S. A. 107: 2367–2372, https://doi.org/10.1073/pnas.0911725107.Search in Google Scholar PubMed PubMed Central

Cunningham, T.J., Leal, S.L., Yassa, M.A., and Payne, J.D. (2018). Post-encoding stress enhances mnemonic discrimination of negative stimuli. Learn. Mem. 25: 611–619, https://doi.org/10.1101/lm.047498.118.Search in Google Scholar PubMed PubMed Central

Currie, J., Ramsbottom, R., Ludlow, H., Nevill, A., and Gilder, M. (2009). Cardio-respiratory fitness, habitual physical activity and serum brain derived neurotrophic factor (BDNF) in men and women. Neurosci. Lett. 451: 152–155, https://doi.org/10.1016/j.neulet.2008.12.043.Search in Google Scholar PubMed

Czarkowska-Paczek, B., Bartlomiejczyk, I., and Przybylski, J. (2006). The serum levels of growth factors: PDGF, TGF-BETA and VEGF are increased after strenuous physical exercise, Retrieved June 28, 2021, from www.jpp.krakow.pl.Search in Google Scholar

Czerniawski, J. and Guzowski, J.F. (2014). Acute neuroinflammation impairs context discrimination memory and disrupts pattern separation processes in hippocampus. J. Neurosci. 34: 12470–12480, https://doi.org/10.1523/jneurosci.0542-14.2014.Search in Google Scholar PubMed PubMed Central

Czerniawski, J., Miyashita, T., Lewandowski, G., and Guzowski, J.F. (2015). Systemic lipopolysaccharide administration impairs retrieval of context-object discrimination, but not spatial, memory: evidence for selective disruption of specific hippocampus-dependent memory functions during acute neuroinflammation. Brain Behav. Immun. 44: 159–166, https://doi.org/10.1016/j.bbi.2014.09.014.Search in Google Scholar PubMed PubMed Central

Dallagnol, K.M.C., Remor, A.P., da Silva, R.A., Prediger, R.D., Latini, A., and Aguiar, A.S. (2017). Running for REST: physical activity attenuates neuroinflammation in the hippocampus of aged mice. Brain Behav. Immun. 61: 31–35, https://doi.org/10.1016/j.bbi.2016.07.159.Search in Google Scholar PubMed

Das, T., Ivleva, E.I., Wagner, A.D., Stark, C.E.L., and Tamminga, C.A. (2014). Loss of pattern separation performance in schizophrenia suggests dentate gyrus dysfunction. Schizophr. Res. 159: 193–197, https://doi.org/10.1016/j.schres.2014.05.006.Search in Google Scholar PubMed PubMed Central

De la Rosa, A., Solana, E., Corpas, R., Bartrés-Faz, D., Pallàs, M., Vina, J., Sanfeliu, C., and Gomez-Cabrera, M.C. (2019). Long-term exercise training improves memory in middle-aged men and modulates peripheral levels of BDNF and Cathepsin B. Sci. Rep. 91: 1–11, https://doi.org/10.1038/s41598-019-40040-8.Search in Google Scholar PubMed PubMed Central

de Miranda, A.S., Zhang, C.J., Katsumoto, A., and Teixeira, A.L. (2017). Hippocampal adult neurogenesis: does the immune system matter? J. Neurol. Sci. 372: 482–495, https://doi.org/10.1016/j.jns.2016.10.052.Search in Google Scholar PubMed

de Quervain, D.J.F., Aerni, A., Schelling, G., and Roozendaal, B. (2009). Glucocorticoids and the regulation of memory in health and disease. Front. Neuroendocrinol. 30: 358–370, https://doi.org/10.1016/j.yfrne.2009.03.002.Search in Google Scholar PubMed

Deng, W., Aimone, J.B., and Gage, F.H. (2010). New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci. 11: 339–350, https://doi.org/10.1038/nrn2822.Search in Google Scholar PubMed PubMed Central

Déry, N., Pilgrim, M., Gibala, M., Gillen, J., Martin Wojtowicz, J., MacQueen, G., and Becker, S. (2013). Adult hippocampal neurogenesis reduces memory interference in humans: opposing effects of aerobic exercise and depression. Front. Neurosci. 7: 66, https://doi.org/10.3389/fnins.2013.00066.Search in Google Scholar PubMed PubMed Central

Dief, A.E., Samy, D.M., and Dowedar, F.I. (2015). Impact of exercise and vitamin B1 intake on hippocampal brain-derived neurotrophic factor and spatial memory performance in a rat model of stress. J. Nutr. Sci. Vitaminol. 61: 1–7, https://doi.org/10.3177/jnsv.61.1.Search in Google Scholar PubMed

Dillon, D.G. and Pizzagalli, D.A. (2018). Mechanisms of memory disruption in depression. Trends Neurosci. 41: 137–149, https://doi.org/10.1016/j.tins.2017.12.006.Search in Google Scholar PubMed PubMed Central

Ding, Q., Vaynman, S., Akhavan, M., Ying, Z., and Gomez-Pinilla, F. (2006a). Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neuroscience 140: 823–833, https://doi.org/10.1016/j.neuroscience.2006.02.084.Search in Google Scholar PubMed

Ding, Y.-H., Li, J., Zhou, Y., Rafols, J., Clark, J., and Ding, Y. (2006b). Cerebral angiogenesis and expression of angiogenic factors in aging rats after exercise. Curr. Neurovasc. Res. 3: 15–23, https://doi.org/10.2174/156720206775541787.Search in Google Scholar PubMed

Dinoff, A., Herrmann, N., Swardfager, W., and Lanct, K.L. (2017). The effect of acute exercise on blood concentrations of brain-derived neurotrophic factor in healthy adults : a meta-analysis. Eur. J. Neurosci. 46: 1635–1646, https://doi.org/10.1111/ejn.13603.Search in Google Scholar PubMed

Donges, C.E., Duffield, R., and Drinkwater, E.J. (2010). Effects of resistance or aerobic exercise training on interleukin-6, C-reactive protein, and body composition. Med. Sci. Sports Exerc. 42: 304–313, https://doi.org/10.1249/mss.0b013e3181b117ca.Search in Google Scholar

Droste, S.K., Gesing, A., Ulbricht, S., Müller, M.B., Linthorst, A.C.E., and Reul, J.M.H.M. (2003). Effects of long-term voluntary exercise on the mouse hypothalamic-pituitary-adrenocortical axis. Endocrinology 144: 3012–3023, https://doi.org/10.1210/en.2003-0097.Search in Google Scholar PubMed

Duclos, M. and Tabarin, A. (2011). Exercise, training, and the hypothalamo–pituitary–adrenal axis. Boston, MA: Springer, pp. 9–15.10.1007/978-1-4419-7014-5_2Search in Google Scholar

Duggan, C., Xiao, L., Wang, C.Y., and McTiernan, A. (2014). Effect of a 12-month exercise intervention on serum biomarkers of angiogenesis in postmenopausal women: a randomized controlled trial. Cancer Epidemiol. Biomarkers Prev. 23: 648–657, https://doi.org/10.1158/1055-9965.epi-13-1155.Search in Google Scholar

Eadie, B.D., Cushman, J., Kannangara, T.S., Fanselow, M.S., and Christie, B.R. (2012). NMDA receptor hypofunction in the dentate gyrus and impaired context discrimination in adult Fmr1 knockout mice. Hippocampus 22: 241–254, https://doi.org/10.1002/hipo.20890.Search in Google Scholar PubMed

Ebrahimi, S., Rashidy-Pour, A., Vafaei, A.A., and Akhavan, M.M. (2010). Central β-adrenergic receptors play an important role in the enhancing effect of voluntary exercise on learning and memory in rat. Behav. Brain Res. 208: 189–193, https://doi.org/10.1016/j.bbr.2009.11.032.Search in Google Scholar PubMed

El-Sayes, J., Harasym, D., Turco, C.V., Locke, M.B., and Nelson, A.J. (2019). Exercise-induced neuroplasticity: a mechanistic model and prospects for promoting plasticity. Neuroscientist 25: 65–85, https://doi.org/10.1177/1073858418771538.Search in Google Scholar PubMed

Erickson, K.I., Prakash, R.S., Voss, M.W., Chaddock, L., Hu, L., Morris, K.S., White, S.M., Wójcicki, T.R., McAuley, E., and Kramer, A.F. (2009). Aerobic fitness is associated with hippocampal volume in elderly humans. Hippocampus 19: 1030–1039, https://doi.org/10.1002/hipo.20547.Search in Google Scholar PubMed PubMed Central

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., et al.. (2011). Exercise training increases size of hippocampus and improves memory. Proc. Natl. Acad. Sci. U. S. A. 108: 3017–3022, https://doi.org/10.1073/pnas.1015950108.Search in Google Scholar PubMed PubMed Central

Eriksson, P.S., Perfilieva, E., Björk-Eriksson, T., Alborn, A.M., Nordborg, C., Peterson, D.A., and Gage, F.H. (1998). Neurogenesis in the adult human hippocampus. Nat. Med. 4: 1313–1317, https://doi.org/10.1038/3305.Search in Google Scholar PubMed

Eyo, U.B., Peng, J., Swiatkowski, P., Mukherjee, A., Bispo, A., and Wu, L.J. (2014). Neuronal hyperactivity recruits microglial processes via neuronal NMDA receptors and microglial P2Y12 receptors after status epilepticus. J. Neurosci. 34: 10528–10540, https://doi.org/10.1523/jneurosci.0416-14.2014.Search in Google Scholar PubMed PubMed Central

Eyre, H. and Baune, B.T. (2012). Neuroimmunological effects of physical exercise in depression. Brain Behav. Immun. 26: 251–266, https://doi.org/10.1016/j.bbi.2011.09.015.Search in Google Scholar

Fabel, K., Fabel, K., Tam, B., Kaufer, D., Baiker, A., Simmons, N., Kuo, C.J., and Palmer, T.D. (2003). VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur. J. Neurosci. 18: 2803–2812, https://doi.org/10.1111/j.1460-9568.2003.03041.x.Search in Google Scholar

Faghihi, F. and Moustafa, A.A. (2015). A computational model of pattern separation efficiency in the dentate gyrus with implications in schizophrenia. Front. Syst. Neurosci. 9, https://doi.org/10.3389/fnsys.2015.00042.Search in Google Scholar

Farmer, J., Zhao, X., Van Praag, H., Wodtke, K., Gage, F.H., and Christie, B.R. (2004). Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley-dawley rats in vivo. Neuroscience 124: 71–79, https://doi.org/10.1016/j.neuroscience.2003.09.029.Search in Google Scholar

Ferreira, A.F.B., Real, C.C., Rodrigues, A.C., Alves, A.S., and Britto, L.R.G. (2011). Short-term, moderate exercise is capable of inducing structural, bdnf-independent hippocampal plasticity. Brain Res. 1425: 111–122, https://doi.org/10.1016/j.brainres.2011.10.004.Search in Google Scholar

Firth, J., Stubbs, B., Vancampfort, D., Schuch, F., Lagopoulos, J., Rosenbaum, S., and Ward, P.B. (2018). Effect of aerobic exercise on hippocampal volume in humans: a systematic review and meta-analysis. NeuroImage 166: 230–238, https://doi.org/10.1016/j.neuroimage.2017.11.007.Search in Google Scholar

Ford, E.S. (2002). Does exercise reduce inflammation? Physical activity and C-reactive protein among U.S. adults. Epidemiology 13: 561–568, https://doi.org/10.1097/00001648-200209000-00012.Search in Google Scholar

Fordyce, D.E. and Farrar, R.P. (1991). Physical activity effects on hippocampal and parietal cortical cholinergic function and spatial learning in F344 rats. Behav. Brain Res. 43: 115–123, https://doi.org/10.1016/s0166-4328(05)80061-0.Search in Google Scholar

Fourrier, C., Singhal, G., and Baune, B.T. (2019). Neuroinflammation and cognition across psychiatric conditions. CNS Spectr. 24: 4–15, https://doi.org/10.1017/s1092852918001499.Search in Google Scholar

França, T.F.A., Bitencourt, A.M., Maximilla, N.R., Barros, D.M., and Monserrat, J.M. (2017). Hippocampal neurogenesis and pattern separation: a meta-analysis of behavioral data. Hippocampus 27: 937–950, https://doi.org/10.1002/hipo.22746.Search in Google Scholar PubMed

Gavin, T.P., Robinson, C.B., Yeager, R.C., England, J.A., Nifong, L.W., and Hickner, R.C. (2004). Angiogenic growth factor response to acute systemic exercise in human skeletal muscle. J. Appl. Physiol. 96: 19–24, https://doi.org/10.1152/japplphysiol.00748.2003.Search in Google Scholar

Ge, S., Yang, C.-H., Hsu, K.-S., Ming, G.-L., and Song, H. (2007). A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54: 559–566, https://doi.org/10.1016/j.neuron.2007.05.002.Search in Google Scholar

Geffken, D.F., Cushman, M., Burke, G.L., Polak, J.F., Sakkinen, P.A., and Tracy, R.P. (2001). Association between physical activity and markers of inflammation in a healthy elderly population. Am. J. Epidemiol. 153: 242–250, https://doi.org/10.1093/aje/153.3.242.Search in Google Scholar

Gemma, C. and Bachstetter, A.D. (2013). The role of microglia in adult hippocampal neurogenesis. Front. Cell. Neurosci. 7: 229, https://doi.org/10.3389/fncel.2013.00229.Search in Google Scholar

Goekint, M., Bos, I., Heyman, E., Meeusen, R., Michotte, Y., and Sarre, S. (2012). Acute running stimulates hippocampal dopaminergic neurotransmission in rats, but has no influence on brain-derived neurotrophic factor. J. Appl. Physiol. 112: 535–541, https://doi.org/10.1152/japplphysiol.00306.2011.Search in Google Scholar

Goel, N., Workman, J.L., Lee, T.T., Innala, L., and Viau, V. (2014). Sex differences in the HPA axis. Compr. Physiol. 4: 1121–1155, https://doi.org/10.1002/cphy.c130054.Search in Google Scholar

Gomez-Merino, D., Béquet, F., Berthelot, M., Chennaoui, M., and Guezennec, C.Y. (2001). Site-dependent effects of an acute intensive exercise on extracellular 5-HT and 5-HIAA levels in rat brain. Neurosci. Lett. 301: 143–146, https://doi.org/10.1016/s0304-3940(01)01626-3.Search in Google Scholar

Gonzalez, P., Machado, I., Vilcaes, A., Caruso, C., Roth, G.A., Schiöth, H., Lasaga, M., and Scimonelli, T. (2013). Molecular mechanisms involved in interleukin 1-beta (IL-1β)-induced memory impairment. Modulation by alpha-melanocyte-stimulating hormone (α-MSH). Brain Behav. Immun. 34: 141–150, https://doi.org/10.1016/j.bbi.2013.08.007.Search in Google Scholar PubMed

Gorham, L.S. and Barch, D.M. (2020). White matter tract integrity, involvement in sports, and depressive symptoms in children. Child Psychiatry Hum. Dev. 51: 490–501, https://doi.org/10.1007/s10578-020-00960-3.Search in Google Scholar PubMed PubMed Central

Gorham, L.S., Jernigan, T., Hudziak, J., and Barch, D.M. (2019). Involvement in sports, hippocampal volume, and depressive symptoms in children. Biol. Psychiatry Cogn. Neurosci. Neuroimaging 4: 484–492, https://doi.org/10.1016/j.bpsc.2019.01.011.Search in Google Scholar PubMed PubMed Central

Gottmann, K., Mittmann, T., and Lessmann, V. (2009). BDNF signaling in the formation, maturation and plasticity of glutamatergic and GABAergic synapses. Exp. Brain Res. 199: 203–234, https://doi.org/10.1007/s00221-009-1994-z.Search in Google Scholar

Greenwood, B.N., Foley, T.E., Day, H.E.W., Burhans, D., Brooks, L., Campeau, S., and Fleshner, M. (2005). Wheel running alters serotonin (5-HT) transporter, 5-HT1A, 5-HT1B, and alpha1b-adrenergic receptor mRNA in the rat raphe nuclei. Biol. Psychiatry 57: 559–568, https://doi.org/10.1016/j.biopsych.2004.11.025.Search in Google Scholar

Griffin, É.W., Mullally, S., Foley, C., Warmington, S.A., O’Mara, S.M., and Kelly, Á.M. (2011). Aerobic exercise improves hippocampal function and increases BDNF in the serum of young adult males. Physiol. Behav. 104: 934–941, https://doi.org/10.1016/j.physbeh.2011.06.005.Search in Google Scholar

Gubba, E.M., Fawcett, J.W., and Herbert, J. (2004). The effects of corticosterone and dehydroepiandrosterone on neurotrophic factor mRNA expression in primary hippocampal and astrocyte cultures. Mol. Brain Res. 127: 48–59, https://doi.org/10.1016/j.molbrainres.2004.05.004.Search in Google Scholar

Hajszan, T., Milner, T.A., and Leranth, C. (2007). Sex steroids and the dentate gyrus. Prog. Brain Res. 163C: 399–816, https://doi.org/10.1016/s0079-6123(07)63023-4.Search in Google Scholar

Hamer, M., Molloy, G.J., de Oliveira, C., and Demakakos, P. (2009). Leisure time physical activity, risk of depressive symptoms, and inflammatory mediators: the English Longitudinal Study of Ageing. Psychoneuroendocrinology 34: 1050–1055, https://doi.org/10.1016/j.psyneuen.2009.02.004.Search in Google Scholar

Hammett, C.J.K., Oxenham, H.C., Baldi, J.C., Doughty, R.N., Ameratunga, R., French, J.K., White, H.D., and Stewart, R.A.H. (2004). Effect of six months’ exercise training on C-reactive protein levels in healthy elderly subjects [2]. J. Am. Coll. Cardiol. 44: 2411–2413, https://doi.org/10.1016/j.jacc.2004.09.030.Search in Google Scholar

Hansson, A.C., Sommer, W., Rimondini, R., Andbjer, B., Strömberg, I., and Fuxe, K. (2003). c-fos reduces corticosterone-mediated effects on neurotrophic factor expression in the rat hippocampal CA1 region. J. Neurosci. 23: 6013–6022, https://doi.org/10.1523/jneurosci.23-14-06013.2003.Search in Google Scholar

Harley, C.W. (2007). Norepinephrine and the dentate gyrus. Prog. Brain Res. 163: 299–318, https://doi.org/10.1016/s0079-6123(07)63018-0.Search in Google Scholar

He, S.B., Tang, W.G., Tang, W.J., Kao, X.L., Zhang, C.G., and Wong, X.T. (2012). Exercise intervention may prevent depression. Int. J. Sports Med. 33: 525–530, https://doi.org/10.1055/s-0032-1306325.Search in Google Scholar PubMed

Heinze, K., Cumming, J., Dosanjh, A., Palin, S., Poulton, S., Bagshaw, A.P., and Broome, M.R. (2020). Neurobiological evidence of longer-term physical activity interventions on mental health outcomes and cognition in young people: a systematic review of randomised controlled trials. Neurosci. Biobehav. Rev. 120: 431–441.10.1016/j.neubiorev.2020.10.014Search in Google Scholar

Heisz, J.J., Clark, I.B., Bonin, K., Paolucci, E.M., Michalski, B., Becker, S., and Fahnestock, M. (2017). The effects of physical exercise and cognitive training on memory and neurotrophic factors. J. Cogn. Neurosci. 29: 1895–1907, https://doi.org/10.1162/jocn_a_01164.Search in Google Scholar

Herting, M.M. and Nagel, B.J. (2012). Aerobic fitness relates to learning on a virtual Morris Water Task and hippocampal volume in adolescents. Behav. Brain Res. 233: 517–525, https://doi.org/10.1016/j.bbr.2012.05.012.Search in Google Scholar

Hill, E.E., Zack, E., Battaglini, C., Viru, M., Viru, A., and Hackney, A.C. (2008). Exercise and circulating cortisol levels: the intensity threshold effect. J. Endocrinol. Invest. 31: 587–591, https://doi.org/10.1007/bf03345606.Search in Google Scholar

Hötting, K., Schickert, N., Kaiser, J., Röder, B., and Schmidt-Kassow, M. (2016). The effects of acute physical exercise on memory, peripheral BDNF, and cortisol in young adults. Neural Plast.: 1–12.10.1155/2016/6860573Search in Google Scholar

Hoyer, D., Hannon, J.P., and Martin, G.R. (2002). Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol. Biochem. Behav. 71: 533–554, https://doi.org/10.1016/s0091-3057(01)00746-8.Search in Google Scholar

Huang, T., Larsen, K.T., Ried-Larsen, M., Møller, N.C., and Andersen, L.B. (2014). The effects of physical activity and exercise on brain-derived neurotrophic factor in healthy humans: a review. Scand. J. Med. Sci. Sports 24: 1–10, https://doi.org/10.1111/sms.12069.Search in Google Scholar PubMed

Hummos, A., Franklin, C.C., and Nair, S.S. (2014). Intrinsic mechanisms stabilize encoding and retrieval circuits differentially in a hippocampal network model. Hippocampus 24: 1430–1448, https://doi.org/10.1002/hipo.22324.Search in Google Scholar PubMed PubMed Central

Ikrar, T., Guo, N., He, K., Besnard, A., Levinson, S., Hill, A., Lee, H.-K., Hen, R., Xu, X., Sahay, A., et al.. (2013). Adult neurogenesis modifies excitability of the dentate gyrus. Front. Neural Circuits 7, https://doi.org/10.3389/fncir.2013.00204.Search in Google Scholar PubMed PubMed Central

Inoue, K., Hanaoka, Y., Nishijima, T., Okamoto, M., Chang, H., Saito, T., and Soya, H. (2015a). Long-term mild exercise training enhances hippocampus-dependent memory in rats. Int. J. Sports Med. 36: 280–285, https://doi.org/10.1055/s-0034-1390465.Search in Google Scholar PubMed

Inoue, K., Okamoto, M., Shibato, J., Lee, M.C., Matsui, T., Rakwal, R., and Soya, H. (2015b). Long-term mild, rather than intense, exercise enhances adult hippocampal neurogenesis and greatly changes the transcriptomic profile of the hippocampus. PLoS One 10, https://doi.org/10.1371/journal.pone.0133089.Search in Google Scholar

Itou, Y., Nochi, R., Kuribayashi, H., Saito, Y., and Hisatsune, T. (2011). Cholinergic activation of hippocampal neural stem cells in aged dentate gyrus. Hippocampus 21: 446–459, https://doi.org/10.1002/hipo.20761.Search in Google Scholar

Ivy, A.S., Rodriguez, F.G., Garcia, C., Chen, M.J., and Russo-Neustadt, A.A. (2003). Noradrenergic and serotonergic blockade inhibits BDNF mRNA activation following exercise and antidepressant. Pharmacol. Biochem. Behav. 75: 81–88, https://doi.org/10.1016/s0091-3057(03)00044-3.Search in Google Scholar

Jacobs, B.L. and Azmitia, E.C. (1992). Structure and function of the brain serotonin system. Physiol. Rev. 72: 165–230, https://doi.org/10.1152/physrev.1992.72.1.165.Search in Google Scholar PubMed

Jahangiri, Z., Gholamnezhad, Z., and Hosseini, M. (2019). Neuroprotective effects of exercise in rodent models of memory deficit and Alzheimer’s. Metab. Brain Dis. 34: 21–37, https://doi.org/10.1007/s11011-018-0343-y.Search in Google Scholar PubMed

Jeon, Y.K. and Ha, C.H. (2017). The effect of exercise intensity on brain derived neurotrophic factor and memory in adolescents. Environ. Health Prev. Med. 22: 22–27, https://doi.org/10.1186/s12199-017-0643-6.Search in Google Scholar PubMed PubMed Central

Jiang, A., Tran, T.T., Madison, F.N., and Bakker, A. (2019). Acute stress-induced cortisol elevation during memory consolidation enhances pattern separation. Learn. Mem. 26: 121–127, https://doi.org/10.1101/lm.048546.118.Search in Google Scholar PubMed PubMed Central

Johnson, T.K., Belcher, D.J., Sousa, C.A., Carzoli, J.P., Visavadiya, N.P., Khamoui, A.V., Whitehurst, M., and Zourdos, M.C. (2020). Low-volume acute multi-joint resistance exercise elicits a circulating brain-derived neurotrophic factor response but not a cathepsin B response in well-trained men. Appl. Physiol. Nutr. Metab. 45: 1–7, https://doi.org/10.1139/apnm-2019-0854.Search in Google Scholar PubMed

Kadoglou, N.P.E., Iliadis, F., Angelopoulou, N., Perrea, D., Ampatzidis, G., Liapis, C.D., and Alevizos, M. (2007). The anti-inflammatory effects of exercise training in patients with type 2 diabetes mellitus. Eur. J. Prev. Cardiol. 14: 837–843, https://doi.org/10.1097/hjr.0b013e3282efaf50.Search in Google Scholar PubMed

Kalafatakis, K., Russell, G.M., and Lightman, S.L. (2019). Mechanisms in endocrinology: does circadian and ultradian glucocorticoid exposure affect the brain? Eur. J. Endocrinol. 180: R73–R89, https://doi.org/10.1530/eje-18-0853.Search in Google Scholar

Kandola, A., Ashdown-Franks, G., Hendrikse, J., Sabiston, C.M., and Stubbs, B. (2019). Physical activity and depression: towards understanding the antidepressant mechanisms of physical activity. Neurosci. Biobehav. Rev. 107: 525–539, https://doi.org/10.1016/j.neubiorev.2019.09.040.Search in Google Scholar

Kandola, A., Hendrikse, J., Lucassen, P.J., and Yücel, M. (2016). Aerobic exercise as a tool to improve hippocampal plasticity and function in humans: practical implications for mental health treatment. Front. Hum. Neurosci. 10, https://doi.org/10.3389/fnhum.2016.00373.Search in Google Scholar

Kannangara, T.S., Eadie, B.D., Bostrom, C.A., Morch, K., Brocardo, P.S., and Christie, B.R. (2015). GluN2A-/- mice lack bidirectional synaptic plasticity in the dentate gyrus and perform poorly on spatial pattern separation tasks. Cerebr. Cortex 25: 2102–2113, https://doi.org/10.1093/cercor/bhu017.Search in Google Scholar

Keeler, J., Lambert, E., Olivola, M., Owen, J., Xia, J., Thuret, S., Himmerich, H., Cardi, V., and Treasure, J. (2021). Lower pattern recognition memory scores in anorexia nervosa. J. Eat. Disord. 9, https://doi.org/10.1186/s40337-021-00406-8.Search in Google Scholar

Kempadoo, K.A., Mosharov, E.V., Choi, S.J., Sulzer, D., and Kandel, E.R. (2016). Dopamine release from the locus coeruleus to the dorsal hippocampus promotes spatial learning and memory. Proc. Natl. Acad. Sci. U. S. A. 113: 14835–14840, https://doi.org/10.1073/pnas.1616515114.Search in Google Scholar

Kempermann, G., Gage, F.H., Aigner, L., Song, H., Curtis, M.A., Thuret, S., Kuhn, H.G., Jessberger, S., Frankland, P.W., Cameron, H.A., et al.. (2018). Human adult neurogenesis: evidence and remaining questions. Cell Stem Cell 23: 25–30, https://doi.org/10.1016/j.stem.2018.04.004.Search in Google Scholar

Kheirbek, M.A., Klemenhagen, K.C., Sahay, A., and Hen, R. (2012a). Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat. Neurosci. 15: 1613–1620, https://doi.org/10.1038/nn.3262.Search in Google Scholar

Kheirbek, M.A., Tannenholz, L., and Hen, R. (2012b). NR2B-dependent plasticity of adult-born granule cells is necessary for context discrimination. J. Neurosci. 32: 8696–8702, https://doi.org/10.1523/jneurosci.1692-12.2012.Search in Google Scholar

Kipnis, J., Cardon, M., Avidan, H., Lewitus, G.M., Mordechay, S., Rolls, A., Shani, Y., and Schwartz, M. (2004). Dopamine, through the extracellular signal-regulated kinase pathway, downregulates CD4+CD25+ regulatory T-cell activity: implications for neurodegeneration. J. Neurosci. 24: 6133–6143, https://doi.org/10.1523/jneurosci.0600-04.2004.Search in Google Scholar

Kitamura, T., Mishina, M., and Sugiyama, H. (2003). Enhancement of neurogenesis by running wheel exercises is suppressed in mice lacking NMDA receptor ε1 subunit. Neurosci. Res. 47: 55–63, https://doi.org/10.1016/s0168-0102(03)00171-8.Search in Google Scholar

Kleemeyer, M.M., Kühn, S., Prindle, J., Bodammer, N.C., Brechtel, L., Garthe, A., Kempermann, G., Schaefer, S., and Lindenberger, U. (2016). Changes in fitness are associated with changes in hippocampal microstructure and hippocampal volume among older adults. Neuroimage 131: 155–161, https://doi.org/10.1016/j.neuroimage.2015.11.026.Search in Google Scholar PubMed

Klempin, F., Beis, D., Mosienko, V., Kempermann, G., Bader, M., and Alenina, N. (2013). Serotonin is required for exercise-induced adult hippocampal neurogenesis. J. Neurosci. 33: 8270–8275, https://doi.org/10.1523/jneurosci.5855-12.2013.Search in Google Scholar PubMed PubMed Central

Knaepen, K., Goekint, M., Heyman, E.M., and Meeusen, R. (2010). Neuroplasticity-exercise-induced response of peripheral brain-derived neurotrophic factor: a systematic review of experimental studies in human subjects. Sports Med. 40, https://doi.org/10.2165/11534530-000000000-00000.Search in Google Scholar PubMed

Knierim, J.J. (2015). The hippocampus. Curr. Biol. 25: 1116–1121, https://doi.org/10.1016/j.cub.2015.10.049.Search in Google Scholar PubMed

Knoth, R., Singec, I., Ditter, M., Pantazis, G., Capetian, P., Meyer, R.P., Horvat, V., Volk, B., and Kempermann, G. (2010). Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS One 5, https://doi.org/10.1371/journal.pone.0008809.Search in Google Scholar PubMed PubMed Central

Kohman, R.A., Bhattacharya, T.K., Wojcik, E., and Rhodes, J.S. (2013). Exercise reduces activation of microglia isolated from hippocampus and brain of aged mice. J. Neuroinflammation 10: 1–9, https://doi.org/10.1186/1742-2094-10-114.Search in Google Scholar PubMed PubMed Central

Kohut, M.L., McCann, D.A., Russell, D.W., Konopka, D.N., Cunnick, J.E., Franke, W.D., Castillo, M.C., Reighard, A.E., and Vanderah, E. (2006). Aerobic exercise, but not flexibility/resistance exercise, reduces serum IL-18, CRP, and IL-6 independent of β-blockers, BMI, and psychosocial factors in older adults. Brain Behav. Immun. 20: 201–209, https://doi.org/10.1016/j.bbi.2005.12.002.Search in Google Scholar PubMed

Koistinen, H., Koistinen, R., Selenius, L., Ylikorkala, O., and Seppälä, M. (1996). Effect of marathon run on serum IGF-I and IGF-binding protein 1 and 3 levels. J. Appl. Physiol. 80: 760–764, https://doi.org/10.1152/jappl.1996.80.3.760.Search in Google Scholar PubMed

Kondo, M., Nakamura, Y., Ishida, Y., and Shimada, S. (2015). The 5-HT3 receptor is essential for exercise-induced hippocampal neurogenesis and antidepressant effects. Mol. Psychiatry 20: 1428–1437, https://doi.org/10.1038/mp.2014.153.Search in Google Scholar PubMed

Kraemer, R.R., Durand, R.J., Acevedo, E.O., Johnson, L.G., Kraemer, G.R., Hebert, E.P., and Castracane, V.D. (2004). Rigorous running increases growth hormone and insulin-like growth factor-I without altering ghrelin. Exp. Biol. Med. 229: 240–246, https://doi.org/10.1177/153537020422900304.Search in Google Scholar PubMed

Kraguljac, N.V., Carle, M., Frölich, M.A., Tran, S., Yassa, M.A., White, D.M., Reddy, A., and Lahti, A.C. (2018). Mnemonic discrimination deficits in first-episode psychosis and a ketamine model suggests dentate gyrus pathology linked to N-methyl-D-aspartate receptor hypofunction. Biol. Psychiatry Cogn. Neurosci. Neuroimaging 3: 231–238, https://doi.org/10.1016/j.bpsc.2017.02.005.Search in Google Scholar

Kraus, R.M., Stallings, H.W., Yeager, R.C., and Gavin, T.P. (2004). Circulating plasma VEGF response to exercise in sedentary and endurance-trained men. J. Appl. Physiol. 96: 1445–1450, https://doi.org/10.1152/japplphysiol.01031.2003.Search in Google Scholar

Kumaran, D. and Maguire, E.A. (2009). Novelty signals: a window into hippocampal information processing. Trends Cogn. Sci. 13: 47–54, https://doi.org/10.1016/j.tics.2008.11.004.Search in Google Scholar

Lacy, J.W., Yassa, M.A., Stark, S.M., Muftuler, L.T., and Stark, C.E.L. (2011). Distinct pattern separation related transfer functions in human CA3/dentate and CA1 revealed using highresolution fMRI and variable mnemonic similarity. Learn. Mem. 18: 15–18, https://doi.org/10.1101/lm.1971111.Search in Google Scholar

Lange, I., Goossens, L., Michielse, S., Bakker, J., Lissek, S., Papalini, S., Verhagen, S., Leibold, N., Marcelis, M., Wichers, M., et al.. (2017). Behavioral pattern separation and its link to the neural mechanisms of fear generalization. Soc. Cogn. Affect. Neurosci.: 1720–1729, https://doi.org/10.1093/scan/nsx104.Search in Google Scholar

Laplante, P., Diorio, J., and Meaney, M.J. (2002). Serotonin regulates hippocampal glucocorticoid receptor expression via a 5-HT7 receptor. Dev. Brain Res. 139: 199–203, https://doi.org/10.1016/s0165-3806(02)00550-3.Search in Google Scholar

Leal, S.L., Tighe, S.K., Jones, C.K., and Yassa, M.A. (2014). Pattern separation of emotional information in hippocampal dentate and CA3. Hippocampus 24: 1146–1155, https://doi.org/10.1002/hipo.22298.Search in Google Scholar PubMed PubMed Central

Leal, S.L. and Yassa, M.A. (2018). Integrating new findings and examining clinical applications of pattern separation. Nat. Neurosci. 21: 163–173, https://doi.org/10.1038/s41593-017-0065-1.Search in Google Scholar PubMed PubMed Central

Lecei, A. and van Winkel, R. (2020). Hippocampal pattern separation of emotional information determining risk or resilience in individuals exposed to childhood trauma: linking exposure to neurodevelopmental alterations and threat anticipation. Neurosci. Biobehav. Rev. 108: 160–170, https://doi.org/10.1016/j.neubiorev.2019.11.010.Search in Google Scholar PubMed

Lee, E. and Son, H. (2009). Adult hippocampal neurogenesis and related neurotrophic factors. BMB Rep. 42: 239–244, https://doi.org/10.5483/bmbrep.2009.42.5.239.Search in Google Scholar PubMed

Lee, M.C., Inoue, K., Okamoto, M., Liu, Y.F., Matsui, T., Yook, J.S., and Soya, H. (2013). Voluntary resistance running induces increased hippocampal neurogenesis in rats comparable to load-free running. Neurosci. Lett. 537: 6–10, https://doi.org/10.1016/j.neulet.2013.01.005.Search in Google Scholar

Leem, Y.H., Lee, Y.I., Son, H.J., and Lee, S.H. (2011). Chronic exercise ameliorates the neuroinflammation in mice carrying NSE/htau23. Biochem. Biophys. Res. Commun. 406: 359–365, https://doi.org/10.1016/j.bbrc.2011.02.046.Search in Google Scholar

Lenz, K.M. and McCarthy, M.M. (2014). A starring role for microglia in brain sex differences. Neuroscientist 21: 306–321, https://doi.org/10.1177/1073858414536468.Search in Google Scholar

Leranth, C. and Hajszan, T. (2007). Extrinsic afferent systems to the dentate gyrus. Prog. Brain Res. 163: 63–84, https://doi.org/10.1016/s0079-6123(07)63004-0.Search in Google Scholar

Li, M.Y., Huang, M.M., Li, S.Z., Tao, J., Zheng, G.H., and Chen, L.D. (2017). The effects of aerobic exercise on the structure and function of DMN-related brain regions: a systematic review. Int. J. Neurosci. 127: 634–649, https://doi.org/10.1080/00207454.2016.1212855.Search in Google Scholar

Lin, C.Y., Hung, S.Y., Chen, H. Te, Tsou, H.K., Fong, Y.C., Wang, S.W., and Tang, C.H. (2014). Brain-derived neurotrophic factor increases vascular endothelial growth factor expression and enhances angiogenesis in human chondrosarcoma cells. Biochem. Pharmacol. 91: 522–533, https://doi.org/10.1016/j.bcp.2014.08.008.Search in Google Scholar

Lin, T.W. and Kuo, Y.M. (2013). Exercise benefits brain function: the monoamine connection. Brain Sci. 3: 39–53, https://doi.org/10.3390/brainsci3010039.Search in Google Scholar

Liu, K.Y., Gould, R.L., Coulson, M.C., Ward, E.V., and Howard, R.J. (2016). Tests of pattern separation and pattern completion in humans – a systematic review. Hippocampus 26: 705–717, https://doi.org/10.1002/hipo.22561.Search in Google Scholar

Livnat, S., Felten, S.Y., Carlson, S.L., Bellinger, D.L., and Felten, D.L. (1985). Involvement of peripheral and central catecholamine systems in neural-immune interactions. J. Neuroimmunol. 10, https://doi.org/10.1016/0165-5728(85)90031-1.Search in Google Scholar

Llorens-Martín, M., Jurado-Arjona, J., Fuster-Matanzo, A., Hernández, F., Rábano, A., and Ávila, J. (2014). Peripherally triggered and GSK-3β-driven brain inflammation differentially skew adult hippocampal neurogenesis, behavioral pattern separation and microglial activation in response to ibuprofen. Transl. Psychiatry 4: e463.10.1038/tp.2014.92Search in Google Scholar PubMed PubMed Central

Lopez-Lopez, C., LeRoith, D., and Torres-Aleman, I. (2004). Insulin-like growth factor I is required for vessel modeling in the adult brain. Proc. Natl. Acad. Sci. U. S. A. 101: 9833–9838, https://doi.org/10.1073/pnas.0400337101.Search in Google Scholar

Loprinzi, P.D. (2019). The effects of physical exercise on parahippocampal function. Physiol. Int. 106: 114–127, https://doi.org/10.1556/2060.106.2019.10.Search in Google Scholar

Loprinzi, P.D., Frith, E., Edwards, M.K., Sng, E., and Ashpole, N. (2018). The effects of exercise on memory function among young to middle-aged adults: systematic review and recommendations for future research. Am. J. Health Promot. 32: 691–704, https://doi.org/10.1177/0890117117737409.Search in Google Scholar

Loprinzi, P.D., Moore, D., and Loenneke, J.P. (2020). Does aerobic and resistance exercise influence episodic memory through unique mechanisms? Brain Sci. 10: 1–13, https://doi.org/10.3390/brainsci10120913.Search in Google Scholar

Louissaint, A., Rao, S., Leventhal, C., and Goldman, S.A. (2002). Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 34: 945–960, https://doi.org/10.1016/s0896-6273(02)00722-5.Search in Google Scholar

Lucassen, P.J., Fitzsimons, C.P., Salta, E., and Maletic-Savatic, M. (2020). Adult neurogenesis, human after all (again): classic, optimized, and future approaches. Behav. Brain Res. 381: 112458, https://doi.org/10.1016/j.bbr.2019.112458.Search in Google Scholar PubMed

Ma, Q. (2008). Beneficial effects of moderate voluntary physical exercise and its biological mechanisms on brain health. Neurosci. Bull. 24: 265–270, https://doi.org/10.1007/s12264-008-0402-1.Search in Google Scholar PubMed PubMed Central

Maass, A., Düzel, S., Brigadski, T., Goerke, M., Becke, A., Sobieray, U., Neumann, K., Lövdén, M., Lindenberger, U., Bäckman, L., et al.. (2016). Relationships of peripheral IGF-1, VEGF and BDNF levels to exercise-related changes in memory, hippocampal perfusion and volumes in older adults. NeuroImage 131: 142–154, https://doi.org/10.1016/j.neuroimage.2015.10.084.Search in Google Scholar PubMed

Maass, A., Düzel, S., Goerke, M., Becke, A., Sobieray, U., Neumann, K., Lövden, M., Lindenberger, U., Bäckman, L., Braun-Dullaeus, R., et al.. (2015). Vascular hippocampal plasticity after aerobic exercise in older adults. Mol. Psychiatry 20: 585–593, https://doi.org/10.1038/mp.2014.114.Search in Google Scholar PubMed

Maddock, R.J., Casazza, G.A., Fernandez, D.H., and Maddock, M.I. (2016). Acute modulation of cortical glutamate and GABA content by physical activity. J. Neurosci. 36: 2449–2457, https://doi.org/10.1523/jneurosci.3455-15.2016.Search in Google Scholar PubMed PubMed Central

Manetta, J., Brun, J.F., Maïmoun, L., Fédou, C., Préfaut, C., and Mercier, J. (2003). The effects of intensive training on insulin-like growth factor I (IGF-I) and IGF binding proteins 1 and 3 in competitive cyclists: relationships with glucose disposal. J. Sports Sci. 21: 147–154, https://doi.org/10.1080/0264041031000070895.Search in Google Scholar

Marcell, T.J., McAuley, K.A., Traustadóttir, T., and Reaven, P.D. (2005). Exercise training is not associated with improved levels of C-reactive protein or adiponectin. Metabolism 54: 533–541, https://doi.org/10.1016/j.metabol.2004.11.008.Search in Google Scholar

Mariga, A., Mitre, M., and Chao, M.V. (2017). Consequences of brain-derived neurotrophic factor withdrawal in CNS neurons and implications in disease. Neurobiol. Dis. 97: 73–79, https://doi.org/10.1016/j.nbd.2016.03.009.Search in Google Scholar

Mark, L.P., Daniels, D.L., Naidich, T.P., and Hendrix, L.E. (1995). Limbic connections. Am. Soc. Neuroradiol. 16: 1303–1306.Search in Google Scholar

Marston, K.J., Brown, B.M., Rainey-Smith, S.R., Bird, S., Wijaya, L.K., Teo, S.Y.M., Martins, R.N., and Peiffer, J.J. (2020). An intense, but ecologically valid, resistance exercise session does not alter growth factors associated with cognitive health. J. Aging Phys. Act. 28: 605–612, https://doi.org/10.1123/japa.2019-0100.Search in Google Scholar

Mastorakos, G., Pavlatou, M.G., Diamanti-Kandarakis, E., and Chrousos, G. (2005). Exercise and the stress system. Hormones (Basel) 4: 73–89.Search in Google Scholar

Mcgaugh, J.L. (2002). Memory consolidation and the amygdala: a systems perspective. Trends Neurosci. 25: 456–461, https://doi.org/10.1016/s0166-2236(02)02211-7.Search in Google Scholar

McGaugh, J.L. (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27: 1–28, https://doi.org/10.1146/annurev.neuro.27.070203.144157.Search in Google Scholar PubMed

McHugh, T.J., Jones, M.W., Quinn, J.J., Balthasar, N., Coppari, R., Elmquist, J.K., Lowell, B.B., Fanselow, M.S., Wilson, M.A., and Tonegawa, S. (2007). Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317: 94–99, https://doi.org/10.1126/science.1140263.Search in Google Scholar PubMed

McNamara, C.G. and Dupret, D. (2017). Two sources of dopamine for the hippocampus. Trends Neurosci. 40: 383–384, https://doi.org/10.1016/j.tins.2017.05.005.Search in Google Scholar PubMed PubMed Central

Memel, M., Staffaroni, A.M., Cobigo, Y., Casaletto, K.B., Fonseca, C., Bettcher, B.M., Yassa, M.A., Elahi, F.M., Wolf, A., Rosen, H.J., et al.. (2021). APOE moderates the effect of hippocampal blood flow on memory pattern separation in clinically normal older adults. Hippocampus: 1–13.10.1002/hipo.23327Search in Google Scholar PubMed PubMed Central

Mishra, A., Singh, S., Tiwari, V., Parul, and Shukla, S. (2019). Dopamine D1 receptor activation improves adult hippocampal neurogenesis and exerts anxiolytic and antidepressant-like effect via activation of Wnt/β-catenin pathways in rat model of Parkinson’s disease. Neurochem. Int. 122: 170–186, https://doi.org/10.1016/j.neuint.2018.11.020.Search in Google Scholar PubMed

Monje, M.L., Toda, H., and Palmer, T.D. (2003). Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760–1766, https://doi.org/10.1126/science.1088417.Search in Google Scholar PubMed

Monteggia, L.M., Barrot, M., Powell, C.M., Berton, O., Galanis, V., Gemelli, T., Meuth, S., Nagy, A., Greene, R.W., and Nestler, E.J. (2004). Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc. Natl. Acad. Sci. U. S. A. 101: 10827–10832, https://doi.org/10.1073/pnas.0402141101.Search in Google Scholar PubMed PubMed Central

Moore, D. and Loprinzi, P.D. (2020). Exercise influences episodic memory via changes in hippocampal neurocircuitry and long-term potentiation. Eur. J. Neurosci. 0–1, https://doi.org/10.1111/ejn.14728.Search in Google Scholar PubMed

Moreno-Jiménez, E.P., Flor-García, M., Terreros-Roncal, J., Rábano, A., Cafini, F., Pallas-Bazarra, N., Ávila, J., and Llorens-Martín, M. (2019). Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease. Nat. Med. 25: 554–560.10.1038/s41591-019-0375-9Search in Google Scholar PubMed

Nauer, R.K., Dunne, M.F., Stern, C.E., Storer, T.W., and Schon, K. (2019). Improving fitness increases dentate gyrus/CA3 volume in the hippocampal head and enhances memory in young adults. Hippocampus 30: 488–504, https://doi.org/10.1002/hipo.23166.Search in Google Scholar PubMed PubMed Central

Neeper, S.A., Gómez-Pinilla, F., Choi, J., and Cotman, C. (1995). Exercise and brain neurotrophins. Nature 373: 109, https://doi.org/10.1038/373109a0.Search in Google Scholar PubMed

Newman-Tancredi, A. (2011). Biased agonism at serotonin 5-HT1A receptors: preferential postsynaptic activity for improved therapy of CNS disorders. Neuropsychiatry 1: 149–164, https://doi.org/10.2217/npy.11.12.Search in Google Scholar

Newton, S. and Duman, R. (2005). Regulation of neurogenesis and angiogenesis in depression. Curr. Neurovasc. Res. 1: 261–267, https://doi.org/10.2174/1567202043362388.Search in Google Scholar PubMed

Nichol, K.E., Poon, W.W., Parachikova, A.I., Cribbs, D.H., Glabe, C.G., and Cotman, C.W. (2008). Exercise alters the immune profile in Tg2576 Alzheimer mice toward a response coincident with improved cognitive performance and decreased amyloid. J. Neuroinflammation 5: 1–15, https://doi.org/10.1186/1742-2094-5-13.Search in Google Scholar PubMed PubMed Central

Nicklas, B.J., Hsu, F.C., Brinkley, T.J., Church, T., Goodpaster, B.H., Kritchevsky, S.B., and Pahor, M. (2008). Exercise training and plasma C-reactive protein and interleukin-6 in elderly people. J. Am. Geriatr. Soc. 56: 2045–2052, https://doi.org/10.1111/j.1532-5415.2008.01994.x.Search in Google Scholar PubMed PubMed Central

Niibori, Y., Yu, T.S., Epp, J.R., Akers, K.G., Josselyn, S.A., and Frankland, P.W. (2012). Suppression of adult neurogenesis impairs population coding of similar contexts in hippocampal CA3 region. Nat. Commun. 3: 4–10, https://doi.org/10.1038/ncomms2261.Search in Google Scholar PubMed PubMed Central

Niklison-Chirou, M.V., Agostini, M., Amelio, I., and Melino, G. (2020). Regulation of adult neurogenesis in mammalian brain. Int. J. Mol. Sci. 21: 4869, https://doi.org/10.3390/ijms21144869.Search in Google Scholar PubMed PubMed Central

Nindl, B.C., Scofield, D.E., Strohbach, C.A., Centi, A.J., Evans, R.K., Yanovich, R., and Moran, D.S. (2012). IGF-I, IGFBPS, and inflammatory cytokine responses during gender-integrated Israeli Army basic combat training. J. Strength Cond. Res. 26, https://doi.org/10.1519/JSC.0b013e31825d81ba.Search in Google Scholar PubMed

Novaes Gomes, F.G., Fernandes, J., Vannucci Campos, D., Cassilhas, R.C., Viana, G.M., D’Almeida, V., de Moraes Rêgo, M.K., Buainain, P.I., Cavalheiro, E.A., and Arida, R.M. (2014). The beneficial effects of strength exercise on hippocampal cell proliferation and apoptotic signaling is impaired by anabolic androgenic steroids. Psychoneuroendocrinology 50: 106–117, https://doi.org/10.1016/j.psyneuen.2014.08.009.Search in Google Scholar PubMed

Nyberg, L., Karalija, N., Salami, A., Andersson, M., Wåhlin, A., Kaboovand, N., Köhncke, Y., Axelsson, J., Rieckmann, A., Papenberg, G., et al.. (2016). Dopamine D2 receptor availability is linked to hippocampal-caudate functional connectivity and episodic memory. Proc. Natl. Acad. Sci. U. S. A. 113: 7918–7923, https://doi.org/10.1073/pnas.1606309113.Search in Google Scholar PubMed PubMed Central

O’Callaghan, R.M., Griffin, É.W., and Kelly, Á.M. (2009). Long-term treadmill exposure protects against age-related neurodegenerative change in the rat hippocampus. Hippocampus 19: 1019–1029.10.1002/hipo.20591Search in Google Scholar PubMed

Oberlin, L.E., Verstynen, T.D., Burzynska, A.Z., Voss, M.W., Prakash, R.S., Chaddock-Heyman, L., Wong, C., Fanning, J., Awick, E., Gothe, N., et al.. (2016). White matter microstructure mediates the relationship between cardiorespiratory fitness and spatial working memory in older adults. NeuroImage 131: 91–101, https://doi.org/10.1016/j.neuroimage.2015.09.053.Search in Google Scholar PubMed PubMed Central

Okamoto, M., Hojo, Y., Inoue, K., Matsui, T., Kawato, S., McEwen, B.S., and Soya, H. (2012). Mild exercise increases dihydrotestosterone in hippocampus providing evidence for androgenic mediation of neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 109: 13100–13105, https://doi.org/10.1073/pnas.1210023109.Search in Google Scholar PubMed PubMed Central

Okamoto, M., Yamamura, Y., Liu, Y.-F., Min-Chul, L., Matsui, T., Shima, T., Soya, M., Takahashi, K., Soya, S., McEwen, B.S., et al.. (2015). Hormetic effects by exercise on hippocampal neurogenesis with glucocorticoid signaling. Brain Plast. 1: 149, https://doi.org/10.3233/bpl-150012.Search in Google Scholar

Orihuela, R., McPherson, C.A., and Harry, G.J. (2016). Microglial M1/M2 polarization and metabolic states. Br. J. Pharmacol. 173: 649–665, https://doi.org/10.1111/bph.13139.Search in Google Scholar PubMed PubMed Central

Ortega, F.B., Campos, D., Cadenas-Sanchez, C., Altmäe, S., Martínez-Zaldívar, C., Martín-Matillas, M., Catena, A., and Campoy, C. (2019). Physical fitness and shapes of subcortical brain structures in children. Br. J. Nutr. 122: 49–58, https://doi.org/10.1017/S0007114516001239.Search in Google Scholar

Otto, S.L. and Yakel, J.L. (2019). The α7 nicotinic acetylcholine receptors regulate hippocampal adult-neurogenesis in a sexually dimorphic fashion. Brain Struct. Funct. 224: 829–846, https://doi.org/10.1007/s00429-018-1799-6.Search in Google Scholar

Pace, T.W.W., Hu, F., and Miller, A.H. (2007). Cytokine-effects on glucocorticoid receptor function: relevance to glucocorticoid resistance and the pathophysiology and treatment of major depression. Brain Behav. Immun. 21: 9–19, https://doi.org/10.1016/j.bbi.2006.08.009.Search in Google Scholar

Packer, N. and Hoffman-Goetz, L. (2015). Acute exercise increases hippocampal TNF-α, Caspase-3 and Caspase-7 expression in healthy young and older mice. J. Sports Med. Phys. Fitness 55: 368–376.Search in Google Scholar

Pagen, L.H.G., Smeets, T., Schmiedek, L., Yassa, M.A., Verhey, F.R.J., and Jacobs, H.I.L. (2021). Elevated activity of the sympathetic nervous system is related to diminished practice effects in memory: a pilot study. J. Alzheimer’s Dis. 80: 1675–1685, https://doi.org/10.3233/jad-200783.Search in Google Scholar

Palacios-Filardo, J. and Mellor, J.R. (2019). Neuromodulation of hippocampal long-term synaptic plasticity. Curr. Opin. Neurobiol. 54: 37–43, https://doi.org/10.1016/j.conb.2018.08.009.Search in Google Scholar

Palmer, T.D., Willhoite, A.R., and Gage, F.H. (2000). Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425: 479–494, https://doi.org/10.1002/1096-9861(20001002)425:4<479::aid-cne2>3.0.co;2-3.10.1002/1096-9861(20001002)425:4<479::AID-CNE2>3.0.CO;2-3Search in Google Scholar

Pan, W. (2006). Permeability of the blood-brain barrier to neurotrophic peptides. Handb. Biol. Act. Pept.: 1435–1441, https://doi.org/10.1016/b978-012369442-3/50203-8.Search in Google Scholar

Pan, W., Banks, W.A., Fasold, M.B., Bluth, J., and Kastin, A.J. (1998). Transport of brain-derived neurotrophic factor across the blood–brain barrier. Neuropharmacology 37: 1553–1561, https://doi.org/10.1016/s0028-3908(98)00141-5.Search in Google Scholar

Panagiotakopoulos, L. and Neigh, G.N. (2014). Development of the HPA axis: where and when do sex differences manifest? Front. Neuroendocrinol. 35: 285–302, https://doi.org/10.1016/j.yfrne.2014.03.002.Search in Google Scholar

Parizkova, M., Lerch, O., Andel, R., Kalinova, J., Markova, H., Vyhnalek, M., Hort, J., and Laczo, J. (2020). Spatial pattern separation in early Alzheimer’s disease. J. Alzheimer’s Dis. 76: 121–138, https://doi.org/10.3233/jad-200093.Search in Google Scholar

Parkhurst, C.N., Yang, G., Ninan, I., Savas, J.N., Yates, J.R., Lafaille, J.J., Hempstead, B.L., Littman, D.R., and Gan, W.-B. (2013). Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155: 1596–1609, https://doi.org/10.1016/j.cell.2013.11.030.Search in Google Scholar

Patten, A.R., Yau, S.Y., Fontaine, C.J., Meconi, A., Wortman, R.C., and Christie, B.R. (2015). The benefits of exercise on structural and functional plasticity in the rodent Hippocampus of different disease models. Brain Plast. 1: 97–127, https://doi.org/10.3233/bpl-150016.Search in Google Scholar

Pawley, L.C., Hueston, C.M., O’Leary, J.D., Kozareva, D.A., Cryan, J.F., O’Leary, O.F., and Nolan, Y.M. (2020). Chronic intrahippocampal interleukin-1β overexpression in adolescence impairs hippocampal neurogenesis but not neurogenesis-associated cognition. Brain Behav. Immun. 83: 172–179, https://doi.org/10.1016/j.bbi.2019.10.007.Search in Google Scholar

Pazos, A. and Palacios, J.M. (1985). Quantitative autoradiographic mapping of serotonin receptors in the rat brain. I. Serotonin-1 receptors. Brain Res.: 205–230, https://doi.org/10.1016/0006-8993(85)90856-x.Search in Google Scholar

Pereira, A.C., Huddleston, D.E., Brickman, A.M., Sosunov, A.A., Hen, R., McKhann, G.M., Sloan, R., Gage, F.H., Brown, T.R., and Small, S.A. (2007). An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. U. S. A. 104: 5638–5643, https://doi.org/10.1073/pnas.0611721104.Search in Google Scholar

Piepmeier, A.T. and Etnier, J.L. (2015). Brain-derived neurotrophic factor (BDNF) as a potential mechanism of the effects of acute exercise on cognitive performance. J. Sport Health Sci. 4: 14–23, https://doi.org/10.1016/j.jshs.2014.11.001.Search in Google Scholar

Pietrelli, A., Matković, L., Vacotto, M., Lopez-Costa, J.J., Basso, N., and Brusco, A. (2018). Aerobic exercise upregulates the BDNF-Serotonin systems and improves the cognitive function in rats. Neurobiol. Learn. Mem. 155: 528–542, https://doi.org/10.1016/j.nlm.2018.05.007.Search in Google Scholar

Quiroga, R.Q. (2020). No pattern separation in the human hippocampus. Trends Cogn. Sci. 24: 994–1007, https://doi.org/10.1016/j.tics.2020.09.012.Search in Google Scholar

Radley, J.J. and Jacobs, B.L. (2002). 5-HT receptor antagonist administration decreases cell proliferation 1A in the dentate gyrus. Brain Res. 955: 264–267, https://doi.org/10.1016/s0006-8993(02)03477-7.Search in Google Scholar

Rebar, A.L., Stanton, R., Geard, D., Short, C., Duncan, M.J., and Vandelanotte, C. (2015). A meta-meta-analysis of the effect of physical activity on depression and anxiety in non-clinical adult populations. Health Psychol. Rev. 9: 366–378, https://doi.org/10.1080/17437199.2015.1022901.Search in Google Scholar PubMed

Rivest, S. (2010). Interactions between the immune and neuroendocrine systems. Prog. Brain Res. 181: 43–53, https://doi.org/10.1016/s0079-6123(08)81004-7.Search in Google Scholar

Rogers, J., Chen, F., Stanic, D., Farzana, F., Li, S., Zeleznikow-Johnston, A.M., Nithianantharajah, J., Churilov, L., Adlard, P.A., Lanfumey, L., et al.. (2019). Paradoxical effects of exercise on hippocampal plasticity and cognition in mice with a heterozygous null mutation in the serotonin transporter gene. Br. J. Pharmacol. 176: 3279–3296, https://doi.org/10.1111/bph.14760.Search in Google Scholar PubMed PubMed Central

Rolls, E.T. (2021). Trends in Cognitive Sciences Letter: On pattern separation in the primate, including human. Trends Cogn. Sci. 25: 920–922, https://doi.org/10.1016/j.tics.2021.07.004.Search in Google Scholar PubMed

Rosendal, L., Langberg, H., Flyvbjerg, A., Frystyk, J., Ørskov, H., and Kjæer, M. (2002). Physical capacity influences the response of insulin-like growth factor and its binding proteins to training. J. Appl. Physiol. 93: 1669–1675, https://doi.org/10.1152/japplphysiol.00145.2002.Search in Google Scholar PubMed

Rossi, C., Angelucci, A., Costantin, L., Braschi, C., Mazzantini, M., Babbini, F., Fabbri, M.E., Tessarollo, L., Maffei, L., Berardi, N., et al.. (2006). Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur. J. Neurosci. 24: 1850–1856, https://doi.org/10.1111/j.1460-9568.2006.05059.x.Search in Google Scholar PubMed

Roy, N.S., Wang, S., Jiang, L., Kang, J., Benraiss, A., Harrison-Restelli, C., Fraser, R.A.R., Couldwell, W.T., Kawaguchi, A., Okano, H., et al.. (2000). In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat. Med. 6: 271–277, https://doi.org/10.1038/73119.Search in Google Scholar PubMed

Rudman, D. and Mattson, D.E. (1994). Serum insulin‐like growth factor I in healthy older men in relation to physical activity. J. Am. Geriatr. Soc. 42: 71–76, https://doi.org/10.1111/j.1532-5415.1994.tb06076.x.Search in Google Scholar PubMed

Ryan, S.M. and Nolan, Y.M. (2016). Neuroinflammation negatively affects adult hippocampal neurogenesis and cognition: can exercise compensate? Neurosci. Biobehav. Rev. 61: 121–131, https://doi.org/10.1016/j.neubiorev.2015.12.004.Search in Google Scholar PubMed

Sahay, A., Scobie, K.N., Hill, A.S., O’Carroll, C.M., Kheirbek, M.A., Burghardt, N.S., Fenton, A.A., Dranovsky, A., and Hen, R. (2011). Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472: 466–470, https://doi.org/10.1038/nature09817.Search in Google Scholar PubMed PubMed Central

Sarbadhikari, S.N. and Saha, A.K. (2006). Moderate exercise and chronic stress produce counteractive effects on different areas of the brain by acting through various neurotransmitter receptor subtypes: a hypothesis. Theor. Biol. Med. Model. 3, https://doi.org/10.1186/1742-4682-3-33.Search in Google Scholar PubMed PubMed Central

Scharfman, H., Goodman, J., Macleod, A., Phani, S., Antonelli, C., and Croll, S. (2005). Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 192: 348–356, https://doi.org/10.1016/j.expneurol.2004.11.016.Search in Google Scholar

Scharfman, H. and MacLusky, N. (2017). Sex differences in hippocampal area CA3 pyramidal cells. J. Neurosci. Res. 95: 563–575, https://doi.org/10.1002/jnr.23927.Search in Google Scholar

Schiffer, T., Schulte, S., Hollmann, W., Bloch, W., and Strüder, H.K. (2009). Effects of strength and endurance training on brain-derived neurotrophic factor and insulin-like growth factor 1 in humans. Horm. Metab. Res. 41: 250–254, https://doi.org/10.1055/s-0028-1093322.Search in Google Scholar

Schinder, A.F. and Poo, M. (2000). The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci. 23: 639–645, https://doi.org/10.1016/s0166-2236(00)01672-6.Search in Google Scholar

Schmahmann, J.D. and Pandya, D.N. (2006). Fiber pathways of the brain. Oxford University Press, New York.10.1093/acprof:oso/9780195104233.001.0001Search in Google Scholar

Schmidt-Hieber, C., Jones, P., and Bischofberger, J. (2004). Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429: 184–187, https://doi.org/10.1038/nature02553.Search in Google Scholar PubMed

Schoenfeld, T.J. and Gould, E. (2013). Differential effects of stress and glucocorticoids on adult neurogenesis. Curr. Top. Behav. Neurosci. 15: 139–164, https://doi.org/10.1007/7854_2012_233.Search in Google Scholar PubMed

Schwarz, A.J., Brasel, J.A., Hintz, R.L., Mohan, S., and Cooper, D.M. (1996). Acute effect of brief low- and high-intensity exercise on circulating insulin-like growth factor (IGF) I, II, and IGF-binding protein-3 and its proteolysis in young healthy men. J. Clin. Endocrinol. Metab. 81: 3492–3497, https://doi.org/10.1210/jcem.81.10.8855791.Search in Google Scholar PubMed

Seel, S.V., Eacott, M.J., Langston, R.F., and Easton, A. (2018). Cholinergic input to the hippocampus is not required for a model of episodic memory in the rat, even with multiple consecutive events. Behav. Brain Res. 354: 48–54, https://doi.org/10.1016/j.bbr.2017.06.001.Search in Google Scholar PubMed

Segal, S.K., Cotman, C.W., and Cahill, L.F. (2012a). Exercise-induced noradrenergic activation enhances memory consolidation in both normal aging and patients with amnestic mild cognitive impairment. J. Alzheimer’s Dis. 32: 1011–1018, https://doi.org/10.3233/jad-2012-121078.Search in Google Scholar

Segal, S.K., Stark, S.M., Kattan, D., Stark, C.E., and Yassa, M.A. (2012b). Norepinephrine-mediated emotional arousal facilitates subsequent pattern separation. Neurobiol. Learn. Mem. 97: 465–469, https://doi.org/10.1016/j.nlm.2012.03.010.Search in Google Scholar PubMed PubMed Central

Sexton, C.E., Betts, J.F., Demnitz, N., Dawes, H., Ebmeier, K.P., and Johansen-Berg, H. (2016). A systematic review of MRI studies examining the relationship between physical fitness and activity and the white matter of the ageing brain. NeuroImage 131: 81–90, https://doi.org/10.1016/j.neuroimage.2015.09.071.Search in Google Scholar PubMed PubMed Central

Shields, G.S., Sazma, M.A., McCullough, A.M., and Yonelinas, A.P. (2017). The effects of acute stress on episodic memory: a meta-analysis and integrative review. Psychol. Bull. 143: 636–675, https://doi.org/10.1037/bul0000100.Search in Google Scholar PubMed PubMed Central

Sierra, A., Beccari, S., Diaz-Aparicio, I., Encinas, J.M., Comeau, S., and Tremblay, M.-È. (2014). Surveillance, phagocytosis, and inflammation: how never-resting microglia influence adult hippocampal neurogenesis. Neural Plast.: 1–15, https://doi.org/10.1155/2014/610343.Search in Google Scholar PubMed PubMed Central

Sigwalt, A.R., Budde, H., Helmich, I., Glaser, V., Ghisoni, K., Lanza, S., Cadore, E.L., Lhullier, F.L.R., de Bem, A.F., Hohl, A., et al.. (2011). Molecular aspects involved in swimming exercise training reducing anhedonia in a rat model of depression. Neuroscience 192: 661–674, https://doi.org/10.1016/j.neuroscience.2011.05.075.Search in Google Scholar PubMed

Silva, W.C.N.d., Köhler, C.C., Radiske, A., and Cammarota, M. (2012). D 1/D 5 dopamine receptors modulate spatial memory formation. Neurobiol. Learn. Mem. 97: 271–275, https://doi.org/10.1016/j.nlm.2012.01.005.Search in Google Scholar PubMed

Sleiman, S.F., Henry, J., Al-Haddad, R., El Hayek, L., Haidar, E.A., Stringer, T., Ulja, D., Karuppagounder, S.S., Holson, E.B., Ratan, R.R., et al.. (2016). Exercise promotes the expression of brain derived neurotrophic factor (BDNF) through the action of the ketone body β- hydroxybutyrate. Elife 5, https://doi.org/10.7554/eLife.15092.Search in Google Scholar PubMed PubMed Central

Sloan, R.P., Shapiro, P.A., DeMeersman, R.E., McKinley, P.S., Tracey, K.J., Slavov, I., Fang, Y., and Flood, P.D. (2007). Aerobic exercise attenuates inducible TNF production in humans. J. Appl. Physiol. 103: 1007–1011, https://doi.org/10.1152/japplphysiol.00147.2007.Search in Google Scholar PubMed

So, J.H., Huang, C., Ge, M., Cai, G., Zhang, L., Lu, Y., and Mu, Y. (2017). Intense exercise promotes adult hippocampal neurogenesis but not spatial discrimination. Front. Cell. Neurosci. 11, https://doi.org/10.3389/fncel.2017.00013.Search in Google Scholar PubMed PubMed Central

Sorrells, S.F., Paredes, M.F., Cebrian-Silla, A., Sandoval, K., Qi, D., Kelley, K.W., James, D., Mayer, S., Chang, J., Auguste, K.I., et al.. (2018). Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults. Nature 555: 377–381, https://doi.org/10.1038/nature25975.Search in Google Scholar PubMed PubMed Central

Spalding, K.L., Bergmann, O., Alkass, K., Bernard, S., Salehpour, M., Huttner, H.B., Boström, E., Westerlund, I., Vial, C., Buchholz, B.A., et al.. (2013). Dynamics of hippocampal neurogenesis in adult humans. Cell 153: 1219–1227, https://doi.org/10.1016/j.cell.2013.05.002.Search in Google Scholar PubMed PubMed Central

Spielman, L.J., Little, J.P., and Klegeris, A. (2016). Physical activity and exercise attenuate neuroinflammation in neurological diseases. Brain Res. Bull. 125: 19–29, https://doi.org/10.1016/j.brainresbull.2016.03.012.Search in Google Scholar PubMed

St-Pierre, D.H. and Richard, D. (2020). The effect of exercise on the hypothalamic-pituitary-adrenal Axis. In: Hackney, A., and Constantini, N. (Eds.), Contemporary endocrinology. Humana Press Inc, pp. 41–54.10.1007/978-3-030-33376-8_3Search in Google Scholar

Stark, S.M., Kirwan, C.B., and Stark, C.E.L. (2019). Mnemonic similarity task: a tool for assessing hippocampal integrity. Trends Cogn. Sci. 23: 938–951, https://doi.org/10.1016/j.tics.2019.08.003.Search in Google Scholar PubMed PubMed Central

Stewart, L.K., Flynn, M.G., Campbell, W.W., Craig, B.A., Robinson, J.P., McFarlin, B.K., Timmerman, K.L., Coen, P.M., Felker, J., and Talbert, E. (2005). Influence of exercise training and age on CD14+ cell-surface expression of toll-like receptor 2 and 4. Brain Behav. Immun. 19: 389–397, https://doi.org/10.1016/j.bbi.2005.04.003.Search in Google Scholar PubMed

Stranahan, A.M., Lee, K., and Mattson, M.P. (2008a). Central mechanisms of HPA axis regulation by voluntary exercise. Neuromolecular Med. 10: 118–127, https://doi.org/10.1007/s12017-008-8027-0.Search in Google Scholar PubMed PubMed Central

Stranahan, A.M., Lee, K., and Mattson, M.P. (2008b). Central mechanisms of HPA axis regulation by voluntary exercise. Neuromolecular Med. 10: 118–127, https://doi.org/10.1007/s12017-008-8027-0.Search in Google Scholar

Strle, K., Broussard, S.R., McCusker, R.H., Shen, W.H., Johnson, R.W., Freund, G.G., Dantzer, R., and Kelley, K.W. (2004). Proinflammatory cytokine impairment of insulin-like growth factor I-induced protein synthesis in skeletal muscle myoblasts requires ceramide. Endocrinology 145: 4592–4602, https://doi.org/10.1210/en.2003-1749.Search in Google Scholar PubMed

Sun, Y., Jin, K., Xie, L., Childs, J., Mao, X.O., Logvinova, A., and Greenberg, D.A. (2003). VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J. Clin. Invest. 111: 1843–1851, https://doi.org/10.1172/jci200317977.Search in Google Scholar

Suthana, N., Ekstrom, A.D., Yassa, M.A., and Stark, C. (2021). Pattern separation in the human hippocampus: response toQuiroga. Trends Cogn. Sci. 25: 423, https://doi.org/10.1016/j.tics.2021.02.005.Search in Google Scholar PubMed PubMed Central

Suwabe, K., Byun, K., Hyodo, K., Reagh, Z.M., Roberts, J.M., Matsushita, A., Saotome, K., Ochi, G., Suzuki, K., Sankai, Y., et al.. (2018). Rapid stimulation of human dentate gyrus function with acute mild exercise. Proc. Natl. Acad. Sci. U. S. A. 115: 10487–10492, https://doi.org/10.1073/pnas.1805668115.Search in Google Scholar PubMed PubMed Central

Suwabe, K., Hyodo, K., Byun, K., Ochi, G., Fukuie, T., Shimizu, T., Kato, M., Yassa, M.A., and Soya, H. (2017a). Aerobic fitness associates with mnemonic discrimination as a mediator of physical activity effects: evidence for memory flexibility in young adults. Sci. Rep. 7: 1–10, https://doi.org/10.1038/s41598-017-04850-y.Search in Google Scholar

Suwabe, K., Hyodo, K., Byun, K., Ochi, G., Yassa, M.A., and Soya, H. (2017b). Acute moderate exercise improves mnemonic discrimination in young adults. Hippocampus 27: 229–234, https://doi.org/10.1002/hipo.22695.Search in Google Scholar

Swain, R.A., Harris, A.B., Wiener, E.C., Dutka, M.V., Morris, H.D., Theien, B.E., Konda, S., Engberg, K., Lauterbur, P.C., and Greenough, W.T. (2003). Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 117: 1037–1046, https://doi.org/10.1016/s0306-4522(02)00664-4.Search in Google Scholar

Światkiewicz, M., Fiedorowicz, M., Orzeł, J., Wełniak-Kamińska, M., Bogorodzki, P., Langfort, J., and Grieb, P. (2017). Increases in brain 1H-MR glutamine and glutamate signals following acute exhaustive endurance exercise in the rat. Front. Physiol. 8.10.3389/fphys.2017.00019Search in Google Scholar PubMed PubMed Central

Tabata, I., Ogita, F., Miyachi, M., and Shibayama, H. (1991). Effect of low blood glucose on plasma CRF, ACTH, and cortisol during prolonged physical exercise. J. Appl. Physiol. 71: 1807–1812, https://doi.org/10.1152/jappl.1991.71.5.1807.Search in Google Scholar PubMed

Takahashi, S., Keeser, D., Rauchmann, B.S., Schneider-Axmann, T., Keller-Varady, K., Maurus, I., Dechent, P., Wobrock, T., Hasan, A., Schmitt, A., et al.. (2020). Effect of aerobic exercise combined with cognitive remediation on cortical thickness and prediction of social adaptation in patients with schizophrenia. Schizophr. Res. 216: 397–407, https://doi.org/10.1016/j.schres.2019.11.004.Search in Google Scholar PubMed

Thacker, J.S., Xu, Y., Tang, C., Tupling, A.R., Staines, W.R., and Mielke, J.G. (2019). A single session of aerobic exercise mediates plasticity-related phosphorylation in both the rat motor cortex and hippocampus. Neuroscience 412: 160–174, https://doi.org/10.1016/j.neuroscience.2019.05.051.Search in Google Scholar PubMed

Tian, Q., Erickson, K.I., Simonsick, E.M., Aizenstein, H.J., Glynn, N.W., Boudreau, R.M., Newman, A.B., Kritchevsky, S.B., Yaffe, K., Harris, T.B., et al.. (2014a). Physical activity predicts microstructural integrity in memory-related networks in very old adults. J. Gerontol. A Biol. Sci. Med. Sci. 69: 1284–1290, https://doi.org/10.1093/gerona/glt287.Search in Google Scholar PubMed PubMed Central

Tian, Q., Simonsick, E.M., Erickson, K.I., Aizenstein, H.J., Glynn, N.W., Boudreau, R.M., Newman, A.B., Kritchevsky, S.B., Yaffe, K., Harris, T., et al.. (2014b). Cardiorespiratory fitness and brain diffusion tensor imaging in adults over 80 years of age. Brain Res. 1588: 63–72, https://doi.org/10.1016/j.brainres.2014.09.003.Search in Google Scholar PubMed PubMed Central

Toda, T. and Gage, F.H. (2018). Review: adult neurogenesis contributes to hippocampal plasticity. Cell Tissue Res. 373: 639–709, https://doi.org/10.1007/s00441-017-2735-4.Search in Google Scholar PubMed

Tong, L., Aleph Prieto, G., Kramár, E.A., Smith, E.D., Cribbs, D.H., Lynch, G., and Cotman, C.W. (2012). Brain-derived neurotrophic factor-dependent synaptic plasticity is suppressed by interleukin-1β via p38 mitogen-activated protein kinase. J. Neurosci. 32: 17714–17724, https://doi.org/10.1523/jneurosci.1253-12.2012.Search in Google Scholar PubMed PubMed Central

Trejo, J.L., Carro, E., and Torres-Alemán, I. (2001). Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J. Neurosci. 21: 1628–1634, https://doi.org/10.1523/jneurosci.21-05-01628.2001.Search in Google Scholar

Van Bodegom, M., Homberg, J.R., and Henckens, M.J.A.G. (2017). Modulation of the hypothalamic-pituitary-adrenal axis by early life stress exposure. Front. Cell. Neurosci. 11, https://doi.org/10.3389/fncel.2017.00087.Search in Google Scholar PubMed PubMed Central

Van Goethem, N.P., Schreiber, R., Newman-Tancredi, A., Varney, M., and Prickaerts, J. (2015). Divergent effects of the “biased” 5-HT1A receptor agonists F15599 and F13714 in a novel object pattern separation task. Br. J. Pharmacol. 172: 2532–2543, https://doi.org/10.1111/bph.13071.Search in Google Scholar PubMed PubMed Central

Van Hoomissen, J.D., Holmes, P.V., Zellner, A.S., Poudevigne, A.M., and Dishman, R.K. (2004). Effects of β-adrenoreceptor blockade during chronic exercise on contextual fear conditioning and mRNA for galanin and brain-derived neurotrophic factor. Behav. Neurosci. 118: 1378–1390, https://doi.org/10.1037/0735-7044.118.6.1378.Search in Google Scholar PubMed

van Praag, H. (2009). Exercise and the brain: something to chew on. Trends Neurosci. 32: 283–290, https://doi.org/10.1016/j.tins.2008.12.007.Search in Google Scholar PubMed PubMed Central

Van Praag, H. (2008). Neurogenesis and exercise: past and future directions. NeuroMolecular Med. 10: 128–140, https://doi.org/10.1007/s12017-008-8028-z.Search in Google Scholar PubMed

Van Praag, H., Christie, B.R., Sejnowski, T.J., and Gage, F.H. (1999a). Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. U. S. A. 96: 13427–13431, https://doi.org/10.1073/pnas.96.23.13427.Search in Google Scholar PubMed PubMed Central

Van Praag, H., Kempermann, G., and Gage, F.H. (1999b). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2: 266–270, https://doi.org/10.1038/6368.Search in Google Scholar PubMed

Van Praag, H., Shubert, T., Zhao, C., and Gage, F.H. (2005a). Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 25: 8680–8685, https://doi.org/10.1523/jneurosci.1731-05.2005.Search in Google Scholar

Van Praag, H., Shubert, T., Zhao, C., and Gage, F.H. (2005b). Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 25: 8680–8685, https://doi.org/10.1523/jneurosci.1731-05.2005.Search in Google Scholar

Vasuta, C., Caunt, C., James, R., Samadi, S., Schibuk, E., Kannangara, T., Titterness, A.K., and Christie, B.R. (2007). Effects of exercise on NMDA receptor subunit contributions to bidirectional synaptic plasticity in the mouse dentate gyrus. Hippocampus 17: 1201–1208, https://doi.org/10.1002/hipo.20349.Search in Google Scholar

Vaynman, S. and Gomez-Pinilla, F. (2005). License to run: exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabilitation Neural Repair 19: 283–295, https://doi.org/10.1177/1545968305280753.Search in Google Scholar

Vaynman, S., Ying, Z., and Gomez-Pinilla, F. (2004). Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur. J. Neurosci. 20: 2580–2590, https://doi.org/10.1111/j.1460-9568.2004.03720.x.Search in Google Scholar

Vaynman, S., Ying, Z., Yin, D., and Gomez-Pinilla, F. (2006). Exercise differentially regulates synaptic proteins associated to the function of BDNF. Brain Res. 1070: 124–130, https://doi.org/10.1016/j.brainres.2005.11.062.Search in Google Scholar

Venters, H.D., Broussard, S.R., Zhou, J.H., Bluthé, R.M., Freund, G.G., Johnson, R.W., Dantzer, R., and Kelley, K.W. (2001). Tumor necrosis factorα and insulin-like growth factor-I in the brain: is the whole greater than the sum of its parts? J. Neuroimmunol. 119: 151–165, https://doi.org/10.1016/s0165-5728(01)00388-5.Search in Google Scholar

Vivar, C. and Van Praag, H. (2017). Running changes the brain: the long and the short of it. Physiology 32: 410–424, https://doi.org/10.1152/physiol.00017.2017.Search in Google Scholar PubMed PubMed Central

Voskuil, D.W., Bueno De Mesquita, H.B., Kaaks, R., Noord, P.A.H.V., Rinaldi, S., Riboli, E., Grobbee, D.E., and Peeters, P.H.M. (2001). Determinants of circulating insulin-like growth factor (IGF)-I and IGF binding proteins 1-3 in premenopausal women: physical activity and anthropometry (Netherlands). Cancer Causes Control 12: 951–958, https://doi.org/10.1023/a:1013708627664.10.1023/A:1013708627664Search in Google Scholar

Voss, M.W., Erickson, K.I., Prakash, R.S., Chaddock, L., Kim, J.S., Alves, H., Szabo, A., Phillips, S.M., Wójcicki, T.R., Mailey, E.L., et al.. (2013a). Neurobiological markers of exercise-related brain plasticity in older adults. Brain Behav. Immun. 28: 90–99, https://doi.org/10.1016/j.bbi.2012.10.021.Search in Google Scholar PubMed PubMed Central

Voss, M.W., Heo, S., Prakash, R.S., Erickson, K.I., Alves, H., Chaddock, L., Szabo, A.N., Mailey, E.L., Wójcicki, T.R., White, S.M., et al.. (2013b). The influence of aerobic fitness on cerebral white matter integrity and cognitive function in older adults: results of a one-year exercise intervention. Hum. Brain Mapp. 34: 2972–2985, https://doi.org/10.1002/hbm.22119.Search in Google Scholar PubMed PubMed Central

Voss, M.W., Soto, C., Yoo, S., Sodoma, M., Vivar, C., and van Praag, H. (2019). Exercise and hippocampal memory systems. Trends Cogn. Sci. 23: 318–333, https://doi.org/10.1016/j.tics.2019.01.006.Search in Google Scholar PubMed PubMed Central

Voss, M.W., Vivar, C., Kramer, A.F., and van Praag, H. (2013c). Bridging animal and human models of exercise-induced brain plasticity. Trends Cogn. Sci. 17: 525–544, https://doi.org/10.1016/j.tics.2013.08.001.Search in Google Scholar PubMed PubMed Central

Wagner, G., Herbsleb, M., de la Cruz, F., Schumann, A., Köhler, S., Puta, C., Gabriel, H.W., Reichenbach, J.R., and Bär, K.J. (2017). Changes in fMRI activation in anterior hippocampus and motor cortex during memory retrieval after an intense exercise intervention. Biol. Psychol. 124: 65–78, https://doi.org/10.1016/j.biopsycho.2017.01.003.Search in Google Scholar PubMed

Wahl, P., Zinner, C., Achtzehn, S., Behringer, M., Bloch, W., and Mester, J. (2011). Effects of acid-base balance and high or low intensity exercise on VEGF and bFGF. Eur. J. Appl. Physiol. 111: 1405–1413, https://doi.org/10.1007/s00421-010-1767-1.Search in Google Scholar PubMed

Walling, S.G. and Harley, C.W. (2004). Locus ceruleus activation initiates delayed synaptic potentiation of perforant path input to the dentate gyrus in awake rats: a novel β-adrenergic- and protein synthesis-dependent mammalian plasticity mechanism. J. Neurosci. 24: 598–604, https://doi.org/10.1523/jneurosci.4426-03.2004.Search in Google Scholar PubMed PubMed Central

Waterhouse, E.G., An, J.J., Orefice, L.L., Baydyuk, M., Liao, G.Y., Zheng, K., Lu, B., and Xu, B. (2012). BDNF promotes differentiation and maturation of adult-born neurons through GABArgic transmission. J. Neurosci. 32: 14318–14330, https://doi.org/10.1523/jneurosci.0709-12.2012.Search in Google Scholar PubMed PubMed Central

Weinberg, L., Hasni, A., Shinohara, M., and Duarte, A. (2014). A single bout of resistance exercise can enhance episodic memory performance. Acta Psychol. 153: 13–19, https://doi.org/10.1016/j.actpsy.2014.06.011.Search in Google Scholar PubMed PubMed Central

Weng, T.B., Pierce, G.L., Darling, W.G., Falk, D., Magnotta, V.A., and Voss, M.W. (2016). The acute effects of aerobic exercise on the functional connectivity of human brain networks. Brain Plast. 2: 171–190, https://doi.org/10.3233/BPL-160039.Search in Google Scholar PubMed PubMed Central

Wesnes, K.A., Annas, P., Basun, H., Edgar, C., and Blennow, K. (2014). Performance on a pattern separation task by Alzheimer’s patients shows possible links between disrupted dentate gyrus activity and apolipoprotein e ∈4 status and cerebrospinal fluid amyloid-β42 levels. Alzheimer’s Res. Ther. 6: 1–8, https://doi.org/10.1186/alzrt250.Search in Google Scholar PubMed PubMed Central

Wesnes, K.A. and Burn, D.J. (2014). Compromised object pattern separation performance in Parkinson’s disease suggests dentate gyrus neurogenesis may be compromised in the condition. J. Alzheimer’s Dis. Park. 04: 5.10.4172/2161-0460.1000131Search in Google Scholar

Whiteman, A.S., Young, D.E., Budson, A.E., Stern, C.E., and Schon, K. (2016). Entorhinal volume, aerobic fitness, and recognition memory in healthy young adults: a voxel-based morphometry study. NeuroImage 126: 229–238, https://doi.org/10.1016/j.neuroimage.2015.11.049.Search in Google Scholar PubMed PubMed Central

Whiteman, A.S., Young, D.E., He, X., Chen, T.C., Wagenaar, R.C., Stern, C.E., and Schon, K. (2014). Interaction between serum BDNF and aerobic fitness predicts recognition memory in healthy young adults. Behav. Brain Res. 259: 302–312, https://doi.org/10.1016/j.bbr.2013.11.023.Search in Google Scholar PubMed PubMed Central

Wingenfeld, K. and Wolf, O.T. (2011). HPA axis alterations in mental disorders: impact on memory and its relevance for therapeutic interventions. CNS Neurosci. Ther. 17: 714–722, https://doi.org/10.1111/j.1755-5949.2010.00207.x.Search in Google Scholar PubMed PubMed Central

Wolf, O.T. (2009). Stress and memory in humans: twelve years of progress? Brain Res. 1293: 142–154, https://doi.org/10.1016/j.brainres.2009.04.013.Search in Google Scholar PubMed

Wong, A.W., Giuffrida, L., Wood, R., Peckham, H., Gonsalvez, D., Murray, S.S., Hughes, R.A., and Xiao, J. (2014). TDP6, a brain-derived neurotrophic factor-based trkB peptide mimetic, promotes oligodendrocyte myelination. Mol. Cell. Neurosci. 63: 132–140, https://doi.org/10.1016/j.mcn.2014.10.002.Search in Google Scholar PubMed

Wrann, C.D., White, J.P., Salogiannnis, J., Laznik-Bogoslavski, D., Wu, J., Ma, D., Lin, J.D., Greenberg, M.E., and Spiegelman, B.M. (2013). Exercise induces hippocampal BDNF through a PGC-1α/FNDC5 pathway. Cell Metab. 18: 649–659, https://doi.org/10.1016/j.cmet.2013.09.008.Search in Google Scholar PubMed PubMed Central

Xiao, J., Wong, A.W., Willingham, M.M., Van Den Buuse, M., Kilpatrick, T.J., and Murray, S.S. (2010). Brain-derived neurotrophic factor promotes central nervous system myelination via a direct effect upon oligodendrocytes. Neurosignals 18: 186–202, https://doi.org/10.1159/000323170.Search in Google Scholar PubMed

Yagi, S., Chow, C., Lieblich, S.E., and Galea, L.A.M. (2016). Sex and strategy use matters for pattern separation, adult neurogenesis, and immediate early gene expression in the hippocampus. Hippocampus 26: 87–101, https://doi.org/10.1002/hipo.22493.Search in Google Scholar PubMed

Yamasaki, M. and Takeuchi, T. (2017). Locus coeruleus and dopamine-dependent memory consolidation. Neural Plast. 2017: 8602690, https://doi.org/10.1155/2017/8602690.Search in Google Scholar PubMed PubMed Central

Yassa, M.A. and Stark, C.E.L. (2011). Pattern separation in the hippocampus. Trends Neurosci. 34: 515–525, https://doi.org/10.1016/j.tins.2011.06.006.Search in Google Scholar PubMed PubMed Central

Yau, S.Y., Lau, B.W.M., and So, K.F. (2011). Adult hippocampal neurogenesis: a possible way how physical exercise counteracts stress. Cell Transplant. 20: 99–111, https://doi.org/10.3727/096368910x532846.Search in Google Scholar

Young, W.S. and Kuhar, M.J. (1980). Noradrenergic α1 and α2 receptors: light microscopic autoradiographic localization. Proc. Natl. Acad. Sci. U. S. A. 77: 1696–1700, https://doi.org/10.1073/pnas.77.3.1696.Search in Google Scholar PubMed PubMed Central

Yun, S., Reynolds, R.P., Masiulis, I., and Eisch, A.J. (2016). Re-evaluating the link between neuropsychiatric disorders and dysregulated adult neurogenesis. Nat. Med. 22: 1239–1247, https://doi.org/10.1038/nm.4218.Search in Google Scholar PubMed PubMed Central

Ziv, Y., Ron, N., Butovsky, O., Landa, G., Sudai, E., Greenberg, N., Cohen, H., Kipnis, J., and Schwartz, M. (2006). Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat. Neurosci. 9: 268–275, https://doi.org/10.1038/nn1629.Search in Google Scholar PubMed

Ziv, Y. and Schwartz, M. (2008). Immune-based regulation of adult neurogenesis: implications for learning and memory. Brain Behav. Immun. 22: 167–176, https://doi.org/10.1016/j.bbi.2007.08.006.Search in Google Scholar PubMed

Zotow, E., Bisby, J.A., and Burgess, N. (2020). Behavioral evidence for pattern separation in human episodic memory. Learn. Mem. 27: 301–310, https://doi.org/10.1101/lm.051821.120.Search in Google Scholar PubMed PubMed Central

Zschucke, E., Renneberg, B., Dimeo, F., Wüstenberg, T., and Ströhle, A. (2015). The stress-buffering effect of acute exercise: evidence for HPA axis negative feedback. Psychoneuroendocrinology 51: 414–425, https://doi.org/10.1016/j.psyneuen.2014.10.019.Search in Google Scholar PubMed