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Phys Act Nutr > Volume 23(4); 2019 > Article
Moon and van Praag: Physical Activity and Brain Plasticity

Abstract

Recent research suggests that the brain has capable of remarkable plasticity and physical activity can enhance it. In this editorial letter, we summarize the role of hippocampal plasticity in brain functions. Furthermore, we briefly sketched the factors and mechanisms of motion that influence brain plasticity. We conclude that physical activity can be an encouraging intervention for brain restoration through neuronal plasticity. At the same time, we suggest that a mechanistic understanding of the beneficial effects of exercise should be accompanied in future studies.

Studies have demonstrated that physical activity affects brain plasticity, cognition and mood1-4. Indeed, animal experiments and clinical studies show tremendous biological and psychological benefits of physical activity, and accompanying structural and functional changes in the various brain regions5,6. In recent years, the effect of physical activity on memory improvement in neurodegenerative diseases patients has attracted attention7. The circuits of the limbic system are known to regulate learning and memory function8,9. Subjects with cognitive impairment have been shown to have reduced volume in the hippocampus and forebrain10-12. Adult neurons have been thought to be unable to be replaced by new cells because cell division is over, but recent studies have found that new neurons are born (neurogenesis) in select regions of the adult brain and may contribute to maintainance of neuronal function13. Experiments utilizing the thymidine analog bromodeoxyuridine (BrdU) to label dividing cells and several genetic markers have revealed that hippocampal dentate gyrus is one of the brain regions showing the neurogenesis in mature animals, and this was conserved in rodents, primates, and humans13,14. Adult neurogenesis was also proven in bird studies; a comparison of hippocampus size and number of neurons with a long-traveled migratory bird and a non-traveling migratory bird also shows that hippocampus may be important for memory and experience15. In addition, chickadees exhibit enhanced neurogenesis when they store seeds for winter16.
Neuronal plasticity is key feature for the cognition and it is regulated by neurogenesis, synapse formation, angiogenesis and changes in neurotransmitter system3,6,9. Animal experiments using voluntary wheel cages and treadmills have reported that exercise increases the proliferation of neurons in the hippocampus of rodents3. Exercise induces the changes of the neurotransmitter systems such as serotonin and acetylcholine and the release of factors such as BDNF and IGF-12,17. Along with these changes, exercise improves the cognitive functions such as spatial and executive functions18,19. These changes may also be very effective interventions in aging and degenerative brain disease models20,21.
Recent studies have shown that exercise promotes the release of factors such as peripheral BDNF22, IRSIN23, IGF24, and Cathepsin B5, which are systemically delivered to the brain and may play a role in cognitive function. Furthermore, we found that conditioned media which containing secreted proteins from skeletal muscle cells could influence adult hippocampal neural progenitor cell (aNPC) differentiation25. Exercise induced neurogenesis can be also affected through epigenetic modifications26 or the balance of intestinal microflora27. In fact, even though the mechanisms are not clearly investigated, there are reports demonstrating exercise affects intestinal microorganisms28 or brain epigenetics29. There has been little research on the effects of metabolites on the brain and nerve system. Studies have shown that these metabolites are not only end products during metabolism but also act as hormones in a variety of physiological and pathological conditions as a signaling material30,31. In the near future, exercise-induced changes in these biological markers may be the candidate target of new exercise mimetics and may play an important role in proposing or prescribing exercise appropriate to the individual's health status. Most of the cross sectional studies investigating changes in the human brain after exercise have limitations in observing the neuronal adaptation during or after exercise. Future studies are needed to understand the effects and mechanisms of exercise from a systemic and longitudinal view. Moreover, human studies are needed to show that exercise is important for the learning and memory function via hippocampal neurogenesis.

Acknowledgments

This work was supported by the National Research Foundation (NRF, 700-20190019) and Korea Mouse Phenotype Center (NRF, 2019M3A9D5A01102794).

References

1.
van Praag H, Shubert T, Zhao C, Gage FH. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci. 2005;25:8680-5.
crossref
van Praag H, Shubert T, Zhao C, Gage FH. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 2005;25:8680-5. PMID: 10.1523/JNEUROSCI.1731-05.2005. PMID: 16177036.
2.
Moon HY, Kim SH, Yang YR, Song P, Yu HS, Park HG, Hwang O, Lee-Kwon W, Seo JK, Hwang D, Choi JH, Bucala R, Ryu SH, Kim YS, Suh PG. Macrophage migration inhibitory factor mediates the antidepressant actions of voluntary exercise. Proc Natl Acad Sci U S A. 2012;109:13094-9.
crossref
Moon HY, Kim SH, Yang YR, Song P, Yu HS, Park HG, Hwang O, Lee-Kwon W, Seo JK, Hwang D, Choi JH, Bucala R, Ryu SH, Kim YS, Suh PG. Macrophage migration inhibitory factor mediates the antidepressant actions of voluntary exercise. Proc Natl Acad Sci U S A 2012;109:13094-9. PMID: 10.1073/pnas.1205535109. PMID: 22826223.
3.
Vivar C, Potter MC, van Praag H. All about running: synaptic plasticity, growth factors and adult hippocampal neurogenesis. Curr Top Behav Neurosci. 2013;15:189-210.
crossref
Vivar C, Potter MC, van Praag H. All about running: synaptic plasticity, growth factors and adult hippocampal neurogenesis. Curr Top Behav Neurosci 2013;15:189-210. PMID: 10.1007/7854_2012_220. PMID: 22847651.
4.
Chang H, Kim K, Jung YJ, Kato M. Effects of acute high-Intensity resistance exercise on cognitive function and oxygenation in prefrontal cortex. J Exerc Nutrition Biochem. 2017;21:1-8.
crossref
Chang H, Kim K, Jung YJ, Kato M. Effects of acute high-Intensity resistance exercise on cognitive function and oxygenation in prefrontal cortex. J Exerc Nutrition Biochem 2017;21:1-8. PMID: 10.20463/jenb.2017.0012.
5.
Moon HY, Becke A, Berron D, Becker B, Sah N, Benoni G, Janke E, Lubejko ST, Greig NH, Mattison JA, Duzel E, van Praag H. Running-Induced Systemic Cathepsin B Secretion Is Associated with Memory Function. Cell Metab. 2016;24:332-40.
crossref
Moon HY, Becke A, Berron D, Becker B, Sah N, Benoni G, Janke E, Lubejko ST, Greig NH, Mattison JA, Duzel E, van Praag H. Running-Induced Systemic Cathepsin B Secretion Is Associated with Memory Function. Cell Metab 2016;24:332-40. PMID: 10.1016/j.cmet.2016.05.025. PMID: 27345423.
6.
Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, Kim JS, Heo S, Alves H, White SM, Wojcicki TR, Mailey E, Vieira VJ, Martin SA, Pence BD, Woods JA, McAuley E, Kramer AF. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A. 2011;108:3017-22.
crossref
Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, Kim JS, Heo S, Alves H, White SM, Wojcicki TR, Mailey E, Vieira VJ, Martin SA, Pence BD, Woods JA, McAuley E, Kramer AF. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A 2011;108:3017-22. PMID: 10.1073/pnas.1015950108. PMID: 21282661.
7.
Radak Z, Hart N, Sarga L, Koltai E, Atalay M, Ohno H, Boldogh I. Exercise plays a preventive role against Alzheimer's disease. J Alzheimers Dis. 2010;20:777-83.
crossref
Radak Z, Hart N, Sarga L, Koltai E, Atalay M, Ohno H, Boldogh I. Exercise plays a preventive role against Alzheimer's disease. J Alzheimers Dis 2010;20:777-83. PMID: 10.3233/JAD-2010-091531. PMID: 20182027.
8.
Vivar C, Peterson BD, van Praag H. Running rewires the neuronal network of adult-born dentate granule cells. Neuroimage. 2016;131:29-41.
crossref
Vivar C, Peterson BD, van Praag H. Running rewires the neuronal network of adult-born dentate granule cells. Neuroimage 2016;131:29-41. PMID: 10.1016/j.neuroimage.2015.11.031. PMID: 26589333.
9.
Greenwood PM, Parasuraman R. Neuronal and cognitive plasticity: a neurocognitive framework for ameliorating cognitive aging. Front Aging Neurosci. 2010;2:150.
crossref
Greenwood PM, Parasuraman R. Neuronal and cognitive plasticity: a neurocognitive framework for ameliorating cognitive aging. Front Aging Neurosci 2010 2:150. PMID: 10.3389/fnagi.2010.00150.
10.
Khan UA, Liu L, Provenzano FA, Berman DE, Profaci CP, Sloan R, Mayeux R, Duff KE, Small SA. Molecular drivers and cortical spread of lateral entorhinal cortex dysfunction in preclinical Alzheimer's disease. Nat Neurosci. 2014;17:304-11.
crossref pdf
Khan UA, Liu L, Provenzano FA, Berman DE, Profaci CP, Sloan R, Mayeux R, Duff KE, Small SA. Molecular drivers and cortical spread of lateral entorhinal cortex dysfunction in preclinical Alzheimer's disease. Nat Neurosci 2014;17:304-11. PMID: 10.1038/nn.3606. PMID: 24362760.
11.
Grothe MJ, Heinsen H, Amaro E, Jr, Grinberg LT, Teipel SJ. Cognitive Correlates of Basal Forebrain Atrophy and Associated Cortical Hypometabolism in Mild Cognitive Impairment. Cereb Cortex. 2016;26:2411-26.
crossref pdf
Grothe MJ, Heinsen H, Amaro E Jr, Grinberg LT, Teipel SJ. Cognitive Correlates of Basal Forebrain Atrophy and Associated Cortical Hypometabolism in Mild Cognitive Impairment. Cereb Cortex 2016;26:2411-26. PMID: 10.1093/cercor/bhv062. PMID: 25840425.
12.
Mueller SG, Schuff N, Yaffe K, Madison C, Miller B, Weiner MW. Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer's disease. Hum Brain Mapp. 2010;31:1339-47.
crossref
Mueller SG, Schuff N, Yaffe K, Madison C, Miller B, Weiner MW. Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer's disease. Hum Brain Mapp 2010;31:1339-47. PMID: 10.1002/hbm.20934. PMID: 20839293.
13.
Gage FH. Adult neurogenesis in mammals. Science. 2019;364:827-28.
crossref
Gage FH. Adult neurogenesis in mammals. Science 2019;364:827-28. PMID: 10.1126/science.aav6885. PMID: 31147506.
14.
Moon HY. Differential expression of genes in the subgranular zone and granular cell layer of the hippocampus after running. J Exerc Nutrition Biochem. 2018;22:1-6.
crossref
Moon HY. Differential expression of genes in the subgranular zone and granular cell layer of the hippocampus after running. J Exerc Nutrition Biochem 2018;22:1-6. PMID: 10.20463/jenb.2018.0025.
15.
Healy SD, Gwinner E, Krebs JR. Hippocampal volume in migratory and non-migratory warblers: effects of age and experience. Behav Brain Res. 1996;81:61-8.
crossref
Healy SD, Gwinner E, Krebs JR. Hippocampal volume in migratory and non-migratory warblers: effects of age and experience. Behav Brain Res 1996;81:61-8. PMID: 10.1016/S0166-4328(96)00044-7. PMID: 8950002.
16.
Barnea A, Nottebohm F. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci U S A. 1994;91:11217-21.
crossref
Barnea A, Nottebohm F. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci U S A 1994;91:11217-21. PMID: 10.1073/pnas.91.23.11217. PMID: 7972037.
17.
Guerrieri D, Moon HY, van Praag H. Exercise in a Pill: The Latest on Exercise-Mimetics. Brain Plast. 2017;2:153-69.
crossref
Guerrieri D, Moon HY, van Praag H. Exercise in a Pill: The Latest on Exercise-Mimetics. Brain Plast 2017;2:153-69. PMID: 10.3233/BPL-160043. PMID: 29765854.
18.
Weinstein AM, Voss MW, Prakash RS, Chaddock L, Szabo A, White SM, Wojcicki TR, Mailey E, McAuley E, Kramer AF, Erickson KI. The association between aerobic fitness and executive function is mediated by prefrontal cortex volume. Brain Behav Immun. 2012;26:811-9.
crossref
Weinstein AM, Voss MW, Prakash RS, Chaddock L, Szabo A, White SM, Wojcicki TR, Mailey E, McAuley E, Kramer AF, Erickson KI. The association between aerobic fitness and executive function is mediated by prefrontal cortex volume. Brain Behav Immun 2012;26:811-9. PMID: 10.1016/j.bbi.2011.11.008. PMID: 22172477.
19.
Creer DJ, Romberg C, Saksida LM, van Praag H, Bussey TJ. Running enhances spatial pattern separation in mice. Proc Natl Acad Sci U S A. 2010;107:2367-72.
crossref
Creer DJ, Romberg C, Saksida LM, van Praag H, Bussey TJ. Running enhances spatial pattern separation in mice. Proc Natl Acad Sci U S A 2010;107:2367-72. PMID: 10.1073/pnas.0911725107. PMID: 20133882.
20.
Kannangara TS, Lucero MJ, Gil-Mohapel J, Drapala RJ, Simpson JM, Christie BR, van Praag H. Running reduces stress and enhances cell genesis in aged mice. Neurobiol Aging. 2011;32:2279-86.
crossref
Kannangara TS, Lucero MJ, Gil-Mohapel J, Drapala RJ, Simpson JM, Christie BR, van Praag H. Running reduces stress and enhances cell genesis in aged mice. Neurobiol Aging 2011;32:2279-86. PMID: 10.1016/j.neurobiolaging.2009.12.025. PMID: 20106549.
21.
Marlatt MW, Potter MC, Bayer TA, van Praag H, Lucassen PJ. Prolonged running, not fluoxetine treatment, increases neurogenesis, but does not alter neuropathology, in the 3xTg mouse model of Alzheimer's disease. Curr Top Behav Neurosci. 2013;15:313-40.
crossref
Marlatt MW, Potter MC, Bayer TA, van Praag H, Lucassen PJ. Prolonged running, not fluoxetine treatment, increases neurogenesis, but does not alter neuropathology, in the 3xTg mouse model of Alzheimer's disease. Curr Top Behav Neurosci 2013;15:313-40. PMID: 10.1007/7854_2012_237. PMID: 23670818.
22.
Nascimento CM, Pereira JR, Pires de Andrade L, Garuffi M, Ayan C, Kerr DS, Talib LL, Cominetti MR, Stella F. Physical exercise improves peripheral BDNF levels and cognitive functions in mild cognitive impairment elderly with different bdnf Val66Met genotypes. J Alzheimers Dis. 2015;43:81-91.
crossref
Nascimento CM, Pereira JR, Pires de Andrade L, Garuffi M, Ayan C, Kerr DS, Talib LL, Cominetti MR, Stella F. Physical exercise improves peripheral BDNF levels and cognitive functions in mild cognitive impairment elderly with different bdnf Val66Met genotypes. J Alzheimers Dis 2015;43:81-91. PMID: 10.3233/JAD-140576. PMID: 25062900.
23.
Lourenco MV, Frozza RL, de Freitas GB, Zhang H, Kincheski GC, Ribeiro FC, Gonçalves RA, Clarke JR, Beckman D, Staniszewski A, Berman H, Guerra LA, Forny-Germano L, Meier S, Wilcock DM, de Souza JM, Alves-Leon S, Prado VF, Prado MAM, Abisambra JF, Tovar-Moll F, Mattos P, Arancio O, Ferreira ST, De Felice FG. Exercise-linked FNDC5/irisin rescues synaptic plasticity and memory defects in Alzheimer's models. Nat Med. 2019;25:165-75.
crossref pdf
Lourenco MV, Frozza RL, de Freitas GB, Zhang H, Kincheski GC, Ribeiro FC, Gonçalves RA, Clarke JR, Beckman D, Staniszewski A, Berman H, Guerra LA, Forny-Germano L, Meier S, Wilcock DM, de Souza JM, Alves-Leon S, Prado VF, Prado MAM, Abisambra JF, Tovar-Moll F, Mattos P, Arancio O, Ferreira ST, De Felice FG. Exercise-linked FNDC5/irisin rescues synaptic plasticity and memory defects in Alzheimer's models. Nat Med 2019;25:165-75. PMID: 10.1038/s41591-018-0275-4. PMID: 30617325.
24.
Stein AM, Silva TMV, Coelho FGM, Arantes FJ, Costa JLR, Teodoro E, Santos-Galduróz RF. Physical exercise, IGF-1 and cognition A systematic review of experimental studies in the elderly. Dement Neuropsychol. 2018;12:114-22.
crossref pdf
Stein AM, Silva TMV, Coelho FGM, Arantes FJ, Costa JLR, Teodoro E, Santos-Galduróz RF. Physical exercise, IGF-1 and cognition A systematic review of experimental studies in the elderly. Dement Neuropsychol 2018;12:114-22. PMID: 10.1590/1980-57642018dn12-020003. PMID: 29988330.
25.
Moon HY, Javadi S, Stremlau M, Yoon KJ, Becker B, Kang SU, Zhao X, van Praag H. Conditioned media from AICAR-treated skeletal muscle cells increases neuronal differentiation of adult neural progenitor cells. Neuropharmacology. 2019;145:123-30.
crossref
Moon HY, Javadi S, Stremlau M, Yoon KJ, Becker B, Kang SU, Zhao X, van Praag H. Conditioned media from AICAR-treated skeletal muscle cells increases neuronal differentiation of adult neural progenitor cells. Neuropharmacology 2019;145:123-30. PMID: 10.1016/j.neuropharm.2018.10.041. PMID: 30391731.
26.
Sun J, Sun J, Ming GL, Song H. Epigenetic regulation of neurogenesis in the adult mammalian brain. Eur J Neurosci. 2011;33:1087-93.
crossref
Sun J, Sun J, Ming GL, Song H. Epigenetic regulation of neurogenesis in the adult mammalian brain. Eur J Neurosci 2011;33:1087-93. PMID: 10.1111/j.1460-9568.2011.07607.x. PMID: 21395852.
27.
Ma Q, Xing C, Long W, Wang HY, Liu Q, Wang RF. Impact of microbiota on central nervous system and neurological diseases: the gut-brain axis. J Neuroinflammation. 2019;16:53.
crossref pdf
Ma Q, Xing C, Long W, Wang HY, Liu Q, Wang RF. Impact of microbiota on central nervous system and neurological diseases: the gut-brain axis. J Neuroinflammation 2019;16:53PMID: 10.1186/s12974-019-1434-3. PMID: 30823925.
28.
Motiani KK, Collado MC, Eskelinen JJ, Virtanen KA, Löyttyniemi E, Salminen S, Nuutila P, Kalliokoski KK, Hannukainen JC. Exercise Training Modulates Gut Microbiota Profile and Improves Endotoxemia. Med Sci Sports Exerc. 2020;52:94-104.
crossref
Motiani KK, Collado MC, Eskelinen JJ, Virtanen KA, Löyttyniemi E, Salminen S, Nuutila P, Kalliokoski KK, Hannukainen JC. Exercise Training Modulates Gut Microbiota Profile and Improves Endotoxemia. Med Sci Sports Exerc 2020;52:94-104. PMID: 10.1249/MSS.0000000000002112. PMID: 31425383.
29.
Fernandes J, Arida RM, Gomez-Pinilla F. Physical exercise as an epigenetic modulator of brain plasticity and cognition. Neurosci Biobehav Rev. 2017;80:443-56.
crossref
Fernandes J, Arida RM, Gomez-Pinilla F. Physical exercise as an epigenetic modulator of brain plasticity and cognition. Neurosci Biobehav Rev 2017;80:443-56. PMID: 10.1016/j.neubiorev.2017.06.012. PMID: 28666827.
30.
Lauber SN, Gooderham NJ. The cooked meat derived genotoxic carcinogen 2-amino-3-methylimidazo[4,5-b]pyridine has potent hormone-like activity: mechanistic support for a role in breast cancer. Cancer Res. 2007;67:9597-602.
crossref
Lauber SN, Gooderham NJ. The cooked meat derived genotoxic carcinogen 2-amino-3-methylimidazo[4,5-b]pyridine has potent hormone-like activity: mechanistic support for a role in breast cancer. Cancer Res 2007;67:9597-602. PMID: 10.1158/0008-5472.CAN-07-1661. PMID: 17909072.
31.
Morali G, Lemus AE, Munguia R, García GA, Grillasca I, Pérez-Palacios G. Hormone-like behavioral effects of levonorgestrel and its metabolites in the male rat. Pharmacol Biochem Behav. 2002;73:951-61.
crossref
Morali G, Lemus AE, Munguia R, García GA, Grillasca I, Pérez-Palacios G. Hormone-like behavioral effects of levonorgestrel and its metabolites in the male rat. Pharmacol Biochem Behav 2002;73:951-61. PMID: 10.1016/S0091-3057(02)00946-2. PMID: 12213542.
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