The beneficial effects of physical activity on impaired adult neurogenesis and cognitive performance

Frontiers in Neuroscience

Volumn , Issue APR, 2011, Pages

  Lafenetre, Pauline ^a,b   Leske, Oliver ^b   Wahle, Petra ^b   Heumann, Rolf ^b  

^a NutriNeuro Bordeaux University   (France)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

BDNF; Exercise; Learning; Memory; Object recognition; Ras

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; METHYLAZOXYMETHANOL; NEUROTROPHIN; TEMOZOLOMIDE;

ADULT; BRAIN CELL; COGNITION; COGNITIVE DEFECT; ENVIRONMENTAL FACTOR; EPIGENETICS; HIPPOCAMPUS; HUMAN; LEARNING; MEMORY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; PHYSICAL ACTIVITY; PROTEIN EXPRESSION; PSYCHOMOTOR DISORDER; REGULATORY MECHANISM; REVIEW; TRANSGENIC MOUSE;

EID: 80051993184     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2011.00051     Document Type: Review

References (79)

1. Aimone, J. B., Deng, W., and Gage, F. H. (2010). Adult neurogenesis: integrating theories and separat-ing functions. Trends Cogn. Sci. 14, 325-337.
2. Aimone, J. B., Wiles, J., and Gage, F. H. (2009). Computational influence of adult neurogenesis on memory encod-ing. Neuron 61, 187-202.
3. Altman, J., and Das, G. D. (1965). Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124, 319-335.
4. Anderson, B. J., Rapp, D. N., Baek, D. H., McCloskey, D. P., Coburn-Litvak, P. S., and Robinson, J. K. (2000). Exercise influences spatial learning in the radial arm maze. Physiol. Behav. 70, 425-429.
5. Baruch, D. E., Swain, R. A., and Helmstetter, F. J. (2004). Effects of exercise on Pavlovian fear condition-ing. Behav. Neurosci. 118, 1123-1127.
6. Bath, K. G., Mandairon, N., Jing, D., Rajagopal, R., Kapoor, R., Chen, Z. Y., Khan, T., Proenca, C. C., Kraemer, R., Cleland, T. A., Hempstead, B. L., Chao, M. V., and Lee, F. S. (2008). Variant brain-derived neurotrophic factor (Val66Met) alters adult olfactory bulb neurogenesis and spontaneous olfactory discrimination. J. Neurosci. 28, 2383-2393.
7. Bergami, M., Rimondini, R., Santi, S., Blum, R., Gotz, M., and Canossa, M. (2008). Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proc. Natl. Acad. Sci. U.S.A. 105, 15570-15575.
8. Binder, D. K., and Scharfman, H. E. (2004). Brain-derived neurotrophic factor. Growth Factors 22, 123-131.
9. Brown, J., Cooper-Kuhn, C. M., Kempermann, G., van Praag,. H., Winkler, J., Gage, F. H., and Kuhn, H. G. (2003). Enriched environment and physical activity stimulate hippocam-pal but not olfactory bulb neurogen-esis. Eur. J. Neurosci. 17, 2042-2046.
10. Bruel-Jungerman, E., Rampon, C., and Laroche, S. (2007). Adult hippocampal neurogenesis, synaptic plasticity and memory: facts and hypotheses. Rev. Neurosci. 18, 93-114.
11. Choi, S. H., Li, Y., Parada, L. F., and Sisodia, S. S. (2009). Regulation of hippocam-pal progenitor cell survival, prolifera-tion and dendritic development by BDNF. Mol. Neurodegener. 4, 52.
12. Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D. Jr., Fragniere, A., Tyers, P., Jessberger, S., Saksida, L. M., Barker, R. A., Gage, F. H., and Bussey, T. J. (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325, 210-213.
13. Cotman, C. W., and Berchtold, N. C. (2002). Exercise: a behavioral inter-vention to enhance brain health and plasticity. Trends Neurosci. 25, 295-301.
14. Covic, M., Karaca, E., and Lie, D.C. (2010). Epigenetic regulation of neurogenesis in the adult hippocampus. Heredity, 105, 122-134.
15. Creer, D. J., Romberg, C., Saksida, L. M., Van Praag, H., and Bussey, T. J. (2010). Running enhances spatial pattern sep-aration in mice. Proc. Natl. Acad. Sci. U.S.A. 107, 2367-2372.
16. D'Alessio, L., Konopka, H., Lopez, E. M., Seoane, E., Consalvo, D., Oddo, S., Kochen, S., and Lopez-Costa, J. J. (2010). Doublecortin (DCX) immunoreactivity in hippocampus of chronic refractory temporal lobe epilepsy patients with hippocampal sclerosis. Seizure 19, 567-572.
17. Deng, W., Aimone, J. B., and Gage, F. H. (2010). New neurons and new memo-ries: how does adult hippocampal neu-rogenesis affect learning and memory? Nat. Rev. Neurosci. 11, 339-350.
18. Deng, W., Saxe, M. D., Gallina, I. S., and Gage, F. H. (2009). Adult-born hippoc-ampal dentate granule cells undergo-ing maturation modulate learning and memory in the brain. J. Neurosci. 29, 13532-13542.
19. Donovan, M. H., Yamaguchi, M., and Eisch, A. J. (2008). Dynamic expression of TrkB receptor protein on prolifer-ating and maturing cells in the adult mouse dentate gyrus. Hippocampus 18, 435-439.
20. Dupret, D., Revest, J. M., Koehl, M., Ichas, F., De Groot, F., Costet, P., Abrous, D. N., and Piazza, P. V. (2008). Spatial relational memory requires hip-pocampal adult neurogenesis. PLoS ONE 3, e1959. doi: 10.1371/journal. pone.0001959
21. Eriksson, P. S., Perfilieva, E., Bjork-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.
22. 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.
23. Fabel, K., and Kempermann, G. (2008). Physical activity and the regulation of neurogenesis in the adult and aging brain. Neuromolecular. Med. 10, 59-66.
24. Farioli-Vecchioli, S., Saraulli, D., Costanzi, M., Pacioni, S., Cina, I., Aceti, M., Micheli,L., Bacci,A., Cestari,V., and Tirone,F. (2008). The timing of dif-ferentiation of adult hippocampal neurons is crucial for spatial memory. PLoS Biol. 6, e246. doi: 10.1371/jour-nal.pbio.0060246
25. 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 rats in vivo. Neuroscience 124, 71-79.
26. Fordyce, D. E., and Farrar, R. P. (1991). Enhancement of spatial learning in F344 rats by physical activity and related learning-associated alterations in hippocampal and cortical choliner-gic functioning. Behav. Brain Res. 46, 123-133.
27. Garthe, A., Behr, J., and Kempermann, G. (2009). Adult-generated hippocampal neurons allow the flexible use of spa-tially precise learning strategies. PLoS ONE 4, e5464. doi: 10.1371/journal. pone.0005464
28. Gilbert, P. E., Kesner, R. P., and Lee, I. (2001). Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1. Hippocampus 11, 626-636.
29. Hernandez-Rabaza, V., Llorens-Martin, M., Velazquez-Sanchez, C., Ferragud, A., Arcusa, A., Gumus, H. G., Gomez-Pinedo, U., Perez-Villalba, A., Rosello, J., Trejo, J. L., Barcia, J. A., and Canales, J. J. (2009). Inhibition of adult hip-pocampal neurogenesis disrupts contextual learning but spares spatial working memory, long-term con-ditional rule retention and spatial reversal. Neuroscience 159, 59-68.
30. Holmes, M. M., Galea, L. A., Mistlberger, R. E., and Kempermann, G. (2004). Adult hippocampal neurogenesis and voluntary running activity: cir-cadian and dose-dependent effects. J. Neurosci. Res. 76, 216-222.
31. Imayoshi, I., Sakamoto, M., Ohtsuka, T., Takao, K., Miyakawa, T., Yamaguchi, M., Mori, K., Ikeda, T., Itohara, S., and Kageyama, R. (2008). Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat. Neurosci. 11, 1153-1161.
32. Jansen, R., Linkenkaer-Hansen, K., Heistek, T., Timmerman, J., Mansvelder, H. D., Brussaard, A. B., de Gunst, G. M., and van Ooyen, O. A. (2009). Inbred mouse strains dif-fer in multiple hippocampal activity traits. Eur. J. Neurosci. 30, 1092-1100.
33. Jessberger, S., Clark, R. E., Broadbent, N. J., Clemenson, G. D. Jr., Consiglio, A., Lie, D. C., Squire, L. R., and Gage, F. H. (2009). Dentate gyrus-specific knock-down of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn. Mem. 16, 147-154.
34. Jin, K., Peel, A. L., Mao, X. O., Xie, L., Cottrell, B. A., Henshall, D. C., and Greenberg, D. A. (2004). Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 101, 343-347.
35. Kannangara, T. S., Lucero, M. J., Gil-Mohapel, J., Drapala, R. J., Simpson, J. M., Christie, B. R., and van Praag, H. (2010). Running reduces stress and enhances cell genesis in aged mice. Neurobiol. Aging. doi:10.1016/j. neurobiolaging.2009.12.025. [Epub ahead of print].
36. Kannangara, T. S., Webber, A., Gil-Mohapel, J., and Christie, B. R. (2009). Stress differentially regulates the effects of voluntary exercise on cell proliferation in the dentate gyrus of mice. Hippocampus 19, 889-897.
37. Kempermann, G., and Gage, F. H. (1999). New nerve cells for the adult brain. Sci. Am. 280, 48-53.
38. Kempermann, G., and Gage, F. H. (2002). Genetic influence on phenotypic dif-ferentiation in adult hippocampal neurogenesis. Brain Res. Dev. Brain Res. 134, 1-12.
39. Kempermann, G., Jessberger, S., Steiner, B., and Kronenberg, G. (2004). Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 27, 447-452.
40. Kempermann, G., Kuhn, H. G., and Gage, F. H. (1998a). Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci. 18, 3206-3212.
41. Kempermann, G., Brandon, E. P., and Gage, F. H. (1998b). Environmental stimulation of 129/SvJ mice causes increased cell proliferation and neu-rogenesis in the adult dentate gyrus. Curr. Biol. 8, 939-942.
42. Kerr, A. L., Steuer, E. L., Pochtarev, V., and Swain, R. A. (2010). Angiogenesis but not neurogenesis is critical for normal learning and memory acquisition. Neuroscience 171, 214-226.
43. Kitamura, T., Saitoh, Y., Takashima, N., Murayama, A., Niibori, Y., Ageta, H., Sekiguchi, M., Sugiyama, H., and Inokuchi, K. (2009). Adult neuro-genesis modulates the hippocampus-dependent period of associative fear memory. Cell 139, 814-827.
44. Ko, H. G., Jang, D. J., Son, J., Kwak, C., Choi, J. H., Ji, Y. H., Lee, Y. S., Son, H., and Kaang, B. K. (2009). Effect of ablated hippocampal neurogenesis on the formation and extinction of con-textual fear memory. Mol. Brain 2, 1.
45. Kronenberg, G., Bick-Sander, A., Bunk, E., Wolf, C., Ehninger, D., and Kempermann, G. (2006). Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiol. Aging 27, 1505-1513.
46. Kuhn, H. G., Dickinson-Anson, H., and Gage, F. H. (1996). Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal pro-genitor proliferation. J. Neurosci. 16, 2027-2033.
47. Lafenetre, P., Leske, O., Ma-Hogemeier, Z., Haghikia, A., Bichler, Z., Wahle, P., and Heumann, R. (2010). Exercise can rescue recognition memory impair-ment in a model with reduced adult hippocampal neurogenesis. Front. Behav. Neurosci. 3:34. doi: 10.3389/ neuro.08.034.2009
48. Leasure, J. L., and Decker, L. (2009). Social isolation prevents exercise-induced proliferation of hippocampal progeni-tor cells in female rats. Hippocampus 19, 907-912.
49. Lee, J., Seroogy, K. B., and Mattson, M. P. (2002). Dietary restriction enhances neurotrophin expression and neuro-genesis in the hippocampus of adult mice. J. Neurochem. 80, 539-547.
50. Madsen, T. M., Kristjansen, P. E., Bolwig, T. G., and Wortwein, G. (2003). Arrested neuronal proliferation and impaired hippocampal function following frac-tionated brain irradiation in the adult rat. Neuroscience 119, 635-642.
51. Manns, M., Bichler, Z., Leske, O., and Heumann, R. (2010). Neuronal Ras activation inhibits adult hippocampal progenitor cell division and impairs spatial short-term memory. Genes Brain Behav. 9, 525-536.
52. Matsuo, N., Takao, K., Nakanishi, K., Yamasaki, N., Tanda, K., and Miyakawa, T. (2010). Behavioral profiles of three C57BL/6 substrains. Front. Behav. Neurosci. 4:29. doi: 10.3389/fnbeh.2010.00029
53. McAllister, A. K., Katz, L. C., and Lo, D. C. (1996). Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 17, 1057-1064.
54. 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 recep-tors mediate rapid pattern separation in the hippocampal network. Science 317, 94-99.
55. Meshi, D., Drew, M. R., Saxe, M., Ansorge, M. S., David, D., Santarelli, L., Malapani, C., Moore, H., and Hen, R. (2006). Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat. Neurosci. 9, 729-731.
56. Olson, A. K., Eadie, B. D., Ernst, C., and Christie, B. R. (2006). Environemental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 16, 250-260.
57. Raber, J., Rola, R., LeFevour, A., Morhardt, D., Curley, J., Mizumatsu, S., VandenBerg, S. R., and Fike, J. R. (2004). Radiation-induced cogni-tive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat. Res. 162, 39-47.
58. Rola, R., Raber, J., Rizk, A., Otsuka, S., VandenBerg, S. R., Morhardt, D. R., and Fike, J. R. (2004). Radiation-induced impairment of hippocampal neurogenesis is associated with cogni-tive deficits in young mice. Exp. Neurol. 188, 316-330.
59. Rossi, C., Angelucci, A., Costantin, L., Braschi, C., Mazzantini, M., Babbini, F., Fabbri, M. E., Tessarollo, L., Maffei, L., Berardi, N., and Caleo, M. (2006). Brain-derived neurotrophic factor (BDNF) is required for the enhance-ment of hippocampal neurogenesis following environmental enrichment. Eur. J. Neurosci. 24, 1850-1856.
60. Sairanen, M., Lucas, G., Ernfors, P., Castren, M., and Castren, E. (2005). Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J. Neurosci. 25, 1089-1094.
61. Saxe, M. D., Battaglia, F., Wang, J. W., Malleret, G., David, D. J., Monckton, J. E., Garcia, A. D., Sofroniew, M. V., Kandel, E. R., Santarelli, L., Hen, R., and Drew, M. R. (2006). Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl. Acad. Sci. U.S.A. 103, 17501-17506.
62. Scharfman, H., Goodman, J., Macleod, A., Phani, S., Antonelli, C., and Croll, S. (2005). Increased neurogenesis and the ectopic granule cells after intrahip-pocampal BDNF infusion in adult rats. Exp. Neurol. 192, 348-356.
63. Shors, T. J., Townsend, D. A., Zhao, M., Kozorovitskiy, Y., and Gould, E. (2002). Neurogenesis may relate to some but not all types of hippocam-pal-dependent learning. Hippocampus 12, 578-584.
64. Siegmund, A., Langnaese, K., and Wotjak, C. T. (2005). Differences in extinction of conditioned fear in C57BL/6 sub-strains are unrelated to expression of alpha-synuclein. Behav. Brain Res. 157, 291-298.
65. Snyder, J. S., Glover, L. R., Sanzone, K. M., Kamhi, J. F., and Cameron, H. A. (2009). The effects of exercise and stress on the survival and matura-tion of adult-generated granule cells. Hippocampus 19, 898-906.
66. Snyder, J. S., Hong, N. S., McDonald, R. J., and Wojtowicz, J. M. (2005). A role for adult neurogenesis in spatial long-term memory. Neuroscience 130, 843-852.
67. Stranahan, A. M., Khalil, D., and Gould, E. (2006). Social isolation delays the positive effects of running on adult neurogenesis. Nat. Neurosci. 9, 526-533.
68. Tolwani, R. J., Buckmaster, P. S., Varma, S., Cosgaya, J. M., Wu, Y., Suri, C., and Shooter, E. M. (2002). BDNF overex-pression increases dendrite complex-ity in hippocampal dentate gyrus. Neuroscience 114, 795-805.
69. van Praag, H., Kempermann, G., and Gage, F. H. (1999a). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2, 266-270.
70. van Praag, H., Christie, B. R., Sejnowski, T. J., and Gage, F. H. (1999b). Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. U.S.A. 96, 13427-13431.
71. van Praag, H., Shubert, T., Zhao, C., and Gage, F. H. (2005). Exercise enhances learning and hippocampal neuro-genesis in aged mice. J. Neurosci. 25, 8680-8685.
72. Vaynman, S., Ying, Z., and Gomez-Pinilla, F. (2003). Interplay between brain-derived neurotrophic factor and sig-nal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience 122, 647-657.
73. Vaynman, S., Ying, Z., and Gomez-Pinilla, F. (2004). Hippocampal BDNF medi-ates the efficacy of exercise on synap-tic plasticity and cognition. Eur. J. Neurosci. 20, 2580-2590.
74. Warner-Schmidt, J. L., Madsen, T. M., and Duman, R. S. (2008). Electroconvulsive seizure restores neurogenesis and hip-pocampus-dependent fear memory after disruption by irradiation. Eur. J. Neurosci. 27, 1485-1493.
75. Winocur, G., Wojtowicz, J. M., Sekeres, M., Snyder, J. S., and Wang, S. (2006). Inhibition of neurogenesis inter-feres with hippocampus-dependent memory function. Hippocampus 16, 296-304.
76. Wirth, M. J., Brun, A., Grabert, J., Patz, S., and Wahle, P. (2003). Accelerated dendritic development of rat cortical pyramidal cells and interneurons after biolistic transfection with BDNF and NT4/5. Development 130, 5827-5838.
77. Zhang, C. L., Zou, Y., He, W., Gage, F. H., and Evans, R. M. (2008). A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451, 1004-1007.
78. Zhao, C., Deng, W., and Gage, F. H. (2008). Mechanisms and functional implica-tions of adult neurogenesis. Cell 132, 645-660.
79. Zhao, C., Teng, E. M., Summers, R. G. Jr., Ming, G. L., and Gage, F. H. (2006). Distinct morphological stages of den-tate granule neuron maturation in the adult mouse hippocampus. J. Neurosci. 26, 3-11.