Exercise enhances learning and hippocampal neurogenesis in aged mice

Journal of Neuroscience

Volumn 25, Issue 38, 2005, Pages 8680-8685

  Van Praag, Henriette ^a   Shubert, Tiffany ^a   Zhao, Chunmei ^a   Gage, Fred H ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Aging; Angiogenesis; Exercise; Learning; Neurogenesis; Spines

Indexed keywords

BROXURIDINE;

AGING; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; EXERCISE; HIPPOCAMPUS; LEARNING; MALE; MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RUNNING; SYNAPTIC TRANSMISSION; TREADMILL EXERCISE;

AGING; ANIMALS; CELL DIFFERENTIATION; HIPPOCAMPUS; LEARNING; MICE; MICE, INBRED C57BL; NEURONS; PHYSICAL CONDITIONING, ANIMAL;

EID: 25444533023     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1731-05.2005     Document Type: Article

References (48)

1. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335.
2. Anderson BJ, Rapp DN, Baek DH, McCloskey DP, Coburn-Litvak PS, Robinson JK (2000) Exercise influences spatial learning in the radial arm maze. Physiol Behav 70:425-429.
3. Barnes CA, Forster MJ, Fleshner M, Ahanotu EN, Laudenslager ML, Mazzeo RS, Maier SF, Lal H (1991) Exercise does not modify spatial memory, brain autoimmunity, or antibody response in aged F-344 rats. Neurobiol Aging 12:47-53.
4. Barnes CA (1994) Normal aging: regionally specific changes in hippocampal synaptic transmission. Trends Neurosci 17:13-18.
5. Bizon JL, Lee HJ, Gallagher M (2004) Neurogenesis in a rat model of age-related cognitive decline. Aging Cell 3:227-234.
6. Black JE, Polinsky M, Greenough WT (1989) Progressive failure of cerebral angiogenesis supporting neural plasticity in aging rats. Neurobiol Aging 10:353-358.
7. Black JE, Isaacs KR, Anderson BJ, Alcantara AA, Greenough WT (1990) Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci USA 87:5568-5572.
8. Burns EM, Kruckeberg TW, Gaetano PK (1981) Changes with age in cerebral capillary morphology. Neurobiol Aging 2:283-291.
9. Cameron HA, McKay RD (1999) Restoring production of hippocampal neurons in old age. Nat Neurosci 10:894-897.
10. Colcombe SJ, Erickson KI, Raz N, Webb AG, Cohen NJ, McAuley E, Kramer AF (2003) Aerobic fitness reduces brain tissue loss in aging humans. J Gerontol A Biol Sci Med Sci 58:M176-M180.
11. Cotman CW, Berchtold NC (2002) Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25:295-301.
12. Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN (2003) Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci USA 100:14385-14390.
13. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
14. Fabel K, Fabel K, Tam B, Kaufer D, Baiker A, Simmons N, Kuo CJ, Palmer TD (2003) VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 18:2803-2812.
15. Farmer J, Zhao X, van Praag H, Wodtke K, Gage FH, Christie BR (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.
16. Fordyce DE, Farrar RP (1991) Enhancement of spatial learning in F344 rats by physical activity and related learning-associated alterations in hippocampal and cortical cholinergic functioning. Behav Brain Res 46:123-133.
17. Gage FH, Kelly PA, Bjorklund A (1984) Regional changes in brain glucose metabolism reflect cognitive impairments in aged rats. J Neurosci 4:2856-2866.
18. Geinisman Y, de Toledo-Morrell L, Morrell F, Persina IS, Rossi M (1992) Age-related loss of axospinous synapses formed by two afferent systems in the rat dentate gyrus as revealed by the unbiased stereological dissector technique. Hippocampus 2:437-444.
19. Heine VM, Maslam S, Joels M, Lucassen PJ (2004) Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol Aging 25:361-375.
20. Jarrard LE (1995) What does the hippocampus really do? Behav Brain Res 71:1-10.
21. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA (2002) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA 99:11946-11950.
22. Jin K, Sun Y, Xie L, Batteur S, Mao XO, Smelick C, Logvinova A, Greenberg DA (2003) Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2:175-183.
23. Kempermann G, Kuhn HG, Gage FH (1998) Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18:3206-3212.
24. Kempermann G, Gast D, Gage FH (2002) Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52:135-143.
25. Kim YP, Kim H, Shin MS, Chang HK, Jang MH, Shin MC, Lee SJ, Lee HH, Yoon JH, Jeong IG, Kim CJ (2004) Age-dependence of the effect of treadmill exercise on cell proliferation in the dentate gyrus of rats. Neurosci Lett 355:152-154.
26. Kramer AF, Hahn S, Cohen NJ, Banich MT, McAuley E, Harrison CR, Chason J, Vakil E, Bardell L, Boileau RA, Colcombe A (1999) Ageing, fitness and neurocognitive function. Nature 400:418-419.
27. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
28. Lemaire V, Koehl M, Le Moal M, Abrous DN (2000) Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 97:11032-11037.
29. Lichtenwalner R, Forbes M, Bennett S, Lynch C, Sonntag W, Riddle D (2001) Intracerebroventricular infusion of insulin-like growth factor-1 ameliorates the age-related decline in hippocampal neurogenesis. Neuroscience 107:606-613.
30. Lopez-Lopez C, LeRoith D, Torres-Aleman I (2004) Insulin-like growth factor I is required for vessel remodeling in the adult brain. Proc Natl Acad Sci USA 101:9833-9888.
31. Merrill DA, Karim R, Darraq M, Chiba AA, Tuszynski MH (2003) Hippocampal cell genesis does not correlate with spatial learning ability in aged rats. J Comp Neurol 459:201-207.
32. Morris RG, Garrud P, Rawlins JN, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
33. Palmer TD, Willhoite A, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479-494.
34. Rao MS, Hattiangady B, Abdel-Rahman A, Stanley DP, Shetty AK (2005) Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur J Neurosci 21:464-476.
35. Rowlatt C, Chesterman FC, Sheriff MU (1976) Lifespan, age changes and tumour incidence in an ageing C57BL mouse colony. Lab Anim 10:419-442.
36. Samorajski T, Delaney C, Durham L, Ordy JM, Johnson JA, Dunlap WP (1985) Effect of exercise on longevity, body weight, locomotor performance, and passive-avoidance memory of C57BL/6J mice. Neurobiol Aging 6:17-24.
37. Shetty AK, Hattiangady B, Shetty GA (2005) Stem/progenitor cell proliferation factors FGF-2, IGF-1, and VEGF exhibit early decline during the course of aging in the hippocampus: role of astrocytes. Glia 51:173-186.
38. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-376.
39. Small SA, Tsai WY, DeLaPaz R, Mayeux R, Stern Y (2002) Imaging hippocampal function across the human life span: is memory decline normal or not? Ann Neurol 51:290-295.
40. Smith TD, Adams MM, Gallagher M, Morrison JH, Rapp PR (2000) Circuit-specific alterations in hippocampal synaptophysin immunoreactivity predict spatial learning impairment in aged rats. J Neurosci 20:6587-6593.
41. Sonntag WE, Lynch CD, Cooney PT, Hutchins PM (1997) Decreases in cerebral microvasculature with age are associated with the decline in growth hormone and insulin-like growth factor 1. Endocrinology 138:3515-3520.
42. Swain RA, Harris AB, Wiener EC, Dutka MV, Morris HD, Theien BE, Konda S, Engberg K, Lauterbur PC, Greenough WT (2003) (2003) Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 117:1037-1046.
43. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999a) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96:13427-13431.
44. van Praag H, Kempermann G, Gage FH (1999b) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270.
45. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
46. Vaynman S, Ying Z, Gomez-Pinilla F (2004) Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur. J Neurosci 20:2580-2590.
47. West MJ (1993) Regionally specific loss of neurons in the aging human hippocampus. Neurobiol Aging 14:287-293.
48. Yaffe K, Barnes D, Nevitt M, Lui LY, Covinsky K (2001) A prospective study of physical activity and cognitive decline in elderly women: women who walk. Arch Intern Med 161:1703-1708.