Exercise and the brain: Neurogenesis, synaptic plasticity, spine density, and angiogenesis

Functional Neuroimaging in Exercise and Sport Sciences

Volumn , Issue , 2012, Pages 1-24

  Wang, Zejun ^a   Van Praag, Henriette ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALS; NEURONS;

BRAIN STRUCTURE; COGNITIVE FUNCTIONS; DENDRITIC BRANCHING; LEARNING AND MEMORY; MUSCLE ACTIVATION; NEURODEGENERATION; NEURONAL MORPHOLOGY; SYNAPTIC PLASTICITY;

NEURODEGENERATIVE DISEASES;

EID: 84948741293     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-3293-7_1     Document Type: Chapter

References (155)

1. Aberg MA, Aberg ND, Hedbacker H, Oscarsson J, Eriksson PS (2000) Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J Neurosci 20:2896-2903
2. Adlard PA, Perreau VM, Pop V, Cotman CW (2005) Voluntary exercise decreases amyloid load in a transgenic model of Alzheimer’s disease. J Neurosci 25:4217-4221
3. Adlard PA, Engesser-Cesar C, Cotman CW (2011) Mild stress facilitates learning and exercise improves retention in aged mice. Exp Gerontol 46:53-59
4. Albeck DS, Sano K, Prewitt GE, Dalton L (2006) Mild forced treadmill exercise enhances spatial learning in the aged rat. Behav Brain Res 168:345-348
5. Al-Jarrah M, Pothakos K, Novikova L, Smirnova IV, Kurz MJ, Stehno-Bittel L, Lau YS (2007) Endurance exercise promotes cardiorespiratory rehabilitation without neurorestoration in the chronic mouse model of parkinsonism with severe neurodegeneration. Neuroscience 149:28-37
6. Allen DM, van Praag H, Ray J, Weaver Z, Winrow CJ, Carter TA, Braquet R, Harrington E, Ried T, Brown KD, Gage FH, Barlow C (2001) Ataxia telangiectasia mutated is essential during adult neurogenesis. Genes Dev 15:554-566
7. Allison DB, Fontaine KR, Manson JE, Stevens J, Vanltallie TB (1999) Annual deaths attributable to obesity in the United States. JAMA 282:1530-1538
8. Altman J (1962) Are new neurons formed in the brains of adult mammals? Science 135:1127-1128
9. Altschuler EL (2006) Strenuous, intensive, long-term exercise does not prevent or delay the onset of Huntington’s disease. Med Hypotheses 67:1429-1430
10. Anderson BJ, Eckburg PB, Relucio KI (2002) Alterations in the thickness of motor cortical subregions after motor-skill learning and exercise. Learn Mem 9:1-9
11. Babyak M, Blumenthal JA, Herman S, Khatri P, Doriaswamy M, Moore K, Craighead WE, Baldewicz TT, Krishnan KR (2000) Exercise treatment for major depression: maintenance of therapeutic benefit at 10 months. Psychosom Med 62:633-638
12. Barnes CA (1994) Normal aging: regionally specific changes in hippocampal synaptic transmission. Trends Neurosci 17:13-18
13. Black JE, Isaacs KR, Anderson BJ, Alcantara AA, Greenough WT (1990) Learning causes synap- togenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci USA 87:5568-5572
14. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39
15. Bohannon RW (1993) Physical rehabilitation in neurologic diseases. Curr Opin Neurol 6:765-772
16. Booth FW, Chakravarthy MV, Gordon SE, Spangenburg EE (2002) Waging war on physical inactivity: using modern molecular ammunition against an ancient enemy. J Appl Physiol 93:3-30
17. Bronzino JD, Abu-Hasaballah K, Austin-LaFrance RJ, Morgane PJ (1994) Maturation of longterm potentiation in the hippocampal dentate gyrus of the freely moving rat. Hippocampus 4:439-446
18. Brown J, Cooper-Kuhn CM, Kempermann G, van Praag H, Winkler J, Gage FH, Kuhn HG (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 17:2042-2046
19. Cao L, Jiao X, Zuzga DS, Liu Y, Fong DM, Young D, During MJ (2004) VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 36:827-835
20. Carro E, Nunez A, Busiguina S, Torres-Aleman I (2000) Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci 20:2926-2933
21. Carro E, Trejo JL, Busiguina S, Torres-Aleman I (2001) Circulating insulin-like growth factor I mediates the protective effects of physical exercise against brain insults of different etiology and anatomy. J Neurosci 21:5678-5684
22. Cepeda C, Cummings DM, Hickey MA, Kleiman-Weiner M, Chen JY, Watson JB, Levine MS (2010) Rescuing the corticostriatal synaptic disconnection in the R6/2 mouse model of Huntington’s disease: exercise, adenosine receptors and ampakines. PLoS Curr 2:RRN1182
23. Chaouloff F (1989) Physical exercise and brain monoamines: a review. Acta Physiol Scand 137:1-13
24. Chen KS, Masliah E, Mallory M, Gage FH (1995) Synaptic loss in cognitively impaired aged rats is ameliorated by chronic human growth factor infusion. Neuroscience 68:19-27
25. Choi SH, Li Y, Parada LF, Sisodia SS (2009) Regulation of hippocampal progenitor cell survival, proliferation and dendritic development by BDNF. Mol Neurodegener 4:52
26. Christie BR, Eadie BD, Kannangara TS, Robillard JM, Shin J, Titterness AK (2008) Exercising our brains: how physical activity impacts synaptic plasticity in the dentate gyrus. Neuromolecular Med 10:47-58
27. Clark PJ, Kohman RA, Miller DS, Bhattacharya TK, Brzezinska WJ, Rhodes JS (2011) Genetic influences on exercise-induced adult hippocampal neurogenesis across 12 divergent mouse strains. Genes Brain Behav 10:345-353
28. Cotman CW, Berchtold NC, Christie LA (2007) Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 30:464-472
29. Creer DJ, Romberg C, Saksida LM, van Praag H, Bussey TJ (2010) Running enhances spatial pattern separation in mice. Proc Natl Acad Sci USA 107:2367-2372
30. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon- Mom WM, Bjork-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RL, Eriksson PS (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243-1249
31. Ding Q, Vaynman S, Akhavan M, Ying Z, 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
32. Ding YH, Li J, Zhou Y, Rafols JA, Clark JC, Ding Y (2006b) Cerebral angiogenesis and expression of angiogenic factors in aging rats after exercise. Curr Neurovasc Res 3:15-23
33. Duman CH, Schlesinger L, Russell DS, Duman RS (2008) Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice. Brain Res 1199:148-158
34. Eadie BD, Redila VA, Christie BR (2005) Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation, dendritic complexity, and spine density. J Comp Neurol 486:39-47
35. Ehninger D, Kempermann G (2003) Regional effects of wheel running and environmental enrichment on cell genesis and microglia proliferation in the adult murine neocortex. Cereb Cortex 13:845-851
36. Encinas JM, Vaahtokari A, Enikolopov G (2006) Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci USA 103:8233-8238
37. Engert F, Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399:66-70
38. 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 (2011) Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA 108:3017-3022
39. 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
40. Ernst C, Olson AK, Pinel JP, Lam RW, Christie BR (2006) Antidepressant effects of exercise: evidence for an adult-neurogenesis hypothesis? J Psychiatry Neurosci 31:84-92
41. 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
42. Fabel K, Wolf SA, Ehninger D, Babu H, Leal-Galicia P, Kempermann G (2009) Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice. Front Neurosci 3:50
43. Falls WA, Fox JH, MacAulay CM (2010) Voluntary exercise improves both learning and consolidation of cued conditioned fear in C57 mice. Behav Brain Res 207:321-331
44. 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
45. Fordyce DE, Farrar RP (1991) Physical activity effects on hippocampal and parietal cortical cholinergic function and spatial learning in F344 rats. Behav Brain Res 43:115-123
46. Friedland RP, Fritsch T, Smyth KA, Koss E, Lerner AJ, Chen CH, Petot GJ, Debanne SM (2001) Patients with Alzheimer’s disease have reduced activities in midlife compared with healthy control-group members. Proc Natl Acad Sci USA 98:3440-3445
47. Ge S, Yang CH, Hsu KS, Ming GL, Song H (2007) A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54:559-566
48. Gimenez-Llort L, García Y, Buccieri K, Revilla S, Sunol C, Cristofol R, Sanfeliu C (2010) Gender-specific neuroimmunoendocrine response to treadmill exercise in 3xTg-ADMice. Int J Alzheimers Dis 2010:128354
49. Gobbo OL, O’Mara SM (2005) Exercise, but not environmental enrichment, improves learning after kainic acid-induced hippocampal neurodegeneration in association with an increase in brain-derived neurotrophic factor. Behav Brain Res 159:21-26
50. Gomez-Pinilla F (2008) Brain foods: the effects of nutrients on brain function. Nat Rev Neurosci 9:568-578
51. Gorton LM, Vuckovic MG, Vertelkina N, Petzinger GM, Jakowec MW, Wood RI (2010) Exercise effects on motor and affective behavior and catecholamine neurochemistry in the MPTP- lesioned mouse. Behav Brain Res 213:253-262
52. Gould E, Woolley CS, McEwen BS (1990) Short-term glucocorticoid manipulations affect neuronal morphology and survival in the adult dentate gyrus. Neuroscience 37:367-375
53. Grealy MA, Johnson DA, Rushton SK (1999) Improving cognitive function after brain injury: the use of exercise and virtual reality. Arch Phys Med Rehabil 80:661-667
54. Hanson ND, Nemeroff CB, Owens MJ (2011) Lithium, but not fluoxetine or the corticotropinreleasing factor receptor 1 receptor antagonist R121919, increases cell proliferation in the adult dentate gyrus. J Pharmacol Exp Ther 337:180-186
55. Hardie DG (2004) The AMP-activated protein kinase pathway - new players upstream and downstream. J Cell Sci 117:5479-5487
56. Hendriksen H, Prins J, Olivier B, Oosting RS (2010) Environmental enrichment induces behavioral recovery and enhanced hippocampal cell proliferation in an antidepressant-resistant animal model for PTSD. PLoS One 5:e11943
57. Hill MN, Titterness AK, Morrish AC, Carrier EJ, Lee TT, Gil-Mohapel J, Gorzalka BB, Hillard CJ, Christie BR (2010) Endogenous cannabinoid signaling is required for voluntary exercise-induced enhancement of progenitor cell proliferation in the hippocampus. Hippocampus 20:513-523
58. Hillman CH, Erickson KI, Kramer AF (2008) Be smart, exercise your heart: exercise effects on brain and cognition. Nat Rev Neurosci 9:58-65
59. Holmes MM, Galea LA, Mistlberger RE, Kempermann G (2004) Adult hippocampal neurogenesis and voluntary running activity: circadian and dose-dependent effects. J Neurosci Res 76:216-222
60. Hunsberger JG, Newton SS, Bennett AH, Duman CH, Russell DS, Salton SR, Duman RS (2007) Antidepressant actions of the exercise-regulated gene VGF. Nat Med 13:1476-1482
61. Isaacs KR, Anderson BJ, Alcantara AA, Black JE, Greenough WT (1992) Exercise and the brain: angiogenesis in the adult rat cerebellum after vigorous physical activity and motor skill learning. J Cereb Blood Flow Metab 12:110-119
62. Jin K, Zhu K, 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
63. Kannangara TS, Webber A, Gil-Mohapel J, Christie BR (2009) Stress differentially regulates the effects of voluntary exercise on cell proliferation in the dentate gyrus of mice. Hippocampus 19:889-897
64. Kannangara TS, Lucero MJ, Gil-Mohapel J, Drapala RJ, Simpson JM, Christie BR, van Praag H (2011) Running reduces stress and enhances cell genesis in aged mice. Neurobiol Aging 32:2279-2286
65. Kaspar BK, Frost LM, Christian L, Umapathi P, Gage FH (2005) Synergy of insulin-like growth factor-1 and exercise in amyotrophic lateral sclerosis. Ann Neurol 57:649-655
66. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495
67. Kim YP, Kim HB, Kim MH, Jang BV, Lim YJ, Kim H, Kim SS, Kim EH, Kim CJ (2003) Magnitude- and time-dependence of the effect of treadmill exercise on cell proliferation in the dentate gyrus of rats. Int J Sports Med 24:114-117
68. Kim SE, Ko IG, Kim BK, Shin MS, Cho S, Kim CJ, Kim SH, Baek SS, Lee EK, Jee YS (2010) Treadmill exercise prevents aging-induced failure of memory through an increase in neurogenesis and suppression of apoptosis in rat hippocampus. Exp Gerontol 45:357-365
69. Kitamura T, Mishina M, Sugiyama H (2003) Enhancement of neurogenesis by running wheel exercises is suppressed in mice lacking NMDA receptor epsilon 1 subunit. Neurosci Res 47:55-63
70. Kleim JA, Cooper NR, VandenBerg PM (2002) Exercise induces angiogenesis but does not alter movement representations within rat motor cortex. Brain Res 934:1-6
71. Kobilo T, Yuan C, van Praag H (2011a) Endurance factors improve hippocampal neurogenesis and spatial memory in mice. Learn Mem 18:103-107
72. Kobilo T, Liu Q, Gandhi K, Mohammed M, Shaham Y, van Praag H (2011b) Running is the neurogenic and neurotrophic stimulus in environmental enrichment. Learn Mem 18(9): 605-609
73. Kohl Z, Kandasamy M, Winner B, Aigner R, Gross C, Couillard-Despres S, Bogdahn U, Aigner L, Winkler J (2007) Physical activity fails to rescue hippocampal neurogenesis deficits in the R6/2 mouse model of Huntington’s disease. Brain Res 1155:24-33
74. Komitova M, Zhao LR, Gido G, Johansson BB, Eriksson P (2005) Postischemic exercise attenuates whereas enriched environment has certain enhancing effects on lesion-induced subventricular zone activation in the adult rat. Eur J Neurosci 21:2397-2405
75. Kosinski CM, Schlangen C, Gellerich FN, Gizatullina Z, Deschauer M, Schiefer J, Young AB, Landwehrmeyer GB, Toyka KV, Sellhaus B, Lindenberg KS (2007) Myopathy as a first symptom of Huntington’s disease in a Marathon runner. Mov Disord 22:1637-1640
76. 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
77. Kronenberg G, Bick-Sander A, Bunk E, Wolf E, Ehninger D, Kempermann G (2006) Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiol Aging 27:1505-1513
78. 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
79. Lang C, Barco A, Zablow L, Kandel ER, Siegelbaum SA, Zakharenko SS (2004) Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation. Proc Natl Acad Sci USA 101:16665-16670
80. Lange-Asschenfeldt C, Kojda G (2008) Alzheimer’s disease, cerebrovascular dysfunction and the benefits of exercise: from vessels to neurons. Exp Gerontol 43(6):499-504
81. Laurin D, Verreault R, Lindsay J, MacPherson K, Rockwood K (2001) Physical activity and risk of cognitive impairment and dementia in elderly persons. Arch Neurol 58:498-504
82. Lawlor DA, Hopker SW (2001) The effectiveness of exercise as an intervention in the management of depression: systematic review and meta-regression analysis of randomised controlled trials. BMJ 322:763-767
83. Leutgeb JK, Leutgeb S, Moser MB, Moser EI (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961-966
84. Li Y, Luikart BW, Birnbaum S, Chen J, Kwon CH, Kernie SG, Bassel-Duby R, Parada LF (2008) TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron 59:399-412
85. 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
86. Liu YF, Chen HI, Lin LC, Yu L, Liu YF, Kuo YM, Huang AM, Chuang JI, Wu FS, Liao PC, Jen CJ (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
87. Llorens-Martin M, Torres-Aleman I, Trejo JL (2006) Pronounced individual variation in the response to the stimulatory action of exercise on immature hippocampal neurons. Hippocampus 16:480-490
88. Lopez-Lopez C, LeRoith T, Torres-Aleman I (2004) Insulin-like growth factor I is required for vessel remodeling in the adult brain. Proc Natl Acad Sci USA 101:9833-9838
89. Lou SJ, Liu JY, Chang H, Chen PJ (2008) Hippocampal neurogenesis and gene expression depend on exercise intensity in juvenile rats. Brain Res 1210:48-55
90. Mahley RW, Weisgraber KH, Huang Y (2006) ApolipoproteinE4: a causative factor and therapeutic target in neuropathology, including Alzheimer’s disease. Proc Natl Acad Sci USA 103:5644-5651
91. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104-9110
92. Marlatt MW, Lucassen PJ, van Praag H (2010) Comparison of neurogenic effects of fluoxetine, duloxetine and running in mice. Brain Res 1341:93-99
93. Massa F, Koelh M, Wiesner T, Grosjean N, Revest JM, Piazza PV, Abrous DN, Oliet SH (2011) Conditional reduction of adult neurogenesis impairs bidirectional hippocampal synaptic plasticity. Proc Natl Acad Sci USA 108:6644-6649
94. McCloskey DP, Adamo DS, Anderson BJ (2001) Exercise increases metabolic capacity in the motor cortex and striatum, but not in the hippocampus. Brain Res 891:168-175
95. McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, Lowell BB, Fanselow MS, Wilson MA, Tonegawa S (2007) Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317:94-99
96. Mello PB, Benetti F, Cammarota M, Izquierdo I (2009) Physical exercise can reverse the deficit in fear memory induced by maternal deprivation. Neurobiol Learn Mem 92:364-369
97. Meshi D, Drew MR, Saxe M, Ansorge MS, David D, Santarelli L, Malapani C, Moore H, Hen R (2006) Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat Neurosci 9:729-731
98. Morton AJ, Skillings E, Bussey TJ, Saksida LM (2006) Measuring cognitive deficits in disabled mice using an automated interactive touchscreen system. Nat Methods 3:767
99. Narkar VA, Downes M, Yu RT, Embler E, Wang YX, Banayo E, Mihaylova MM, Nelson MC, Zou Y, Juguilon H, Kang H, Shaw RJ, Evans RM (2008) AMPK and PPARdelta agonists are exercise mimetics. Cell 134:405-415
100. Neeper SA, Gomez-Pinilla F, Choi J, Cotman C (1995) Exercise and brain neurotrophins. Nature 373:109
101. Nichol KE, Parachikova AI, Cotman CW (2007) Three weeks of running wheel exposure improves cognitive performance in the aged Tg2576 mouse. Behav Brain Res 184:124-132
102. Nichol K, Deeny SP, Seif J, Camaclang K, Cotman CW (2009) Exercise improves cognition and hippocampal plasticity in APOE epsilon4 mice. Alzheimers Dement 5:287-294
103. O’Callaghan RM, Ohle R, Kelly AM (2007) The effects of forced exercise on hippocampal plasticity in the rat: a comparison of LTP, spatial- and non-spatial learning. Behav Brain Res 176:362-366
104. O’Dell, SJ, Gross, NB, Fricks, AN, Casiano, BD, Nguyen, TB, Marshall, JF (2007) Running wheel exercise enhances recovery from nigrostriatal dopamine injury without inducing neuroprotection. Neuroscience 144:1141-1151
105. Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479-494
106. Pang TY, Stam NC, Nithianantharajah J, Howard ML, Hannan AJ (2006) Differential effects of voluntary physical exercise on behavioral and brain-derived neurotrophic factor expression deficits in Huntington’s disease transgenic mice. Neuroscience 141:569-584
107. Parachikova A, Nichol KE, Cotman CW (2008) Short-term exercise in aged Tg2576 mice alters neuroinflammation and improves cognition. Neurobiol Dis 30:121-129
108. Pereira AC, Huddleston DE, Brickman AM, Susonov AA, Hen R, McKhann GM, Sloan R, Gage FH, Brown TR, Small SA (2007) An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci USA 104:5638-5643
109. Persson AI, Naylor AS, Jonsottir IH, Nyberg F, Eriksson PS, Thorlin T (2004) Differential regulation of hippocampal progenitor proliferation by opioid receptor antagonists in running and non-running spontaneously hypertensive rats. Eur J Neurosci 19:1847-1855
110. Petzinger GM, Walsh JP, Akopian G, Hogg E, Abernathy A, Arevalo P, Turnquist P, Vuckovic M, Fisher BE, Togasaki DM, Jakowec MW (2007) Effects of treadmill exercise on dopaminergic transmission in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse model of basal ganglia injury. J Neurosci 27:5291-5300
111. Pothakos K, Kurz MJ, Lau YS (2009) Restorative effect of endurance exercise on behavioral deficits in the chronic mouse model of Parkinson’s disease with severe neurodegeneration. BMC Neurosci 10:6
112. Potter M, Yuan C, Ottenritter C, Mughal M, van Praag H (2010) Exercise is not beneficial and may accelerate symptom onset in a mouse model of Huntington’s disease. PLoS Curr 2:RRN1201
113. Powell KE, Blair SN (1994) The public health burdens of sedentary living habits: theoretical but realistic estimates. Med Sci Sports Exerc 26:851-856
114. Radley JJ, Jacobs BL (2002) 5-HT1A receptor antagonist administration decreases cell proliferation in the dentate gyrus. Brain Res 955:264-267
115. Redila VA, Christie BR (2006) Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus. Neuroscience 137:1299-1307
116. Rhodes JS, Hosack GR, Girard I, Kelley AE, Mitchell GS, Garland T Jr (2001) Differential sensitivity to acute administration of cocaine, GBR 12909, & fluoxetine in mice selectively bred for hyperactive wheel-running behavior. Psychopharmacology 158:120-131
117. Rhodes JS, van Praag H, Jeffrey S, Girard I, Mitchell GS, Garland T Jr, Gage FH (2003) Exercise increases hippocampal neurogenesis to high levels but does not improve spatial learning in mice bred for increased voluntary wheel running. Behav Neurosci 117:1006-1016
118. Rogers RL, Meyer JS, Mortel KF (1990) After reaching retirement age physical activity sustains cerebral perfusion and cognition. J Am Geriatr Soc 38:123-128
119. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805-809
120. Schmidt-Hieber C, Jonas P, Bischofberger J (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184-187
121. Sforzo GA, Seeger TF, Pert CB, Pert A, Dotson CO (1986) In vivo opioid receptor occupation in the rat brain following exercise. Med Sci Sports Exerc 18:380-384
122. Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S (2004) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338-1340
123. Smith AD, Zigmond MJ (2003) Can the brain be protected through exercise? Lessons from an animal model of parkinsonism. Exp Neurol 184:31-39
124. Steinmetz KA, Potter JD (1996) Vegetables, fruit, and cancer prevention: a review. J Am Diet Assoc 96:1027-1039
125. Stranahan AM, Khalil D, Gould E (2007) Running induces widespread structural alterations in the hippocampus and entorhinal cortex. Hippocampus 17:1017-1022
126. Stummer W, Weber K, Tranmer B, Baethmann A, Kempski O (1994) Reduced mortality and brain damage after locomotor activity in gerbil forebrain ischemia. Stroke 25:1862-1869
127. Suominen-Troyer S, Davis KJ, Ismail AH, Salvendy G (1986) Impact of physical fitness on strategy development in decision-making tasks. Percept Mot Skills 62:71-77
128. Suwa M, Nakano H, Radak Z, Kumagai S (2011) Short-term adenosine monophosphate-activated protein kinase activator 5-aminoimidazole-4-carboxamide-1-beta-d-ribofuranoside treatment increases the sirtuin 1 protein expression in skeletal muscle. Metabolism 60:394-403
129. Swain RA, Harris AB, Wiener EC, Dutka MV, Morris HD, Theien BE, Konda S, Engberg K, Lauterbur PC, Greenough WT (2003) Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 117:1037-1046
130. Tajiri N, Yasuhara T, Shingo T, Kondo A, Yuan W, Kadota T, Wang F, Baba T, Tayra JT, Morimoto T, Jing M, Kikuchi Y, Kuramoto S, Agari T, Miyoshi Y, Fujino H, Obata F, Takeda I, Furuta T, Date I (2010) Exercise exerts neuroprotective effects on Parkinson’s disease model of rats. Brain Res 1310:200-207
131. Thored P, Wood J, Arvidsson A, Cammenga J, Kokaia Z, Lindvall O (2007) Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke. Stroke 38:3032-3039
132. Tillerson JL, Caudle WM, Reveron ME, Miller GW (2003) Exercise induces behavioral recovery and attenuates neurochemical deficits in rodent models of Parkinson’s disease. Neuroscience 119:899-911
133. Trejo JL, Carro E, Torres-Aleman 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
134. Uda M, Ishido M, Kami K, Masuhara M (2006) Effects of chronic treadmill running on neurogenesis in the dentate gyrus of the hippocampus of adult rat. Brain Res 1104:64-72
135. Um HS, Kang EB, Koo JH, Kim HT, Jin-Lee, Kim EJ, Yang CH, An GY, Cho IH, Cho JY (2011) Treadmill exercise represses neuronal cell death in an aged transgenic mouse model of Alzheimer’s disease. Neurosci Res 69:161-173
136. van Dellen A, Blakemore C, Deacon R, York D, Hannan AJ (2000) Delaying the onset of Huntington’s in mice. Nature 404:721-722
137. van Dellen A, Cordery PM, Spires TL, Blakemore C, Hannan AJ (2008) Wheel running from a juvenile age delays onset of specific motor deficits but does not alter protein aggregate density in a mouse model of Huntington’s disease. BMC Neurosci 9:34
138. van der Borght K, Ferrari F, Klauke K, Roman V, Havekes R, Sgoifo A, van der Zee EA, Meerlo P (2006)Hippocampal cell proliferation across the day: increase by running wheel activity, but no effect of sleep and wakefulness. Behav Brain Res 167:36-41
139. van der Borght K, Havekes R, Bos T, Eggen BJ, van der Zee EA (2007) Exercise improves memory acquisition and retrieval in the Y-maze task: relationship with hippocampal neurogenesis. Behav Neurosci 121:324-334
140. van der Borght K, Kobor-Nyakas DE, Klauke K, Eggen BJ, Nyakas C, van der Zee EA, Meerlo P (2009) Physical exercise leads to rapid adaptations in hippocampal vasculature: temporal dynamics and relationship to cell proliferation and neurogenesis. Hippocampus 19:928-936
141. van Praag H (2008) Neurogenesis and exercise: past and future directions. Neuromolecular Med 10:128-140
142. 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
143. 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
144. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034
145. van Praag H, Shubert T, Zhao C, Gage FH (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25:8680-8685
146. van Praag H, Lucero MJ, Yeo GW, Stecker K, Heivand N, Zhao C, Yip E, Afandor M, Schroeter H, Hammerstone J, Gage FH (2007) Plant-derived flavanol (-)epicatechin enhances angiogenesis and retention of spatial memory in mice. J Neurosci 27:5869-5878
147. VanLeeuwen JE, Petzinger GM, Walsh JP, Akopian GK, Vuckovic M, Jakowec MW (2010) Altered AMPA receptor expression with treadmill exercise in the 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine-lesioned mouse model of basal ganglia injury. J Neurosci Res 88:650-668
148. Vasuta C, Caunt C, James R, Samadi S, Schibuk E, Kannangara T, Titterness AK, Christie BR (2007) Effects of exercise on NMDA receptor subunit contributions to bidirectional synaptic plasticity in the mouse dentate gyrus. Hippocampus 17:1201-1208
149. Voss MW, Nagamatsu LS, Liu-Ambrose T, Kramer AF (2011) Exercise, brain, and cognition across the lifespan. J Appl Physiol. doi:10.1152/japplphysiol.00210.2011
150. Wang S, Scott BW, Wojtowicz JM (2000) Heterogenous properties of dentate granule neurons in the adult rat. J Neurobiol 42:248-257
151. Wang YX, Zhang CL, Yu RT, Cho HK, Nelson MC, Bayuga-Ocampo CR, Ham J, Kang H, Evans RM (2004) Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol 2:e294
152. Yoon MC, Shin MS, Kim TS, Kim BK, Ko IG, Sung YH, Kim SE, Lee HH, Kim YP, Kim CJ (2007) Treadmill exercise suppresses nigrostriatal dopaminergic neuronal loss in 6-hydroxydo- pamine-induced Parkinson’s rats. Neurosci Lett 423:12-17
153. Zhao C, Teng EM, Summers RG Jr, Ming GL, Gage FH (2006) Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26:3-11
154. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645-660
155. Zhou Q, Homma KJ, Poo MM (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749-757