Effects of aerobic exercise training on cognitive function and cortical vascularity in monkeys

Neuroscience

Volumn 167, Issue 4, 2010, Pages 1239-1248

  Rhyu, I J ^a   Bytheway, J A ^b,c   Kohler, S J ^d   Lange, H ^b   Lee, K J ^a   Boklewski, J ^d   McCormick, K ^b   Williams, N I ^e   Stanton, G B ^d   Greenough, W T ^d   Cameron, J L ^b,f  

^a Korea University College of Medicine   (South Korea)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^e PENNSYLVANIA STATE UNIVERSITY   (United States)

^f OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Blood flow; Discrimination; Learning; Motor cortex; Primate; Spatial cognition

Indexed keywords

AEROBIC EXERCISE; AGE DISTRIBUTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD VESSEL; BRAIN BLOOD VOLUME; COGNITION; CONTROLLED STUDY; FEMALE; FITNESS; MENTAL FUNCTION; MONKEY; MOTOR CORTEX; NONHUMAN; PRIORITY JOURNAL; RUNNING; SITTING; TREADMILL EXERCISE;

AGE FACTORS; ANIMALS; COGNITION; FEMALE; LEARNING; MACACA FASCICULARIS; MOTOR CORTEX; PHYSICAL CONDITIONING, ANIMAL;

EID: 77952552221     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.03.003     Document Type: Article

References (64)

1. Abernethy W.B., Bell M.A., Morris M Moody D.M. Microvascular density of the human paraventricular nucleus decreases with aging but not hypertension. Exp Neurol 1993, 121:270-274.
2. Albelda S.M., Oliver P.D., Romer L.H., Buck C.A. EndoCAM: a novel endothelial cell-cell adhesion molecule. J Cell Biol 1990, 110:1227-1237.
3. Albelda S.M., Muller W.A., Buck C.A., Newman P.J. Molecular and cellular properties of PECAM-1 (endoCAM/CD31): a novel vascular cell-cell adhesion molecule. J Cell Biol 1991, 114:1059-1068.
4. Anderson B.J., Rapp D.N., Baek D.H., McCloskey D.P., Coburn-Litvak P.S., Robinson J.K. Exercise influences spatial learning in the radial arm maze. Physiol Behav 2000, 70:425-429.
5. Balady G.J., Weiner D.A. Exercise testing for sports and the exercise prescription. Cardiol Clin 1987, 5:183-196.
6. Barnes C.A., Forster M.J., Fleshner M., Ahanotu E.N., Laudenslager M.L., Mazzeo R.S., Maier S.F., Lal H. Exercise does not modify spatial memory, brain autoimmunity, or antibody response in aged F344 rats. Neurobiol Aging 1991, 12:47-53.
7. Bherer L., Kramer A.F., Peterson M.S., Colcombe S., Erickson K., Becic E. Transfer effects in task-set cost and dual-task cost after dual-task training in older and younger adults: further evidence for cognitive plasticity in attentional control in late adulthood. Exp Aging Res 2008, 34:188-219.
8. Black J.E., Isaacs K.R., Anderson B.J., Alcantara A.A., Greenough W.T. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebeller cortex of adult rats. Proc Natl Acad Sci U S A 1990, 87:5568-5572.
9. Brooks G.A. Lactate production under fully aerobic conditions: the lactate shuttle during rest and exercise. Fed Proc 1986, 45:2924-2929.
10. Carro E., Nunez A., Busiguina S., Torres-Aleman I. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci 2000, 20:2926-2933.
11. Chen H., Zhang S.M., Schwarzschild M.A., Hernan M.A., Ascherio A. Physical activity and the risk of Parkinson disease. Neurology 2005, 64:664-669.
12. Clifton D.K., Bremner W.J., Steiner R.A. An automated technique for the radiographic determination of bone age. J Med Primatol 1982, 11:147-154.
13. Colcombe S.J., Erickson K.I., Raz N., Webb A.G., Cohen N.J., McAuley E., Kramer A.F. Aerobic fitness reduces brain tissue loss in aging humans. J Gerontol A Biol Sci Med Sci 2003, 58:176.v-180.v.
14. Colcombe S.J., Erickson S.I., Scalf P.E., Kim J.S., Prakash R., McAuley E., Elavsky S., Marquez D.X., Hu L., Kramer A.F. Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci 2006, 61:1166-1170.
15. Colcombe S., Kramer A.F. Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol Sci 2003, 14:125-130.
16. Colcombe S.J., Kramer A.F., Erickson K.I., Scalf P., McAuley E., Cohen N.J., Webb A., Jerome G.J., Marquez D.X., Elavsky S. Cardiovascular fitness, cortical plasticity, and aging. Proc Natl Acad Sci U S A 2004, 101:3316-3321.
17. Cotman C.W., Berchtold N.C. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 2002, 25:295-301.
18. Cotman C.W., Berchtold N.C., Christie L.A. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 2007, 30:464-472.
19. Ding Y., Li J., Luan X., Ding Y.H., Lai Q., Rafols J.A., Phillis J.W., Clark J.C., Diaz F.G. Exercise pre-conditioning reduces brain damage in ischemic rats that may be associated with regional angiogenesis and cellular overexpression of neurotrophin. Neuroscience 2004, 124:583-591.
20. Ding Y.H., Li J., Zhou Y., Rafols J.A., Clark J.C., Ding Y. Cerebral angiogenesis and expression of angiogenic factors in aging rats after exercise. Curr Neurovasc Res 2006, 3:15-23.
21. Ding Y.H., Luan X.D., Li J., Rafols J.A., Guthinkonda M., Diaz F.G., Ding Y. Exercise-induced overexpression of angiogenic factors and reduction of ischemia/reperfusion injury in stroke. Curr Neurovasc Res 2004, 1:411-420.
22. Dishman R.K., Berthoud H.R., Booth F.W., Cotman C.W., Edgerton V.R., Fleshner M.R., Gandevia S.C., Gomez-Pinilla F., Greenwood B.N., Hillman C.H., Kramer A.F., Levin B.E., Moran T.H., Russo-Neustadt A.A., Salamone J.D., Van Hoomissen J.D., Wade C.E., York D.A., Zigmond M.J. Neurobiology of exercise. Obesity (Silver Spring) 2006, 14:345-356.
23. Etnier J.L., Berry M. Fluid intelligence in an older COPD sample after short- and long-term exercise. Med Sci Sports Exerc 2001, 33:1620-1628.
24. Farkas E., Luiten P.G. Cerebral microvascular pathology in aging and Alzheimer's disease. Prog Neurobiol 2001, 64:575-611.
25. Fillit H.M., Butler R.N., O'Connell A.W., Albert M.S., Birren J.E., Cotman C.W., Greenough W.T., Gold P.E., Kramer A.F., Kuller L.H., Perls T.T., Shagan B.G., Tully T. Achieving and maintaining cognitive vitality with aging. Mayo Clin Proc 2002, 77:681-696.
26. Fordyce D.E., Farrar R.P. Physical activity effects on hippocampal and parietal cortical cholinergic function and spatial learning in F344 rats. Behav Brain Res 1991, 43:115-123.
27. Fordyce D.E., Wehner J.M. Physical activity enhances spatial learning performance with an associated alteration in hippocampal protein kinase C activity in C57BL/6 and DBA/2 mice. Brain Res 1993, 619:111-119.
28. Gomez-Pinilla F., Dao L., So V. Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Res 1997, 764:1-8.
29. Gordon B.A., Rykhlevskaia E.I., Brumback C.R., Lee Y., Elavsky S., Konopack J.F., McAuley E., Kramer A.F., Colcombe S., Gratton G., Fabiani M. Neuroanatomical correlates of aging, cardiopulmonary fitness level, and education. Psychophysiology 2008, 45:825-838.
30. Griesback G.S., Hoyda D.A., Comez-Pinilla F. Exercise-induced improvement in cognitive performance after traumatic brain injury in rats is dependent on BDNS activation. Brain Res 2009, 1288:105-115.
31. Gundersen H.J., Bendtsen T.F., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., West M.J. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 1988, 96:379-394.
32. Hamer M., Chida Y. Physical activity and risk of neurodegenerative disease: a ystematic review of prospective evidence. Psychol Med 2009, 39:3-11.
33. Haskell W.L., Lee I.M., Pate R.R., Powell K.E., Blair S.N., Franklin B.A., Macera C.A., Heath G.W., Thompson P.D., Bauman A. Physical activity and public health: updated recommendation for adults from the American College of sports medicine and the American Heart Association. Med Sci Sports Exerc 2007, 39:1423-1434.
34. Khatri P., Blumenthal J.A., Babyak M.A., Craighead W.E., Herman S., Baldewicz T., Madden D.J., Doraiswamy M., Waugh R., Krishnan K.R. Effects of exercise training on cognitive functioning among depressed older men and women. J Aging Phys Activ 2001, 9:43-57.
35. Kleim J.A., Cooper N.R., VandenBerg P.M. Exercise induces angiogenesis but does not alter movement representations within rat motor cortex. Brain Res 2002, 934:1-6.
36. Klintsova A.Y., Dickson E., Yoshida R., Greenough W.T. Altered expression of BDNF and its high-affinity receptor TrkB in response to complex motor learning and moderate exercise. Brain Res 2004, 1028:92-104.
37. Kohler S.J., Jennings V., Todd S.V., Rhyu I., Williams N.I., Cameron J., Greenough W.T. Exercise increases capillary volume in the neostriatum of macaque monkeys 2007, Society for Neuroscience, San Diego, CA, Program No. 589.11 [online].
38. Kohler S.J., Boklewski J.L., Stanton G.B., Kleczek A.S., Jennings V.L., Cameron J.L., Greenough W.T. Characterization of adult born cells in the precentral gyrus of nonhuman primates 2009, Society for Neuroscience, Chicago, IL, Program No. 308.20 [online].
39. Leggio M.G., Mandolesi L., Federico F., Spirito F., Ricci B., Gelfo F., Petrosini L. Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res 2005, 163:78-90.
40. Llorens-Martin M., Torres-Aleman I., Trejo J.L. Mechanism mediating brain plasticity: IGF1 and adult hippocampal neurogenesis. Neuroscientist 2009, 15:134-148.
41. Martin R.F., Bowden D.M. Primate brain maps: structure of the macaque brain 2000, Elsevier, Amsterdam.
42. Meunier M., Bachevalier J., Mishkin M. Effects of orbital frontal and anterior cingulate lesions on object and spatial memory in rhesus monkeys. Neuropsychology 1996, 35:999-1015.
43. Miller R.G. Nonparametric techniques in simultaneous statistical inference 1981, 129-188. Springer-Verlag, New York. 2nd ed.
44. Neeper S.A., Gomez-Pinilla F., Choi J., Cotman C. Exercise and brain neurotrophins. Nature 1995, 373:109.
45. Podewils L.H., Guallar E., Kuller L.H., Fried L.P., Lopez O.L., Carlson M., Lyketsos C.G. Physical activity, APOE genotype, and dementia risk: findings from the cardiovascular health cognition study. Am J Epidemiol 2005, 161:639-651.
46. Radak Z., Kaneko T., Tahara S., Nakamoto H., Pucsok J., Sasvari M., Nyakas C., Goto S. Regular exercise improves cognitive function and decreases oxidative damage in rat brain. Neurochem Int 2001, 38:17-23.
47. Rhodes J.S., Van Praag H., Jeffrey S., Girard I., Mitchell G.S., Garland T., Gage F. Exercise increases hippocampal neurogenesis to high levels but does not improve spatial learning in mice bred for increased voluntary wheel running. Behav Neurosci 2003, 117(5):1006-1016.
48. Rolland Y., Pillard F., Klapouszczak A., Reynish E., Thomas D., Andrieu S., Riviere D., Vellas B. Exercise program for nursing home residents with Alzheimer's disease: a 1-year randomized, controlled trial. J Am Geriatr Soc 2007, 55:158-165.
49. Ruscheweyh R, Willemer C, Kruger K, Duning T, Warnecke T, Sommer J, Volker K, Ho HV, Mooren F, Knecht S, Floel A (in press) Physical activity and memory functions: an interventional study. Neurobiol Aging, in press.
50. Sasco A.J., Paffenbarger R.S., Gendre I., Wing A.L. The role of physical exercise in the occurrence of Parkinson's disease. Arch Neurol 1992, 49:360-365.
51. Scarmeas N., Luchsinger J.A., Schupf N., Brickman A.M., Cosentino S., Tang M.X., Stern Y. Physical activity, diet, and risk of Alzheimer disease. JAMA 2009, 302:627-637.
52. Sonntag W.E., Lynch C.D., Cooney P.T., Hutchins P.M. Decreases in cerebral microvasculature with age are associated with the decline in growth hormone and insulin-like growth factor 1. Endocrinology 1997, 138:3515-3520.
53. Swain R.A., Harris A.B., Wiener E.C., Dutka M.V., Morris H.D., Theien B.E., Konda S., Eckberg K., Lauterbur P.C., Greenough W.T. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 2003, 117:1037-1046.
54. Swindler D.R. Nonhuman primate dental development and its relationship to human dental development. Nonhuman primate models for human growth and development 1985, 67-94. Alan R. Liss, Inc, New York. E.S. Watts (Ed.).
55. Teri L., Gibbons L.E., McCurry S.M., Logsdon R.G., Buchner D.M., Barlow W.E., Kukull W.A., LaCroix A.Z., McCormick W., Larson E.B. Exercise plus behavioral management in patients with Alzheimer disease: a randomized controlled trail. JAMA 2003, 290:2015-2022.
56. Uranishi R., Awadallah N.A., Ogunshola O.O., Awad I.A. Further study of CD 31 protein and messenger ribonucleic acid expression in human cerebral vascular malformations. Neurosurgery 2002, 50:110-116.
57. Uranishi R., Baev N.I., Ng P.Y., Kim J.H., Awad I.A. Expression of endothelial cell angiogenesis receptors in human cerebrovascular malformations. Neurosurgery 2001, 48:359-367.
58. Van Boxtel M.P., Paas F.G., Houx P.J., Adam J.J., Teeken J.C., Jolles J. Aerobic capacity and cognitive performance in a cross-sectional aging study. Med Sci Sports Exerc 1997, 29:1357-1365.
59. Van Praag H., Christie B.R., Sejnowski T.J., Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 1999, 96:13427-13431.
60. Van Praag H., Shubert T., Zhao C., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 2005, 25:8680-8685.
61. Vaynman S., Ying Z., Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 2004, 20:2580-2590.
62. Williams N.I., Berga S.L., Cameron J.L. Synergism between psychosocial and metabolic stressors: impact on reproductive function in cynomolgus monkeys. Am J Physiol Endocrinol Metab 2007, 293:270-276.
63. Williams N.I., Caston-Balderrama A.L., Helmreich D.L., Parfitt D.B., Nosbisch C., Cameron J.L. Induction of menstrual cycle disturbances in cynomolgus monkeys during strenuous exercise training: longitudinal changes in reproductive hormones and menstrual cyclicity. Endocrinology 2001, 142:2381-2389.
64. Williams N.I., Caston-Balderrama A.L., Helmreich D.L., Parfitt D.B., Cameron J.L. Induction of menstrual cycle disturbances in cynomolgus monkeys during strenuous exercise training: evidence for a causal role of low energy availability. J Clin Endocrinol Metab 2001, 86:5184-5193.