Long-term mild exercise training enhances hippocampus-dependent memory in rats

International Journal of Sports Medicine

Volumn 36, Issue 4, 2015, Pages 280-285

  Inoue, K ^a,b   Hanaoka, Y ^a   Nishijima, T ^a   Okamoto, M ^a   Chang, H ^a,c   Saito, T ^a   Soya, H ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b HEALTH SCIENCES UNIVERSITY OF HOKKAIDO   (Japan)

^c Shizuoka University of Welfare   (Japan)

Author keywords

exercise intensity; hippocampal function; lactate threshold; Morris water maze; stress

Indexed keywords

CORTICOSTERONE; LACTIC ACID;

ANIMAL; ANIMAL EXPERIMENT; BLOOD; COGNITION; HIPPOCAMPUS; MALE; MAZE TEST; MEMORY; MENTAL STRESS; PHYSIOLOGY; SKELETAL MUSCLE; WISTAR RAT;

ANIMALS; COGNITION; CORTICOSTERONE; HIPPOCAMPUS; LACTIC ACID; MALE; MAZE LEARNING; MEMORY; MUSCLE, SKELETAL; PHYSICAL CONDITIONING, ANIMAL; RATS, WISTAR; STRESS, PSYCHOLOGICAL;

EID: 84925866263     PISSN: 01724622     EISSN: 14393964     Source Type: Journal    
DOI: 10.1055/s-0034-1390465     Document Type: Article

References (42)

1. Aguiar A. S. Jr, Boemer G., Rial D., Cordova F. M., Mancini G., Walz R., de Bem A. F., Latini A., Leal R. B., Pinho R. A., Prediger R. D. High-intensity physical exercise disrupts implicit memory in mice: involvement of the striatal glutathione antioxidant system and intracellular signaling. Neuroscience: 2010; 171 1216 1227
2. Alaei H., Moloudi R., Sarkaki A. R. Effects of treadmill running on mid-term memory and swim speed in the rat with Morris water maze test. J Bodyw Mov Ther: 2008; 12 72 75
3. Ang E. T., Dawe G. S., Wong P. T., Moochhala S., Ng Y. K. Alterations in spatial learning and memory after forced exercise. Brain Res: 2006; 1113 186 193
4. Clark P. J., Brzezinska W. J., Thomas M. W., Ryzhenko N. A., Toshkov S. A., Rhodes J. S. Intact neurogenesis is required for benefits of exercise on spatial memory but not motor performance or contextual fear conditioning in C57BL/6J mice. Neuroscience: 2008; 155 1048 1058
5. Conrad C. D. A critical review of chronic stress effects on spatial learning and memory. Prog Neuropsychopharmacol Biol Psychiatry: 2010; 34 742 755
6. 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
7. Duan X., Kang E., Liu C. Y., Ming G. L., Song H. Development of neural stem cell in the adult brain. Curr Opin Neurobiol: 2008; 18 108 115
8. Erickson K. I., Voss M. W., Prakash R. S., Basak C., Szabo A., Chaddock L., Kim J. S., Heo S., Alves H., White S. M., Wojcicki T. R., Mailey E., Vieira V. J., Martin S. A., Pence B. D., Woods J. A., McAuley E., Kramer A. F. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA: 2011; 108 3017 3022
9. Fabel K., Fabel K., Tam B., Kaufer D., Baiker A., Simmons N., Kuo C. J., Palmer T. D. VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci: 2003; 18 2803 2812
10. Fordyce D. E., Farrar R. P. Enhancement of spatial learning in F344 rats by physical activity and related learning-associated alterations in hippocampal and cortical cholinergic functioning. Behav Brain Res: 1991; 46 123 133
11. Ge S. Y., Sailor K. A., Ming G. L., Song H. J. Synaptic integration and plasticity of new neurons in the adult hippocampus. J Physiol: 2008; 586 3759 3765
12. Harriss D. J., Atkinson G. Ethical standards in sport and exercise science research: 2014 update. Int J Sports Med: 2013; 34 1025 1028
13. Hoveida R., Alaei H., Oryan S., Parivar K., Reisi P. Treadmill running improves spatial memory in an animal model of Alzheimer's disease. Behav Brain Res: 2011; 216 270 274
14. Hyodo K., Dan I., Suwabe K., Kyutoku Y., Yamada Y., Akahori M., Byun K., Kato M., Soya H. Acute moderate exercise enhances compensatory brain activation in older adults. Neurobiol Aging: 2012; 33 2621 2632
15. Joels M., Krugers H., Karst H. Stress-induced changes in hippocampal function. Prog Brain Res: 2008; 167 3 15
16. Kamijo K., Nishihira Y., Higashiura T., Kuroiwa K. The interactive effect of exercise intensity and task difficulty on human cognitive processing. Int J Psychophysiol: 2007; 65 114 121
17. Kawashima H., Saito T., Yoshizato H., Fujikawa T., Sato Y., McEwen B. S., Soya H. Endurance treadmill training in rats alters CRH activity in the hypothalamic paraventricular nucleus at rest and during acute running according to its period. Life Sci: 2004; 76 763 774
18. Kim Y. P., Kim H. B., Jang M. H., Lim B. V., Kim Y. J., Kim H., Kim S. S., Kim E. H., Kim C. J. Magnitude- and time-dependence of the effect of treadmill exercise on cell proliferation in the dentate gyrus of rats. Int J Sports Med: 2003; 24 114 117
19. Marlatt M. W., Potter M. C., Lucassen P. J., van Praag H. Running throughout middle-age improves memory function, hippocampal neurogenesis, and BDNF levels in female C57BL/6J mice. Dev Neurobiol: 2012; 72 943 952
20. Mirescu C., Gould E. Stress and adult neurogenesis. Hippocampus: 2006; 16 233 238
21. Naylor A. S., Persson A. I., Eriksson P. S., Jonsdottir I. H., Thorlin T. Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat. J Neurophysiol: 2005; 93 2406 2414
22. Nishijima T., Soya H. Evidence of functional hyperemia in the rat hippocampus during mild treadmill running. Neurosci Res: 2006; 54 186 191
23. Okamoto M., Hojo Y., Inoue K., Matsui T., Kawato S., McEwen B. S., Soya H. Mild exercise increases dihydrotestosterone in hippocampus providing evidence for androgenic mediation of neurogenesis. Proc Natl Acad Sci USA: 2012; 109 13100 13105
24. Rhodes J. S., van Praag H., Jeffrey S., Girard I., Mitchell G. S., Garland T. Jr, Gage F. H. 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 1006 1016
25. Rothman S. M., Mattson M. P. Adverse stress, hippocampal networks, and Alzheimer's disease. Neuromolecular Med: 2010; 12 56 70
26. Schena M., Shalon D., Davis R. W., Brown P. O. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science: 1995; 270 467 470
27. Selye H. A syndrome produced by diverse nocuous agents. Nature: 1936; 138 32
28. Shaw K. N., Commins S., O'Mara S. M. Deficits in spatial learning and synaptic plasticity induced by the rapid and competitive broad-spectrum cyclooxygenase inhibitor ibuprofen are reversed by increasing endogenous brain-derived neurotrophic factor. Eur J Neurosci: 2003; 17 2438 2446
29. Soya H. Stress response to exercise and its hypothalamic regulation: role of arginine-vasopressin. In: Nose H., Gisolfi C. V., Imaizumi K. (eds.) Exercise, Nutrition and Environmental Stress. Mich, USA Cooper Publishing Group: 2001; 21 37
30. Soya H., Mukai A., Deocaris C. C., Ohiwa N., Chang H., Nishijima T., Fujikawa T., Togashi K., Saito T. Threshold-like pattern of neuronal activation in the hypothalamus during treadmill running: establishment of a minimum running stress (MRS) rat model. Neurosci Res: 2007; 58 341 348
31. Soya H., Nakamura T., Deocaris C. C., Kimpara A., Iimura M., Fujikawa T., Chang H., McEwen B. S., Nishijima T. BDNF induction with mild exercise in the rat hippocampus. Biochem Biophys Res Commun: 2007; 358 961 967
32. Soya H., Okamoto M., Matsui T., Lee M., Inoue K., Soya S., Nishikawa S., Fujikawa T., Chang H., Nishijima T. Brain activation via exercise: exercise conditions leading to neuronal activation & hippocampal neurogenesis. J Exerc Nutr Biochem: 2011; 15 1 10
33. Spina R. J., Chi M. M., Hopkins M. G., Nemeth P. M., Lowry O. H., Holloszy J. O. Mitochondrial enzymes increase in muscle in response to 7-10 days of cycle exercise. J Appl Physiol: 1996; 80 2250 2254
34. Srere P. A. Citrate synthase. In: Lowestein J. M. (ed.) Methods in Enzymology.: 1969; 3 11
35. Sutanto W., Dekloet E. R. The use of various animal-models in the study of stress and stress-related phenomena. Lab Anim: 1994; 28 293 306
36. Trejo J. L., Llorens-Martin M. V., Torres-Aleman I. The effects of exercise on spatial learning and anxiety-like behavior are mediated by an IGF-I-dependent mechanism related to hippocampal neurogenesis. Mol Cell Neurosci: 2008; 37 402 411
37. Uysal N., Tugyan K., Kayatekin B. M., Acikgoz O., Bagriyanik H. A., Gonenc S., Ozdemir D., Aksu I., Topcu A., Semin I. The effects of regular aerobic exercise in adolescent period on hippocampal neuron density, apoptosis and spatial memory. Neurosci Lett: 2005; 383 241 245
38. Valor L. M., Barco A. Hippocampal gene profiling: toward a systems biology of the hippocampus. Hippocampus: 2012; 22 929 941
39. 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 USA: 1999; 96 13427 13431
40. Yanagisawa H., Dan I., Tsuzuki D., Kato M., Okamoto M., Kyutoku Y., Soya H. Acute moderate exercise elicits increased dorsolateral prefrontal activation and improves cognitive performance with Stroop test. Neuroimage: 2010; 50 1702 1710
41. Yirmiya R., Goshen I. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun: 2011; 25 181 213
42. Zhao C., Deng W., Gage F. H. Mechanisms and functional implications of adult neurogenesis. Cell: 2008; 132 645 660