Translating the impact of exercise on cognition: Methodological issues in animal research

Behavioural Brain Research

Volumn 273, Issue , 2014, Pages 177-188

  Hatchard, Taylor ^a   Ting, Jaimee J ^a   Messier, Claude ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Alzheimer's disease; Cognitive stimulation; Fitness; Metabolism; Physical exercise; Social stimulation

Indexed keywords

AGE; ANIMAL EXPERIMENT; ARTICLE; COGNITION; CONTROLLED STUDY; EXERCISE; EXERCISE INTENSITY; EXPERIMENTAL ANIMAL; HOUSING; MENTAL PERFORMANCE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RUNNING; SOCIAL ISOLATION; TREADMILL EXERCISE; AGING; ANIMAL; FEMALE; HUMAN; MALE; META ANALYSIS; MICROCLIMATE; MOUSE; PHYSIOLOGY; RAT;

AGING; ANIMALS; COGNITION; ENVIRONMENT, CONTROLLED; EXERCISE; FEMALE; HUMANS; MALE; MICE; PHYSICAL CONDITIONING, ANIMAL; RATS; SOCIAL ISOLATION;

EID: 84906346913     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.06.043     Document Type: Article

References (119)

1. Angevaren M., Aufdemkampe G., Verhaar H.J., Aleman A., Vanhees L. Physical activity and enhanced fitness to improve cognitive function in older people without known cognitive impairment. Cochrane Database Syst Rev 2008, 3. 10.1002/14651858.CD005381.pub3.
2. Chang Y.K., Labban J.D., Gapin J.I., Etnier J.L. The effects of acute exercise on cognitive performance: a meta-analysis. Brain Res 2012, 1453:87-101. 10.1016/j.brainres.2012.02.068.
3. Colcombe S., Kramer A.F. Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol Sci 2003, 14(2):125-130.
4. Erickson K.I., Kramer A.F. Aerobic exercise effects on cognitive and neural plasticity in older adults. Br J Sports Med 2009, 43(1):22-24. bjsm.2008.052498[pii]10.1136/bjsm.2008.052498.
5. Etnier J.L., Nowell P.M., Landers D.M., Sibley B.A. A meta-regression to examine the relationship between aerobic fitness and cognitive performance. Brain Res Rev 2006, 52(1):119-130.
6. Heyn P., Abreu B.C., Ottenbacher K.J. The effects of exercise training on elderly persons with cognitive impairment and dementia: a meta-analysis. Arch Phys Med Rehabil 2004, 85(10):1694-1704.
7. Hillman C.H., Erickson K.I., Kramer A.F. Be smart, exercise your heart: exercise effects on brain and cognition. Nat Rev Neurosci 2008, 9(1):58-65. nrn2298[pii]10.1038/nrn2298.
8. Kramer A.F., Erickson K.I. Capitalizing on cortical plasticity: influence of physical activity on cognition and brain function. Trends Cogn Sci 2007, 11(8):342-348.
9. Kramer A.F., Erickson K.I., Colcombe S.J. Exercise, cognition, and the aging brain. J Appl Physiol 2006, 101(4):1237-1242. 00500.2006[pii]10.1152/japplphysiol.00500.2006.
10. Rockwood K., Middleton L. Physical activity and the maintenance of cognitive function. Alzheimers Dement 2007, 3(2 Suppl):S38-S44. S1552-5260(07)00006-4[pii]10.1016/j.jalz.2007.01.003.
11. Hertzog C., Kramer A.F., Wilson R.S., Lindenberger U. Enrichment effects on adult cognitive development: can the functional capacity of older adults be preserved and enhanced?. Psychological Science in the Public Interest 2009, 9:1-65.
12. Miller D.I., Taler V., Davidson P.S.R., Messier C. Measuring the impact of exercise on cognitive aging: methodological issues. Neurobiol Aging 2012, 33(3):622.e29-622.e43. 10.1016/j.neurobiolaging.2011.02.020.
13. Stranahan A.M., Lee K., Martin B., Maudsley S., Golden E., Cutler R.G., Mattson M.P. Voluntary exercise and caloric restriction enhance hippocampal dendritic spine density and BDNF levels in diabetic mice. Hippocampus 2009, 19(10):951-961. 10.1002/hipo.20577.
14. Moraska A., Deak T., Spencer R.L., Roth D., Fleshner M. Treadmill running produces both positive and negative physiological adaptations in Sprague-Dawley rats. Am J Physiol Regul Integr Comp Physiol 2000, 279(4):R1321-R1329.
15. Lerman I., Harrison B.C., Freeman K., Hewett T.E., Allen D.L., Robbins J., Leinwand L.A. Genetic variability in forced and voluntary endurance exercise performance in seven inbred mouse strains. J Appl Physiol (1985) 2002, 92(6):2245-2255. 10.1152/japplphysiol.01045.2001.
16. Doallo S., Patai E.Z., Nobre A.C. Reward associations magnify memory-based biases on perception. J Cogn Neurosci 2013, 25(2):245-257.
17. Messier C., White N.M. Contingent and non-contingent actions of sucrose and saccharin reinforcers: effects on taste preference and memory. Physiol Behav 1984, 32:195-203.
18. White N.M., Milner P.M. The psychobiology of reinforcers. Annu Rev Psychol 1992, 43:443-471.
19. Tukey D.S., Lee M., Xu D., Eberle S.E., Goffer Y., Manders T.R., Ziff E.B., Wang J. Differential effects of natural rewards and pain on vesicular glutamate transporter expression in the nucleus accumbens. Mol Brain 2013, 6:32. 10.1186/1756-6606-6-32.
20. Glasper E.R., Schoenfeld T.J., Gould E. Adult neurogenesis: optimizing hippocampal function to suit the environment. Behav Brain Res 2012, 227(2):380-383. 10.1016/j.bbr.2011.05.013.
21. Taylor C.R., Heglund N.C., Maloiy G.M. Energetics and mechanics of terrestrial locomotion. I. Metabolic energy consumption as a function of speed and body size in birds and mammals. J Exp Biol 1982, 97:1-21.
22. Toscano-Silva M., da Silva S.G., Scorza F.A., Bonvent J.J., Cavalheiro E.A., Arida R.M. Hippocampal mossy fiber sprouting induced by forced and voluntary physical exercise. Physiol Behav 2010, 101(2):302-308. 10.1016/j.physbeh.2010.05.012.
23. 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(1):186-193.
24. Gulve E.A., Rodnick K.J., Henriksen E.J., Holloszy J.O. Effects of wheel running on glucose transporter (GLUT4) concentration in skeletal muscle of young adult and old rats. Mech Ageing Dev 1993, 67(1-2):187-200.
25. Armstrong R.B., Laughlin M.H., Rome L., Taylor C.R. Metabolism of rats running up and down an incline. J Appl Physiol: Respir, Environ Exercise Physiol 1983, 55(2):518-521.
26. Hamzah S., Higgins S., Abraham T., Taylor P., Vizbaraite D., Malkova D. The effect of glycaemic index of high carbohydrate diets consumed over 5 days on exercise energy metabolism and running capacity in males. J Sports Sci 2009, 27(14):1545-1554. 10.1080/02640410903134115.
27. Coggan A.R., Abduljalil A.M., Swanson S.C., Earle M.S., Farris J.W., Mendenhall L.A., Robitaille P.M. Muscle metabolism during exercise in young and older untrained and endurance-trained men. J Appl Physiol (1985) 1993, 75(5):2125-2133.
28. Vaanholt L.M., Garland T., Daan S., Visser G.H. Wheel-running activity and energy metabolism in relation to ambient temperature in mice selected for high wheel-running activity. J Comp Physiol B 2007, 177(1):109-118. 10.1007/s00360-006-0113-8.
29. Taylor C.R., Schmidt-Nielsen K., Raab J.L. Scaling of energetic cost of running to body size in mammals. Am J Physiol 1970, 219(4):1104-1107.
30. Minetti A.E., Gaudino P., Seminati E., Cazzola D. The cost of transport of human running is not affected, as in walking, by wide acceleration/deceleration cycles. J Appl Physiol 2013, 114(4):498-503. 10.1152/japplphysiol.00959.2012.
31. Daffner K.R. Promoting successful cognitive aging: a comprehensive review. J Alzheimers Dis 2009, HG3886624M103218[pii]10.3233/JAD-2009-1306.
32. Depp C., Vahia I.V., Jeste D. Successful aging: focus on cognitive and emotional health. Annu Rev Clin Psychol 2010, 10.1146/annurev.clinpsy.121208.131449.
33. Dell P.A., Rose F.D. The impairing effects of environmental impoverishment in rats-a cognitive deficit. Bull Br Psychol Soc 1987, 40:A71.
34. Diamond M.C., Lindner B., Johnson R., Bennett E.L., Rosenzweig M.R. Differences in occipital cortical synapses from environmentally enriched, impoverished, and standard colony rats. J Neurosci Res 1975, 1(2):109-119. 10.1002/jnr.490010203.
35. Diamond M.C., Rosenzweig M.R., Bennett E.L., Lindner B., Lyon L. Effects of environmental enrichment and impoverishment on rat cerebral cortex. J Neurobiol 1972, 3(1):47-64. 10.1002/neu.480030105.
36. Klippel J.A. Behavioral persistence following switchovers between environmental enrichment and impoverishment in mice. Dev Psychobiol 1978, 11(6):541-557. 10.1002/dev.420110604.
37. Melendez R.I., Gregory M.L., Bardo M.T., Kalivas P.W. Impoverished rearing environment alters metabotropic glutamate receptor expression and function in the prefrontal cortex. Neuropsychopharmacology 2004, 29(11):1980-1987. 10.1038/sj.npp.1300507.
38. Mohammed A.H., Zhu S.W., Darmopil S., Hjerling-Leffler J., Ernfors P., Winblad B., Diamond M.C., Eriksson P.S., Bogdanovic N. Environmental enrichment and the brain. Prog Brain Res 2002, 138:109-133. 10.1016/S0079-6123(02)38074-9.
39. Szeligo F., Leblond C.P. Response of the three main types of glial cells of cortex and corpus callosum in rats handled during suckling or exposed to enriched, control and impoverished environments following weaning. J Comp Neurol 1977, 172(2):247-263. 10.1002/cne.901720205.
40. Liu J., Dietz K., DeLoyht J.M., Pedre X., Kelkar D., Kaur J., Vialou V., Lobo M.K., Dietz D.M., Nestler E.J., Dupree J., Casaccia P. Impaired adult myelination in the prefrontal cortex of socially isolated mice. Nat Neurosci 2012, 15(12):1621-1623. 10.1038/nn.3263.
41. Campi K.L., Collins C.E., Todd W.D., Kaas J., Krubitzer L. Comparison of area 17 cellular composition in laboratory and wild-caught rats including diurnal and nocturnal species. Brain Behav Evol 2011, 77(2):116-130. 10.1159/000324862.
42. Martin B., Ji S., Maudsley S., Mattson M.P. "Control" laboratory rodents are metabolically morbid: why it matters. Proc Nat Acad Sci USA 2010, 107(14):6127-6133. 10.1073/pnas.0912955107.
43. Wojtowicz J.M., Kee N. BrdU assay for neurogenesis in rodents. Nat Protoc 2006, 1(3):1399-1405. nprot.2006.224[pii]10.1038/nprot.2006.224.
44. Borenstein M., Hedges L.V., Higgins J.P.T., Rothstein H.R. Introduction to meta-analysis 2009, Wiley, Wiltshire, England.
45. Cumming G., Finch S. Inferenes by eye: confidence internals, and how to read pictures of data. Am Psychol 2005, 60(2):170-180.
46. Epp J.R., Barker J.M., Galea L.A. Running wild: neurogenesis in the hippocampus across the lifespan in wild and laboratory-bred Norway rats. Hippocampus 2009, 19(10):1040-1049. 10.1002/hipo.20546.
47. Klaus F., Hauser T., Lindholm A.K., Cameron H.A., Slomianka L., Lipp H.P., Amrein I. Different regulation of adult hippocampal neurogenesis in Western house mice (Mus musculus domesticus) and C57BL/6 mice. Behav Brain Res 2012, 227(2):340-347. 10.1016/j.bbr.2011.07.026.
48. Klaus F., Amrein I. Running in laboratory and wild rodents: differences in context sensitivity and plasticity of hippocampal neurogenesis. Behav Brain Res 2012, 227(2):363-370.
49. Alaei H., Borjeian L., Azizi M., Orian S., Pourshanazari A., Hanninen O. Treadmill running reverses retention deficit induced by morphine. Eur J Pharmacol 2006, 536(1-2):138-141. 10.1016/j.ejphar.2006.02.025.
50. 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 Bodywork Mov Ther 2008, 12(1):72-75. 10.1016/j.jbmt.2007.05.004.
51. Asl N.A., Sheikhzade F., Torchi M., Roshangar L., Khamnei S. Long-term regular exercise promotes memory and learning in young but not in older rats. Pathophysiology 2008, 15(1):9-12. 10.1016/j.pathophys.2007.10.002.
52. Griffin E.W., Bechara R.G., Birch A.M., Kelly A.M. Exercise enhances hippocampal-dependent learning in the rat: evidence for a BDNF-related mechanism. Hippocampus 2009, 19(10):973-980. 10.1002/hipo.20631.
53. Kinni H., Guo M., Ding J.Y., Konakondla S., Dornbos D., Tran R., Guthikonda M., Ding Y. Cerebral metabolism after forced or voluntary physical exercise. Brain Res 2011, 1388:48-55. 10.1016/j.brainres.2011.02.076.
54. Aguiar A.S., Castro A.A., Moreira E.L., Glaser V., Santos A.R., Tasca C.I., Latini A., Prediger R.D. Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: involvement of hippocampal plasticity via AKT, CREB and BDNF signaling. Mech Ageing Dev 2011, 132(11-12):560-567. 10.1016/j.mad.2011.09.005.
55. Akhavan M.M., Emami-Abarghoie M., Sadighi-Moghaddam B., Safari M., Yousefi Y., Rashidy-Pour A. Hippocampal angiotensin II receptors play an important role in mediating the effect of voluntary exercise on learning and memory in rat. Brain Res 2008, 1232:132-138. 10.1016/j.brainres.2008.07.042.
56. Albeck D.S., Sano K., Prewitt G.E., Dalton L. Mild forced treadmill exercise enhances spatial learning in the aged rat. Behav Brain Res 2006, 168(2):345-348.
57. 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(5):425-429.
58. Cechetti F., Worm P.V., Elsner V.R., Bertoldi K., Sanches E., Ben J., Siqueira I.R., Netto C.A. Forced treadmill exercise prevents oxidative stress and memory deficits following chronic cerebral hypoperfusion in the rat. Neurobiol Learn Mem 2012, 97(1):90-96. 10.1016/j.nlm.2011.09.008.
59. Chae C.H., Jung S.L., An S.H., Park B.Y., Wang S.W., Cho I.H., Cho J.Y., Kim H.T. Treadmill exercise improves cognitive function and facilitates nerve growth factor signaling by activating mitogen-activated protein kinase/extracellular signal-regulated kinase1/2 in the streptozotocin-induced diabetic rat hippocampus. Neuroscience 2009, 164(4):1665-1673. 10.1016/j.neuroscience.2009.09.075.
60. Christie B.R., Swann S.E., Fox C.J., Froc D., Lieblich S.E., Redila V., Webber A. Voluntary exercise rescues deficits in spatial memory and long-term potentiation in prenatal ethanol-exposed male rats. Eur J Neurosci 2005, 21(6):1719-1726.
61. Clark P.J., Brzezinska W.J., Puchalski E.K., Krone D.A., Rhodes J.S. Functional analysis of neurovascular adaptations to exercise in the dentate gyrus of young adult mice associated with cognitive gain. Hippocampus 2009, 19(10):937-950. 10.1002/hipo.20543.
62. Clark P.J., Bhattacharya T.K., Miller D.S., Kohman R.A., Deyoung E.K., Rhodes J.S. New neurons generated from running are broadly recruited into neuronal activation associated with three different hippocampus-involved tasks. Hippocampus 2012, 10.1002/hipo.22020.
63. Creer D.J., Romberg C., Saksida L.M., van Praag H., Bussey T.J. Running enhances spatial pattern separation in mice. Proc Nat Acad Sci USA 2010, 107(5):2367-2372. 10.1073/pnas.0911725107.
64. Ding Q., Vaynman S., Akhavan M., Ying Z., Gomez-Pinilla F. Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neuroscience 2006, 140(3):823-833.
65. Eadie B.D., Redila V.A., Christie B.R. Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation, dendritic complexity, and spine density. J Comp Neurol 2005, 486(1):39-47.
66. Ebrahimi S., Rashidy-Pour A., Vafaei A.A., Akhavan M.M. Central beta-adrenergic receptors play an important role in the enhancing effect of voluntary exercise on learning and memory in rat. Behav Brain Res 2010, 208(1):189-193. 10.1016/j.bbr.2009.11.032.
67. Fabel K., Wolf S.A., Ehninger D., Babu H., Leal-Galicia P., Kempermann G. Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice. Front Neurosci 2009, 3:50. 10.3389/neuro.22.002.2009.
68. Farmer J., Zhao X., van Praag H., Wodtke K., Gage F.H., Christie B.R. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 2004, 124(1):71-79. 10.1016/j.neuroscience.2003.09.029[0306452203007450S][pii].
69. Ferreira A.F., Real C.C., Rodrigues A.C., Alves A.S., Britto L.R. Short-term, moderate exercise is capable of inducing structural, BDNF-independent hippocampal plasticity. Brain Res 2011, 1425:111-122. 10.1016/j.brainres.2011.10.004.
70. Garza A.A., Ha T.G., Garcia C., Chen M.J., Russo-Neustadt A.A. Exercise, antidepressant treatment, and BDNF mRNA expression in the aging brain. Pharmacol Biochem Behav 2004, 77(2):209-220. 10.1016/j.pbb.2003.10.020.
71. Hajisoltani R., Rashidy-Pour A., Vafaei A.A., Ghaderdoost B., Bandegi A.R., Motamedi F. The glucocorticoid system is required for the voluntary exercise-induced enhancement of learning and memory in rats. Behav Brain Res 2011, 219(1):75-81. 10.1016/j.bbr.2010.12.005.
72. Huang F.L., Huang K.P., Wu J., Boucheron C. Environmental enrichment enhances neurogranin expression and hippocampal learning and memory but fails to rescue the impairments of neurogranin null mutant mice. J Neurosci 2006, 26(23):6230-6237.
73. Ivy A.S., Rodriguez F.G., Garcia C., Chen M.J., Russo-Neustadt A.A. Noradrenergic and serotonergic blockade inhibits BDNF mRNA activation following exercise and antidepressant. Pharmacol Biochem Behav 2003, 75(1):81-88. 10.1016/s0091-3057(03)00044-3.
74. Kennard J., Woodruff-Pak D. Aging and exercise effects on motor learning and spatial memory. Ageing Res 2011, 3:4-11. e2 3(e2).
75. Kennard J.A., Woodruff-Pak D.S. A comparison of low- and high-impact forced exercise: effects of training paradigm on learning and memory. Physiol Behav 2012, 106(4):423-427. 10.1016/j.physbeh.2012.02.023.
76. Kumar A., Rani A., Tchigranova O., Lee W.H., Foster T.C. Influence of late-life exposure to environmental enrichment or exercise on hippocampal function and CA1 senescent physiology. Neurobiol Aging 2012, 33(4). 828 e1-828 e17. 10.1016/j.neurobiolaging.2011.06.023.
77. Leasure J.L., Jones M. Forced and voluntary exercise differentially affect brain and behavior. Neuroscience 2008, 156(3):456-465. 10.1016/j.neuroscience.2008.07.041.
78. Leasure J.L., Decker L. Social isolation prevents exercise-induced proliferation of hippocampal progenitor cells in female rats. Hippocampus 2009, 19(10):907-912. 10.1002/hipo.20563.
79. Lee M.C., Okamoto M., Liu Y.F., Inoue K., Matsui T., Nogami H., Soya H. Voluntary resistance running with short distance enhances spatial memory related to hippocampal BDNF signaling. J Appl Physiol (1985) 2012, 113(8):1260-1266. 10.1152/japplphysiol.00869.2012.
80. Liu H.L., Zhao G., Cai K., Zhao H.H., Shi L.D. Treadmill exercise prevents decline in spatial learning and memory in APP/PS1 transgenic mice through improvement of hippocampal long-term potentiation. Behav Brain Res 2011, 218(2):308-314. 10.1016/j.bbr.2010.12.030.
81. 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(6):943-952. 10.1002/dneu.22009.
82. Miladi-Gorji H., Rashidy-Pour A., Fathollahi Y., Akhavan M.M., Semnanian S., Safari M. Voluntary exercise ameliorates cognitive deficits in morphine dependent rats: the role of hippocampal brain-derived neurotrophic factor. Neurobiol Learn Mem 2011, 96(3):479-491. 10.1016/j.nlm.2011.08.001.
83. Molteni R., Wu A., Vaynman S., Ying Z., Barnard R.J., Gomez-Pinilla F. Exercise reverses the harmful effects of consumption of a high-fat diet on synaptic and behavioral plasticity associated to the action of brain-derived neurotrophic factor. Neuroscience 2004, 123(2):429-440.
84. Mustroph M.L., Chen S., Desai S.C., Cay E.B., Deyoung E.K., Rhodes J.S. Aerobic exercise is the critical variable in an enriched environment that increases hippocampal neurogenesis and water maze learning in male C57BL/6J mice. Neuroscience 2012, 10.1016/j.neuroscience.2012.06.007.
85. O'Callaghan R.M., Ohle R., Kelly A.M. The effects of forced exercise on hippocampal plasticity in the rat: a comparison of LTP, spatial- and non-spatial learning. Behav Brain Res 2007, 176(2):362-366.
86. Pang T.Y., Stam N.C., Nithianantharajah J., Howard M.L., Hannan A.J. Differential effects of voluntary physical exercise on behavioral and brain-derived neurotrophic factor expression deficits in Huntington's disease transgenic mice. Neuroscience 2006, 141(2):569-584.
87. Reisi P., Alaei H., Babri S., Sharifi M.R., Mohaddes G. Effects of treadmill running on spatial learning and memory in streptozotocin-induced diabetic rats. Neurosci Lett 2009, 455(2):79-83. 10.1016/j.neulet.2009.03.052.
88. Rhodes J.S., van Praag H., Jeffrey S., Girard I., Mitchell G.S., Garland T., 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(5):1006-1016.
89. Speisman R.B., Kumar A., Rani A., Foster T.C., Ormerod B.K. Daily exercise improves memory, stimulates hippocampal neurogenesis and modulates immune and neuroimmune cytokines in aging rats. Brain Behav Immun 2013, 28:25-43. 10.1016/j.bbi.2012.09.013.
90. Suijo K., Inoue S., Ohya Y., Odagiri Y., Takamiya T., Ishibashi H., Itoh M., Fujieda Y., Shimomitsu T. Resistance exercise enhances cognitive function in mouse. Int J Sports Med 2013, 34(4):368-375. 10.1055/s-0032-1323747.
91. Tanehkar F., Rashidy-Pour A., Vafaei A.A., Sameni H.R., Haghighi S., Miladi-Gorji H., Motamedi F., Akhavan M.M., Bavarsad K. Voluntary exercise does not ameliorate spatial learning and memory deficits induced by chronic administration of nandrolone decanoate in rats. Horm Behav 2013, 63(1):158-165. 10.1016/j.yhbeh.2012.10.003.
92. Titterness A.K., Wiebe E., Kwasnica A., Keyes G., Christie B.R. Voluntary exercise does not enhance long-term potentiation in the adolescent female dentate gyrus. Neuroscience 2011, 183:25-31. 10.1016/j.neuroscience.2011.03.050.
93. van Praag H., Christie B.R., Sejnowski T.J., Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Nat Acad Sci USA 1999, 96(23):13427-13431.
94. van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999, 2(3):266-270.
95. van Praag H., Shubert T., Zhao C., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 2005, 25(38):8680-8685.
96. Vaynman S., Ying Z., Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 2004, 20(10):2580-2590.
97. Vaynman S., Ying Z., Gomez-Pinilla F. Exercise induces BDNF and synapsin I to specific hippocampal subfields. J Neurosci Res 2004, 76(3):356-362. 10.1002/jnr.20077.
98. Vaynman S., Ying Z., Gomez-Pinilla F. The select action of hippocampal calcium calmodulin protein kinase II in mediating exercise-enhanced cognitive function. Neuroscience 2007, 144(3):825-833. 10.1016/j.neuroscience.2006.10.005.
99. Wojtowicz J.M., Askew M.L., Winocur G. The effects of running and of inhibiting adult neurogenesis on learning and memory in rats. Eur J Neurosci 2008, 27(6):1494-1502. EJN6128[pii]10.1111/j.1460-9568.2008.06128.x.
100. Yau S.Y., Lau B.W., Tong J.B., Wong R., Ching Y.P., Qiu G., Tang S.W., Lee T.M., So K.F. Hippocampal neurogenesis and dendritic plasticity support running-improved spatial learning and depression-like behaviour in stressed rats. PLoS one 2011, 6(9):e24263. 10.1371/journal.pone.0024263.
101. Yu F., Xu B., Song C., Ji L., Zhang X. Treadmill exercise slows cognitive deficits in aging rats by antioxidation and inhibition of amyloid production. NeuroReport 2013, 24(6):342-347. 10.1097/WNR.0b013e3283606c5e.
102. Zagaar M., Alhaider I., Dao A., Levine A., Alkarawi A., Alzubaidy M., Alkadhi K. The beneficial effects of regular exercise on cognition in REM sleep deprivation: behavioral, electrophysiological and molecular evidence. Neurobiol Dis 2012, 45(3):1153-1162. 10.1016/j.nbd.2011.12.039.
103. Stranahan A.M., Khalil D., Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nature Neurosci 2006, 9:526-533.
104. Stranahan A.M., Lee K., Becker K.G., Zhang Y., Maudsley S., Martin B., et al. Hippocampal gene expression patterns underlying the enhancement of memory by running in aged mice. Neurobiol Aging 2010, 31:1937-1949.
105. Belke T.W., Wagner J.P. The reinforcing property and the rewarding aftereffect of wheel running in rats: a combination of two paradigms. Behav Processes 2005, 68:165-172.
106. Iversen I.H. Techniques for Establishing Schedules with Wheel Running as Reinforcement in Rats. J Exp Anal Behav. 1993, 60:219-238.
107. Pierce W.D., Epling W.F., Boer D.P. Deprivation and satiation: The interrelations between food and wheel running. J Exp Anal Behav 1986, 46:199-210.
108. Kruska D. Comparative quantitative study on brains of wild and laboratory rats, I. Comparison of volume of total brain and classical brain parts. J Hirnforsch 1975, 16:469-483.
109. Ebinger P., Röhrs M. Volumetric analysis of brain structures, especially of the visual system in wild and domestic turkeys (Meleagris gallopavo). J Hirnforsch 1995, 36:219-228.
110. Plogmann D., Kruska D. Volumetric comparison of auditory structures in the brains of European wild boars (Sus scrofa) and domestic pigs (Sus scrofa f. dom.). Brain Behav Evol 1990, 35:146-155.
111. Popova N.K., Voitenko N.N., Kulikov A.V., Avgustinovich D.F. Evidence for the involvement of central serotonin in mechanism of domestication of silver foxes. Pharmacol Biochem Behav 1991, 40:751-756.
112. Markham J.A., Greenough W.T. Experience-driven brain plasticity: beyond the synapse. Neuron glia biology 2004, 1:351-363.
113. Diniz D.G., Foro C.A., Rego C.M., Gloria D.A., de Oliveira F.R., Paes J.M., et al. Environmental impoverishment and aging alter object recognition, spatial learning, and dentate gyrus astrocytes. Eur J Neurosci 2010, 32:509-519.
114. Haemisch A., Voss T., Gartner K. Effects of Environmental Enrichment on Aggressive-Behavior, Dominance Hierarchies, and Endocrine States in Male Dba/2j Mice. Physiology & Behavior 1994, 56:1041-1048.
115. Haemisch A., Gartner K. Effects of cage enrichment on territorial aggression and stress physiology in male laboratory mice. Acta Physiol Scand 1997, 161:73-76.
116. Van Loo P.L.P., Kruitwagen C.L.J.J., Koolhaas J.M., Van de Weerd H.A., Van Zutphen L.F.M., Baumans V. Influence of cage enrichment on aggressive behaviour and physiological parameters in male mice. Appl Anim Behav Sci 2002, 76:65-81.
117. Farley C.T., Gonzalez O. Leg stiffness and stride frequency in human running. J Biomech 1996, 29:181-186.
118. Holguin S., Huang Y., Liu J., Wurtman R. Chronic administration of DHA and UMP improves the impaired memory of environmentally impoverished rats. Behav Brain Res 2008, 191:11-16.
119. Tine M. Acute aerobic exercise: an intervention for the selective visual attention and reading comprehension of low-income adolescents. Front Psychol 2014, 5:575.