Use it and boost it with physical and mental activity

Hippocampus

Volumn 23, Issue 11, 2013, Pages 1125-1135

  Korol, Donna L ^a   Gold, Paul E ^a   Scavuzzo, Claire J ^b  

^a SYRACUSE UNIVERSITY   (United States)

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

Author keywords

BDNF; Learning strategy; Memory systems; Plasticity; Voluntary exercise

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

COGNITION; CORPUS STRIATUM; HIPPOCAMPUS; HUMAN; LEARNING; MEMORY; MENTAL PERFORMANCE; NEUROMODULATION; NONHUMAN; NOTE; PHYSICAL ACTIVITY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TASK PERFORMANCE; WORKING MEMORY;

BDNF; LEARNING STRATEGY; MEMORY SYSTEMS; PLASTICITY; VOLUNTARY EXERCISE;

AGING; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CORPUS STRIATUM; HIPPOCAMPUS; HUMANS; LEARNING; MAZE LEARNING; MEMORY; MOTOR ACTIVITY; NEURONAL PLASTICITY; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY;

EID: 84886500719     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22197     Document Type: Note

References (118)

1. Adlard PA, Perreau VM, Engesser-Cesar C, Cotman CW. 2004. The timecourse of induction of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus following voluntary exercise. Neurosci Lett 1:43-48.
2. 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.
3. Albert MS, Jones K, Savage CR, Berkman L, Seeman T, Blazer D, Rowe JW. 1995. Predictors of cognitive change in older persons: MacArthur studies of successful aging. Psychol Aging 10:578-589.
4. Alonso M, Vianna MR, Depino AM, Mello e Souza T, Pereira P, Szapiro G, Viola H, Pitossi F, Izquierdo I, Medina JH. 2002. BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation. Hippocampus 12:551-560.
5. Anderson BJ, Greenwood SJ, McCloskey D. 2010. Exercise as an intervention for the age-related decline in neural metabolic support. Front Aging Neurosci 2.
6. Anderson BJ, Li X, Alcantara AA, Isaacs KR, Black JE, Greenough WT. 1994. Glial hypertrophy is associated with synaptogenesis following motor-skill learning, but not with angiogenesis following exercise. Glia 11:73-80.
7. Ball K, Berch DB, Helmers KF, Jobe JB, Leveck MD, Marsiske M, Morris JN, Rebok GW, Smith DM, Tennstedt SL, Unverzagt FW, Willis SL. 2002. Effects of cognitive training interventions with older adults. JAMA 288:2271-2281.
8. Basak C, Boot WR, Voss MW, Kramer AF. 2008. Can training in a real-time strategy video game attenuate cognitive decline in older adults? Psych Aging 23:765-777.
9. Bekinschtein P, Cammarota M, Igaz LM, Bevilaqua LR, Izquierdo I, Medina JH. 2007. Persistence of long-term memory storage requires a late protein synthesis-and BDNF-dependent phase in the hippocampus. Neuron 53:261-277.
10. Bekinschtein P, Oomen CA, Saksida LM, Bussey TJ. 2011. Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable? Sem Cell Devel Biol 22:536-542.
11. Berchtold NC, Castello N, Cotman CW. 2010. Exercise and time-dependent benefits to learning and memory. Neuroscience 167:588-597.
12. Berchtold NC, Chinn G, Chou M, Kesslak JP, Cotman CW. 2005. Exercise primes a molecular memory for brain-derived neurotrophic factor protein induction in the rat hippocampus. Neuroscience 133:853-861.
13. Black JE, Issacs 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.
14. Brown DA, Johnson MS, Armstrong CJ, Lynch JM, Caruso NM, Ehlers LB, Fleshner M, Spencer RL, Moore RL. 2007. Short-term treadmill running in the rat: What kind of stressor is it? J App Physiol 103:1979-1985.
15. Buschkuehl M, Jaeggi SM, Hutchison S, Perrig-Chiello P, Däpp C, Müller M, Breil F, Hoppeler H, Perrig WJ. 2008. Impact of working memory training on memory performance in old-old adults. Psychol Aging 23:743-753.
16. Chang Q, Gold PE. 2003a. Intrahippocampal lidocaine injections impair acquisition of a place task and facilitate acquisition of a response task in rats. Behav Brain Res 144:19-24.
17. Chang Q, Gold PE. 2003b. Switching memory systems during learning: Changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats. J Neurosci 23:3001-3005.
18. Chang Q, Gold PE. 2004. Inactivation of dorsolateral striatum impairs acquisition of a response learning in cue-deficient, but not cue-available conditions. Behav Neurosci 118:383-388.
19. Churchill JD, Galvez R, Colcombe S, Swain RA, Kramer AF, Greenough WT. 2002. Exercise, experience and the aging brain. Neurobiol Aging 23:941-955.
20. Colcombe S, Kramer AF. 2003. Fitness effects on the cognitive function of older adults: A meta-analytic study. Psychol Sci 14:125-130.
21. Colcombe SJ, Kramer AF, Erickson KI, Scalf P, McAuley E, Cohen NJ, Webb A, Jerome GJ, Marquez DX, Elavsky S. 2004. Cardiovascular fitness, cortical plasticity and aging. Proc Natl Acad Sci USA 101:3316-3321.
22. Colombo PJ, Brightwell JJ, Countryman RA. 2003. Cognitive strategy-specific increases in phosphorylated cAMP response element-binding protein and c-Fos in the hippocampus and dorsal striatum. J Neurosci 23:3547-3554.
23. Colombo PJ. 2004 Learning-induced activation of transcription factors among multiple memory systems. Neurobiol Learn Mem 82:268-277.
24. Conner JM, Lauterborn JC, Yan Q, Gall CM, Varon S. 1997. Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: Evidence for anterograde axonal transport. J Neurosci 17:2295-2313.
25. Cotman CW, Berchtold NC. 2002. Exercise: A behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25:295-301.
26. Cotman CW, Berchtold N, Christie LA. 2007. Exercise builds brain health: Key roles of growth factor cascades and inflammation. Trends Neurosci 30:464-472.
27. Daniel JM, Lee CD. 2004. Estrogen replacement in ovariectomized rats affects strategy selection in the Morris water maze. Neurobiol Learn Mem 82:142-149.
28. Diamond MC, Lindner B, Johnson R, Bennett EL, Rosenzweig MR. 1975. Difference in occipital cortical synapses from environmentally enriched, impoverished, and standard colony rats. J Neurosci Res 1:109-119.
29. Ding Y, Li J, Luan X, Ding YH, Lai Q, Rafols JA, Phillis JW, Clark JC, Diaz FG. 2004. Exercise pre-conditioning reduces brain damage in ischemic rats that may be associated with regional angiogenesis and cellular overexpression of neurotrophin. Neuroscience 124:583-591.
30. Dishman RK, Berthoud HR, Booth FW, Cotman CW, Edgerton VR, Fleshner MR, Gandevia SC, Gomez-Pinilla F, Breenwood BN, Hillman CH, Kramer AF, Levin BE, Moran TH, Russo-Neustadt AA, Salamone JD, Van Hoomissen JD, Wade CE, York DA, Zigmond MJ. 2006. Neurobiology of exercise. Obesity 14:345-356.
31. Edelmann E, Leßmann V, Brigadski T. Pre- and postsynaptic twists in BDNF secretion and action in synaptic plasticity. Neuropharmacology (in press).
32. Ellen P, Deloache J. 1968. Hippocampal lesions and spontaneous alternation behavior in the rat. Physiol Behav 3:857-860.
33. Erickson KI, Prakash RS, Voss MW, Chaddock L, Hu L, Morris KS, White SM, Wojcicki TR, McAuley E, Kramer AF. 2009. Aerobic fitness is associated with hippocampal volume in elderly humans. Hippocampus 19:1030-1039.
34. 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 107:3017-3022.
35. Featherstone RE, McDonald RJ. 2004. Dorsal striatum and stimulus-response learning: Lesions of the dorsolateral, but not dorsomedial, striatum impair acquisition of a stimulus-response-based instrumental discrimination task, while sparing conditioned place preference learning. Neuroscience 124:23-31.
36. Fillit HM, Butler RN, O'Connell AW, Albert MS, Birren JE, Cotman CW, Greenough WT, Gold PE, Kramer AF, Kuller LH, Perls TT, Sahagan BG, Tully T. 2002. Achieving and maintaining cognitive vitality with aging. Mayo Clin Proc 77:681-696.
37. Frick KM, Benoit JD. 2010. Use it or lose it: Environmental enrichment as a means to promote successful cognitive aging. Scientific World J 10:1129-1141.
38. Friederici AD, Steinhauer K, Frisch S. 1999. Lexical integration: Sequential effects of syntactic and semantic information. Mem Cog 27:438-453.
39. Gold PE, Korol DL. 2010. Hormones and memory. In: Koob GF, Le Moal M, Thompson RF, editors. Encyclopedia of Behavioral Neuroscience, Vol 2, R. Dantzer, section ed. Oxford: Academic Press. pp 57-64.
40. Gold PE, Newman LA, Scavuzzo CJ, Korol DL. 2013. Modulation of multiple memory systems: From neurotransmitters to metabolic substrates. Hippocampus 23:1053-1065.
41. Gomez-Pinilla F, So V, Kesslak JP. 2001. Spatial learning induces neurotrophin receptor and synapsin I in the hippocampus. Brain Res 904:13-19.
42. Grazina R, Massano J. 2013. Physical exercise and Parkinson's disease: Influence on symptoms, disease course and prevention. Rev Neurosci 24:139-152.
43. Green CS, Bavelier D. 2008. Exercising your brain: A review of human brain plasticity and training-induced learning. Psychol Aging 23:692-701.
44. Greenough WT, Wood WE, Madden TC. 1972. Possible memory storage differences among mice reared in environments varying in complexity. Behav Biol 7:717-722.
45. Hall CB, Lipton RB, Sliwinski M, Katz MJ, Derby CA, Verghese J. 2009. Cognitive activities delay onset of memory decline in persons who develop dementia. Neurology 73:356-361.
46. Hall J, Thomas KL, Everitt BJ. 2000. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat Neurosci 3: 533-535.
47. Hallock HL, Arreola AC, Shaw CL, Griffin AL. 2013. Dissociable roles of the dorsal striatum and dorsal hippocampus in conditional discrimination and spatial alternation T-maze tasks. Neurobiol Learn Mem 100:108-116.
48. Hillman CH, Erickson KI, Kramer AF. 2008. Be smart, exercise your heart: Exercise effects on brain and cognition. Nat Rev Neurosci 9:58-65.
49. Hopkins ME, Bucci DJ. 2010. BDNF expression in perirhinal cortex is associated with exercise-induced improvement in object recognition memory. Neurobiol Learn Mem 94:278-284.
50. Hopkins ME, Nitecki R, Bucci DJ. 2011. Physical exercise during adolescence versus adulthood: Differential effects on object recognition memory and brain derived neurotrophic factor levels. Neurosci 194:84-94.
51. Horch HW, Katz LC. 2002. BDNF release from single cells elicits local dendritic growth in nearby neurons. Nat Neurosci 5:1177-1184.
52. Iaria G, Petrides M, Dagher A, Pike B, Bohbot VD. 2003. Cognitive strategies dependent on the hippocampus and caudagte nucleus in human navigation: Variability and change with practice. J Neurosci 23:5945-5952.
53. Intlekofer KA, Cotman CW. 2013. Exercise counteracts declining hippocampal function in aging and Alzheimer's disease. Neurobiol Dis 57:47-55.
54. 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.
55. Jia Y, Gall CM, Lynch G. 2010. Presynaptic BDNF promotes postsynaptic long-term potentiation in the dorsal striatum. J Neurosci 30:14440-14445.
56. Johnson CT, Olton DS, Gage FH, Jenko PG. 1977. Damage to hippocampus and hippocampal connections: Effects on DRL and spontaneous alternation. J Comp Physiol Psych 91: 508-522.
57. Kesslak JP, So V, Choi J, Cotman CW, Gomez-Pinilla F. 1998. Learning upregulates brain-derived neurotrophic factor messenger ribonucleic acid: A mechanism to facilitate encoding and circuit maintenance? Behav Neurosci. 112:1012-1019.
58. Kleinknecht KR, Bedenk BT, Kaltwasser SF, Gruenecker B, Yen YC, Czisch M, Wotjak CT. 2012. Hippocampus-dependent place learning enables spatial flexibility in C57BL6/N mice. Front Behav Neurosci 6:87:1-17.
59. Klintsova AY, Dickson E, Yoshida R, Greenough WT. 2004. Altered expression of BDNF and its high-affinity receptor TrkB in response to complex motor learning and moderate exercise. Brain Res 1028:92-104.
60. Kolb B, Gibb R. 1991. Environmental enrichment and cortical injury: Behavioral and anatomical consequences of frontal cortex lesions. Cereb Cortex 1:189-198.
61. Korol DL. 2002. Enhancing cognitive functions across the life span. In: Harman D, editor. Increasing the Healthy Life Span: Conventional Measures and Slowing the Innate Aging Process. Annals of the New York Academy of Sciences, Vol. 959. p 167-179.
62. Korol DL, Kolo LL. 2002. Estrogen-induced changes in place and response learning in young adult female rats. Behav Neurosci 116:411-420.
63. Korol DL, Malin EL, Borden KA, Busby RA, Couper-Leo JM. 2004. Shifts in preferred learning strategy across the estrous cycle in female rats. Horm Behav 45:330-338.
64. Kramer AF, Erickson KI. 2007. Capitalizing on cortical plasticity: Influence of physical activity on cognition and brain function. Trends Cog Sci 11:342-348.
65. Kramer AF, Colcombe S, Erickson K, Belopolsky A, McAuley E, Cohen NJ, Webb A, Jerome GJ, Marquez DX, Wszalek TM. 2002. Effects of aerobic fitness training on human cortical function. J Mol Neurosci 19:227-231.
66. 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.
67. Lalonde R. 2002. The neurobiological basis of spontaneous alternation. Neurosci Biobehav Rev 26:91-104.
68. Leasure JL, Jones M. 2008. Forced and voluntary exercise differentially affect brain and behavior. Neurosci 156:456-465.
69. Lee JLC, Everitt BJ, Thomas KL. 2004. Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science 304:839-843.
70. Liu YF, Chen HI, Wu CL, Kuo YM, Yu L, Huang AM, Wu F-S, Chuang J-I, Jen CJ. 2009. Differential effects of treadmill running and wheel running on spatial or aversive learning and memory: Roles of amygdalar brain-derived neurotrophic factor and synaptotagmin I. J Physiol 587:3221-3231.
71. Lu B. 2003. BDNF and activity-dependent synaptic modulation. Learn Mem 10:86-98.
72. Marais L, Stein DJ, Daniels WM. 2009. Exercise increases BDNF levels in the striatum and decreases depressive-like behavior in chronically stressed rats. Metab Brain Dis 24: 587-597.
73. Markowska AL, Savonenko AV. 2002. Protective effect of practice on cognition during aging: Implications for predictive characteristics of performance and efficacy of practice. Neurobiol Learn Mem 778L294-320.
74. Matthews DB, Ilgen M, White AM, Best PJ. 1999. Ethanol disrupts spatial performance while facilitating non-spatial performance in the rat. Neurobiol Learn Mem 72:169-179.
75. McIntyre CK, Marriott LK, Gold PE. 2003. Patterns of brain acetylcholine release predict individual differences in preferred learning strategies in rats. Neurobiol Learn Mem 79:177-183.
76. McNay EC, Fries TM, Gold PE. 2000. Decreases in rat extracellular hippocampal glucose concentration associated with cognitive demand during a spatial task. Proc Nat Acad Sci USA 97:2881-2885.
77. Mello PB, Benetti F, Cammarota M, Izquierdo I. 2008. Effects of acute and chronic physical exercise and stress on different types of memory in rats. Anais Acad Brasil Ciências 80:301-309.
78. Minichiello L. 2009. TrkB signalling pathways in LTP and learning. Nat Rev Neurosci 10:850-860.
79. Mizuno M, Yamada K, Olariu A, Nawa H, Nabeshima T. 2000. Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J Neurosci 20:7116-7121.
80. Molteni R, Wu A, Vaynman S, Ying Z, Barnard RJ, Gomez-Pinilla F. 2004. Exercise reverses the harmful effects of a high fat diet on synaptic and behavioral plasticity associated to the action of brain-derived neurotrophic factor. Neurosci 123:429-440.
81. Moraska A, Deak T, Spencer RL, Roth D, Fleshner M. 2000. Treadmill running produces both positive and negative physiological adaptations in Sprague-Dawley rats. Am J Physiol Regul Integr Comp Physiol 279:R1321-R1329.
82. Neeper SA, Gomez-Pinilla F, Choi J, Cotman CW. 1995. Exercise and brain neurotrophins. Nature 373:109.
83. Newman LA, Korol DL, Gold PE. 2011. Lactate produced by glycogenolysis in astrocytes regulates memory processing. PLoS ONE 6:e28427.
84. 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. Neurosci 144:1141-1151.
85. Olson AK, Eadie BD, Ernst C, Christie BR. 2006. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 16:250-260.
86. Ou LC, Gean PW. 2005. Regulation of amygdala-dependent learning by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol-3-kinase. Neuropsychopharm 31:287-296.
87. Packard MG, McGaugh JL. 1996. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65:65-72.
88. Packard MG, Hirsh R, White NM. 1989. Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: Evidence for multiple memory systems. J Neurosci 9:1465-1472.
89. Parpura V, Zorec R. 2010. Gliotransmission: Exocytotic release from astrocytes. Brain Res Rev 63:83-92.
90. Pisani SL, Neese SL, Doerge DR, Helferich WG, Schantz SL, Korol DL. 2012. Acute genistein treatment mimics the effects of estradiol by enhancing place learning and impairing response learning in young adult female rats. Horm Behav 62:491-499.
91. Poo MM. 2001. Neurotrophins as synaptic modulators. Nat Rev Neurosci 2:24-32.
92. Pych JC, Chang Q, Colon-Rivera C, Gold PE. 2005. Acetylcholine release in hippocampus and striatum during testing on a rewarded spontaneous alternation task. Neurobiol Learn Mem 84:93-101.
93. Ragozzino KE, Leutgeb S, Mizumori SJ. 1999. Dorsal striatal head direction and hippocampal place representations during spatial navigation. Exp Brain Res 139:372-376.
94. Rampon C, Tang YP, Goodhouse J, Shimizu E, Kyin M, Tsien JZ. 2000. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat Neurosci 3:238-244.
95. Raz N, Lindenberger U, Rodrigue KM, Kennedy KM, Head D, Williamson A, Dahle C, Gerstorf D, Acker JD. 2005. Regional brain changes in aging healthy adults: General trends, individual differences and modifiers. Cereb Cortex 15:1676-1689.
96. Roux PP, Dorval G, Boudreau M, Angers-Loustau A, Morris SJ, Makkerh J, Barker PA. 2002. K252a and CEP1347 are neuroprotective compounds that inhibit mixed-lineage kinase-3 and induce activation of Akt and ERK. J Biol Chem 277:49473-49480.
97. Sadowski RN, Jackson GR, Wieczorek L, Gold PE. 2009. Effects of stress, corticosterone, and epinephrine administration on learning in place and response tasks. Behav Brain Res 205:19-25.
98. Schinder AF, Poo M. 2000. The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci 23:639-645.
99. Schwabe L, Schächinger H, de Kloet ER, Oitzl MS. 2010. Corticosteroids operate as a switch between memory systems. J Cog Neurosci 22:1362-1372.
100. Schwabe L, Wolf OT. 2009. Stress prompts habit behavior in humans. J Neurosci 29:7191-7198.
101. Sherwin CM. 1998. Voluntary wheel running: A review and novel interpretation. Anim Behav 56:11-27.
102. Sirevaag AM, Greenough WT. 1987. Differential rearing effects on rat visual cortex synapses.: III. Neuronal and glial nuclei, boutons, dendrites, and capillaries. Brain Res 424:320-332.
103. Smith AD, Zigmond MJ. 2003. Can the brain be protected through exercise? Lessons from an animal model of parkinsonism. Exp Neurol 184:31-39.
104. Stevens R, Cowey A. 1973. Effects of dorsal and ventral hippocampal lesions on spontaneous alternation, learned alternation and probability learning in rats. Brain Res 52:203-224.
105. Stroth S, Hille K, Spitzer M, Reinhardt R. 2009. Aerobic endurance exercise benefits memory and affect in young adults. Neuropsych Rehab 19:223-243.
106. Tapley P, Lamballe F, Barbacid M. 1992. K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors. Oncogene 7:371-381.
107. Tyas SL, Snowdon DA, Desrosiers MF, Riley KP, Markesbery WR. 2007. Healthy ageing in the Nun Study: Definition and neuropathologic correlates. Age Ageing 36:650-655.
108. van Praag H, Christie BR, Sejnowski TJ, Gage FH. 1999. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96:13427-13431.
109. Van Praag H, Shubert T, Zhao C, Gage FH. 2005. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25:8680-8685.
110. 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.
111. Weuve J, Kang JH, Manson JE, Breteler MM, Ware JH, Grodstein F. 2004. Physical activity, including walking, and cognitive function in older women. J Am Med Assoc 292:1454-1461.
112. White NM, McDonald RJ. 2002. Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem 77:125-184.
113. Will B, Galani R, Kelche C, Rosenzweig MR. 2004. Recovery from brain injury in animals: Relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Prog Neurobiol 72:167-182.
114. Woodlee MT, Schallert T. 2006. The Impact of Motor Activity and Inactivity on the Brain Implications for the Prevention and Treatment of Nervous-System Disorders. Curr Dir Psych Sci 15:203-206.
115. Yaffe K, Barnes D, Nevitt M, Lui LY, Covinsky K. 2001. A prospective study of physical activity and cognitive decline in elderly women who walk. Arch Int Med 161:1703-1708.
116. Yanagita S, Amemiya S, Suzuki S, Kita I. 2007. Effects of spontaneous and forced running on activation of hypothalamic corticotropin-releasing hormone neurons in rats. Life Sci 80:356-363.
117. Zurkovsky L, Brown SL, Korol DL. 2006. Estrogen enhances place learning through estrogen receptors in the hippocampus. Neurobiol Learn Mem 86:336-343.
118. Zurkovsky L, Brown SL, Boyd SE, Fell JA, Korol DL. 2007. Estrogen modulates learning in female rats by acting directly at distinct memory systems. Neurosci 144:26-37.