Exercise neuroprotection in a rat model of binge alcohol consumption

Alcoholism: Clinical and Experimental Research

Volumn 34, Issue 3, 2010, Pages 404-414

  Leasure, J Leigh ^a   Nixon, Kimberly ^b  

^a UNIVERSITY OF HOUSTON   (United States)

^b University of Kentucky   (United States)

Author keywords

Adult Neurogenesis; Alcoholism; Dentate Gyrus; Ethanol; Neurodegeneration

Indexed keywords

ALCOHOL; KI 67 ANTIGEN;

ALCOHOL CONSUMPTION; ALCOHOL INTOXICATION; ALCOHOLISM; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIORAL SENSITIVITY; BRAIN; BRAIN CORTEX; CELL DEATH; CELL LOSS; CELL PROLIFERATION; CELL PROTECTION; CONTROLLED STUDY; DENTATE GYRUS; ENTORHINAL CORTEX; EXERCISE; FEMALE; GRANULE CELL; HISTOLOGY; LIVER METABOLISM; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PYRIFORM CORTEX; RAT;

ALCOHOLIC INTOXICATION; ANIMALS; BODY WEIGHT; BRAIN; CELL DEATH; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DENTATE GYRUS; ETHANOL; FEMALE; HIPPOCAMPUS; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, LONG-EVANS; STEM CELLS;

ANIMALIA; RATTUS;

EID: 77749261113     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2009.01105.x     Document Type: Article

References (111)

1. Agartz I, Momenan R, Rawlings RR, Kerich MJ, Hommer DW (1999) Hippocampal volume in patients with alcohol dependence. Arch Gen Psychiatry 56 : 356 363.
2. Alessio HM, Hagerman AE, Nagy S, Philip B, Byrnes RN, Woodward JL, Callahan P, Wiley RL (2005) Exercise improves biomarkers of health and stress in animals fed ad libitum. Physiol Behav 84 : 65 72.
3. Ardies CM, Morris GS, Erickson CK, Farrar RP (1989) Both acute and chronic exercise enhance in vivo ethanol clearance in rats. J Appl Physiol 66 : 555 560.
4. Asano M, Kaneoka K, Nomura T, Asano K, Sone H, Tsurumaru K, Yamashita K, Matsuo K, Suzuki H, Okuda Y (1998) Increase in serum vascular endothelial growth factor levels during altitude training. Acta Physiol Scand 162 : 455 459. (Pubitemid 28188263)
5. Bengochea O, Gonzalo LM (1990) Effect of chronic alcoholism on the human hippocampus. Histol Histopathol 5 : 349 357.
6. 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.
7. Black JE, Isaacs 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.
8. Brown RA, Abrantes AM, Read JP, Marcus BH, Jakicic J, Strong DR, Oakley JR, Ramsey SE, Kahler CW, Stuart G, Dubreuil ME, Gordon AA (2009) Aerobic exercise for alcohol recovery: rationale, program description, and preliminary findings. Behav Modif 33 : 220 249.
9. Cadete-Leite A, Tavares MA, Uylings HBM, Paula-Barbosa MM (1988) Granule cell loss and dendritic regrowth in the hippocampal dentate gyrus of the rat after chronic alcohol consumption. Brain Res 473 : 1 14.
10. Calabrese V, Scapagnini G, Latteri S, Colombrita C, Ravagna A, Catalano C, Pennisi G, Calvani M, Butterfield DA (2002) Long-term ethanol administration enhances age-dependent modulation of redox state in different brain regions in the rat: protection by acetyl carnitine. Int J Tissue React 24 : 97 104. (Pubitemid 36292240)
11. Canzanelli A, Guild R, Rapport D (1934) The use of ethyl alcohol as a fuel in muscular exercise. Am J Physiol 110 : 416 421.
12. Carpenter T, Lee RC, Burdett M (1933) The effect of muscular exercise on the disappearance of ethyl alcohol in man. Am J Physiol 105 : 17.
13. Carro E, Nunez A, Busiguina S, Torres-Aleman I (2000) Circulating insulin-like growth factor I mediates the effects of exercise on the brain. J Neurosci 20 : 2926 2933.
14. 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.
15. Christie BR, Swann SE, Fox CJ, Froc D, Lieblich SE, Redila V, Webber A (2005) Voluntary exercise rescues deficits in spatial memory and long-term potentiation in prenatal ethanol-exposed male rats. Eur J Neurosci 21 : 1719 1726.
16. Collins MA, Corse TD, Neafsey EJ (1996) Neuronal degeneration in rat cerebrocortical and olfactory regions during subchronic "binge" intoxication with ethanol: possible explanation for olfactory deficits in alcoholics. Alcohol Clin Exp Res 20 : 284 292.
17. Corbin WR, Vaughan EL, Fromme K (2008) Ethnic differences and the closing of the sex gap in alcohol use among college-bound students. Psychol Addict Behav 22 : 240 248.
18. Cotman CW, Berchtold NC (2002) Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25 : 295 301.
19. Courtney KE, Polich J (2009) Binge drinking in young adults: data, definitions, and determinants. Psychol Bull 135 : 142 156.
20. Crews FT (1999) Alcohol and neurodegeneration. CNS Drug Rev 5 : 379 394.
21. Crews FT, Braun CJ, Hoplight B, Switzer RC III., Knapp DJ (2000) Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. Alcohol Clin Exp Res 24 : 1712 1723.
22. Crews FT, Mdzinarishvili A, Kim D, He J, Nixon K (2006b) Neurogenesis in adolescent brain is potently inhibited by ethanol. Neuroscience 137 : 437 445.
23. Crews FT, Nixon K (2009) Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcohol 44 : 115 127.
24. Crews F, Nixon K, Kim D, Joseph J, Shukitt-Hale B, Qin L, Zou J (2006a) BHT blocks NF-kappaB activation and ethanol-induced brain damage. Alcohol Clin Exp Res 30 : 1938 1949.
25. Crews FT, Nixon K, Wilkie ME (2004) Exercise reverses ethanol inhibition of neural stem cell proliferation. Alcohol 33 : 63 71.
26. Davis MI (2008) Ethanol-BDNF interactions: still more questions than answers. Pharmacol Ther 118 : 36 57.
27. De Bellis MD, Clark DB, Beers SR, Soloff PH, Boring AM, Hall J, Kersh A, Keshavan MS (2000) Hippocampal volume in adolescent-onset alcohol use disorders. Am J Psychiatry 157 : 737 744.
28. 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.
29. 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.
30. Faherty CJ, Raviie Shepherd K, Herasimtschuk A, Smeyne RJ (2005) Environmental enrichment in adulthood eliminates neuronal death in experimental Parkinsonism. Brain Res Mol Brain Res 134 : 170 179.
31. 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.
32. Fuchs E, Czeh B, Kole MH, Michaelis T, Lucassen PJ (2004) Alterations of neuroplasticity in depression: the hippocampus and beyond. Eur Neuropsychopharmacol 14 (Suppl. 5 S481 S490.
33. Galea LA (2008) Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res Rev 57 : 332 341.
34. Gomez-Pinilla F, Dao L, So V (1997) Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Res 764 : 1 8.
35. Gonenc S, Uysal N, Acikgoz O, Kayatekin BM, Sonmez A, Kiray M, Aksu I, Gulecer B, Topcu A, Semin I (2005) Effects of melatonin on oxidative stress and spatial memory impairment induced by acute ethanol treatment in rats. Physiol Res 54 : 341 348.
36. Griesbach GS, Gomez-Pinilla F, Hovda DA (2004) The upregulation of plasticity-related proteins following TBI is disrupted with acute voluntary exercise. Brain Res 1016 : 154 162.
37. Gundersen HJ, Jensen EB, Kiêu K, Nielsen J (1999) The efficiency of systematic sampling in stereology - reconsidered. J Microsc 193 : 199 211.
38. Harper C (1985) Brain atrophy in chronic alcoholic patients: a quantitative pathological study. J Neurol Neurosurg Psychiatry 48 : 211 217. (Pubitemid 15085005)
39. Hartzler B, Fromme K (2003) Heavy episodic drinking and college entrance. J Drug Educ 33 : 259 274.
40. Hashimoto JG, Wiren KM (2008) Neurotoxic consequences of chronic alcohol withdrawal: expression profiling reveals importance of gender over withdrawal severity. Neuropsychopharmacology 33 : 1084 1096.
41. Hasin DS, Stinson FS, Ogburn E, Grant BF (2007) Prevalence, correlates, disability, and comorbidity of DSM-IV alcohol abuse and dependence in the United States: results from the National Epidemiologic Survey on Alcohol and Related Conditions. Arch Gen Psychiatry 64 : 830 842.
42. Hayes K, Sprague S, Guo M, Davis W, Friedman A, Kumar A, Jimenez DF, Ding Y (2008) Forced, not voluntary, exercise effectively induces neuroprotection in stroke. Acta Neuropathol 115 : 289 296.
43. He J, Nixon K, Shetty AK, Crews FT (2005) Chronic alcohol exposure reduces hippocampal neurogenesis and dendritic growth of newborn neurons. Eur J Neurosci 21 : 2711 2720.
44. Herrera DG, Yague AG, Johnsen-Soriano S, Bosch-Morell F, Collado-Morente L, Muriach M, Romero FJ, Garcia-Verdugo JM (2003) Selective impairment of hippocampal neurogenesis by chronic alcoholism: protective effects of an antioxidant. Proc Natl Acad Sci USA 100 : 7919 7924.
45. Hommer D, Momenan R, Kaiser E, Rawlings R (2001) Evidence for a gender-related effect of alcoholism on brain volumes. Am J Psychiatry 158 : 198 204.
46. Hunt WA (1993) Are binge drinkers more at risk of developing brain damage? Alcohol 10 : 559 561.
47. Johnsen-Soriano S, Bosch-Morell F, Miranda M, Asensio S, Barcia JM, Roma J, Monfort P, Felipo V, Romero FJ (2007) Ebselen prevents chronic alcohol-induced rat hippocampal stress and functional impairment. Alcohol Clin Exp Res 31 : 486 492.
48. Johnston LD, O'Malley PM, Bachman JG, Schulenberg JE (2007) Monitoring the Future National Survey Results on Drug Use, 1975-2006: Volume I, Secondary School Students. National Institute on Drug Abuse, Bethesda, MD.
49. 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.
50. Keyes KM, Grant BF, Hasin DS (2008) Evidence for a closing gender gap in alcohol use, abuse, and dependence in the United States population. Drug Alcohol Depend 93 : 21 29.
51. Knapp DJ, Crews FT (1999) Induction of cyclooxygenase-2 in brain during acute and chronic ethanol treatment and ethanol withdrawal. Alcohol Clin Exp Res 23 : 633 643.
52. Koob GF, Le Moal M (1997) Drug abuse: hedonic homeostatic dysregulation. Science 278 : 52 58.
53. Ku BM, Joo Y, Mun J, Roh GS, Kang SS, Cho GJ, Choi WS, Kim HJ (2006) Heme oxygenase protects hippocampal neurons from ethanol-induced neurotoxicity. Neurosci Lett 405 : 168 171.
54. Lambert GW, Jonsdottir IH (1998) Influence of voluntary exercise on hypothalamic norepinephrine. J Appl Physiol 85 : 962 966.
55. Leasure JL, Decker L (2009) Social Isolation prevents exercise-induced proliferation of hippocampal progenitor cells in female rats. Hippocampus 19 : 907 912.
56. Leasure JL, Jones M (2008) Forced and voluntary exercise differentially affect brain and behavior. Neuroscience 156 : 456 465.
57. 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.
58. Liu YF, Chen HI, Yu L, Kuo YM, Wu FS, Chuang JI, Liao PC, Jen CJ (2008) Upregulation of hippocampal TrkB and synaptotagmin is involved in treadmill exercise-enhanced aversive memory in mice. Neurobiol Learn Mem 90 : 81 89.
59. Majchrowicz E (1975) Induction of physical dependence upon ethanol and the associated behavioral changes in rats. Psychopharmacology 43 : 245 254.
60. Mann K, Batra A, Gunthner A, Schroth G (1992) Do women develop alcoholic brain damage more readily than men? Alcohol Clin Exp Res 16 : 1052 1056.
61. Montoliu C, Valles S, Renau-Piqueras J, Guerri C (1994) Ethanol-induced oxygen radical formation and lipid peroxidation in rat brain: effect of chronic alcohol consumption. J Neurochem 63 : 1855 1862.
62. 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.
63. Morris SA, Smith AR, Eaves DW, Nixon K (2010) Alcohol inhibition of neurogenesis: a mechanism of hippocampal neurodegeneration in an adolescent alcohol abuse model. Hippocampus (in press).
64. NRC (1996) Guide for the Care and Use of Laboratory Animals. The National Academies Press, Washington, D.C.
65. Naylor AS, Persson AI, Eriksson PS, Jonsdottir IH, Thorlin T (2005) Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat. J Neurophysiol 93 : 2406 2414.
66. Neal DJ, Fromme K (2007) Hook 'em horns and heavy drinking: alcohol use and collegiate sports. Addict Behav 32 : 2681 2693.
67. Neeper SA, Gomez-Pinilla F, Choi J, Cotman C (1995) Exercise and brain neurotrophins. Nature 373 : 109.
68. Nixon K, Crews FT (2002) Binge ethanol exposure decreases neurogenesis in adult rat hippocampus. J Neurochem 83 : 1087 1093.
69. Nixon K, Crews FT (2004) Temporally specific burst in cell proliferation increases hippocampal neurogenesis in protracted abstinence from alcohol. J Neurosci 24 : 9714 9722.
70. Nixon K, Kim DH, Potts EN, He J, Crews FT (2008) Distinct cell proliferation events during abstinence after alcohol dependence: microglia proliferation precedes neurogenesis. Neurobiol Dis 31 : 218 229.
71. Nixon SJ, Tivis R, Parsons OA (1995) Behavioral dysfunction and cognitive efficiency in male and female alcoholics. Alcohol Clin Exp Res 19 : 577 581.
72. Noble EG, Moraska A, Mazzeo RS, Roth DA, Olsson MC, Moore RL, Fleshner M (1999) Differential expression of stress proteins in rat myocardium after free wheel or treadmill run training. J Appl Physiol 86 : 1696 1701.
73. Obernier JA, Bouldin TW, Crews FT (2002a) Binge ethanol exposure in adult rats causes necrotic cell death. Alcohol Clin Exp Res 26 : 547 557.
74. Obernier JA, White AM, Swartzwelder HS, Crews FT (2002b) Cognitive deficits and CNS damage after a 4-day binge ethanol exposure in rats. Pharmacol Biochem Behav 72 : 521 532.
75. Oliff HS, Berchtold NC, Isackson P, Cotman CW (1998) Exercise-induced regulation of brain-derived neurotrophic factor (BDNF) transcriipts in the rat hippocampus. Brain Res Mol Brain Res 61 : 147 153.
76. Pandey SC, Chandler LJ, Nixon K, Crews FT, Hensler JG, Ukai W, Saito T (2005a) Neurotrophic factor signaling in alcoholism. Alcohol Clin Exp Res 29 : 1098 1105.
77. Pandey SC, Chartoff EH, Carlezon WA Jr., Zou J, Zhang H, Kreibich AS, Blendy JA, Crews FT (2005b) CREB gene transcription factors: role in molecular mechanisms of alcohol and drug addiction. Alcohol Clin Exp Res 29 : 176 184.
78. Pescatello LS, Franklin BA, Fagard R, Farquhar WB, Kelley GA, Ray CA (2004) American College of Sports Medicine position stand. Exercise and hypertension. Med Sci Sports Exerc 36 : 533 553.
79. Pfefferbaum A, Kim KO, Zipursky RB, Mathalon DH, Lane B, Ha CN, Rosenbloom MJ, Sullivan EV (1992) Brain gray and white matter volume loss accelerates with aging in chronic alcoholics: a quantitative MRI study. Alcohol Clin Exp Res 16 : 1078 1089.
80. Prendergast MA (2004) Do women possess a unique susceptibility to the neurotoxic effects of alcohol? J Am Med Womens Assoc 59 : 225 227.
81. Radak Z, Kaneko T, Tahara S, Nakamoto H, Pucsok J, Sasvari M, Nyakas C, Goto S (2001) Regular exercise improves cognitive function and decreases oxidative damage in rat brain. Neurochem Int 38 : 17 23.
82. Redila VA, Christie BR (2006) Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus. Neuroscience 137 : 1299 1307.
83. Redila VA, Olson AK, Swann SE, Mohades G, Webber AJ, Weinberg J, Christie BR (2006) Hippocampal cell proliferation is reduced following prenatal ethanol exposure but can be rescued with voluntary exercise. Hippocampus 16 : 305 311.
84. Reifman A, Watson WK (2003) Binge drinking during the first semester of college: continuation and desistance from high school patterns. J Am Coll Health 52 : 73 81.
85. Renis M, Calabrese V, Russo A, Calderone A, Barcellona ML, Rizza V (1996) Nuclear DNA strand breaks during ethanol-induced oxidative stress in rat brain. FEBS Lett 390 : 153 156.
86. Revest JM, Dupret D, Koehl M, Funk-Reiter C, Grosjean N, Piazza PV, Abrous DN (2009) Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Mol Psychiatry 14 : 959 967.
87. Russo-Neustadt AA, Beard RC, Huang YM, Cotman CW (2000) Physical activity and antidepressant treatment potentiate the exression of specific brain-derived neurotrophic factor transcripts in the rat hippocampus. Neuroscience 101 : 305 312.
88. Schmued LC, Hopkins KJ (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874 : 123 130.
89. Scholzen T, Gerdes J (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182 : 311 322.
90. Schuckit MA, Monteiro MG (1988) Alcoholism, anxiety and depression. Br J Addict 83 : 1373 1380.
91. Siler-Marsiglio KI, Pan Q, Paiva M, Madorsky I, Khurana NC, Heaton MB (2005) Mitochondrially targeted vitamin E and vitamin E mitigate ethanol-mediated effects on cerebellar granule cell antioxidant defense systems. Brain Res 1052 : 202 211.
92. Siler-Marsiglio KI, Shaw G, Heaton MB (2004) Pycnogenol and vitamin E inhibit ethanol-induced apoptosis in rat cerebellar granule cells. J Neurobiol 59 : 261 271.
93. Skalicky M, Viidik A (1999) Comparison between continuous and intermittent physical exercise on aging rats: changes in patterns of spontaneous activity and connective tissue stability. Aging (Milano) 11 : 227 234.
94. Somani SM, Ravi R, Rybak LP (1995) Effect of exercise training on antioxidant system in brain regions of rat. Pharmacol Biochem Behav 50 : 635 639.
95. 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.
96. Sullivan EV, Marsh L, Mathalon DH, Lim KO, Pfefferbaum A (1995) Anterior hippocampal volume deficits in nonamnesic, aging chronic alcoholics. Alcohol Clin Exp Res 19 : 110 122.
97. Sullivan EV, Pfefferbaum A (2005) Neurocircuitry in alcoholism: a substrate of disruption and repair. Psychopharmacology 180 : 583 594.
98. 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.
99. Tanapat P, Hastings NB, Reeves AJ, Gould E (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19 : 5792 5801.
100. Thomas JD, Sather TM, Whinery LA (2008) Voluntary exercise influences behavioral development in rats exposed to alcohol during the neonatal brain growth spurt. Behav Neurosci 122 : 1264 1273.
101. Thome J, Foley P, Gsell W, Davids E, Wodarz N, Wiesbeck GA, Boning J, Riederer P (1997a) Increased concentrations of manganese superoxide dismutase in serum of alcohol-dependent patients. Alcohol Alcohol 32 : 65 69. (Pubitemid 27092455)
102. Thome J, Nara K, Foley P, Gsell W, Wiesbeck GA, Boning J, Riederer P (1997b) Time course of manganese superoxide dismutase concentrations in serum of alcohol-dependent patients during abstinence. Drug Alcohol Depend 44 : 151 155. (Pubitemid 27129508)
103. Thome J, Zhang J, Davids E, Foley P, Weijers HG, Wiesbeck GA, Boning J, Riederer P, Gerlach M (1997c) Evidence for increased oxidative stress in alcohol-dependent patients provided by quantification of in vivo salicylate hydroxylation products. Alcohol Clin Exp Res 21 : 82 85.
104. Thoren P, Floras JS, Hoffmann P, Seals DR (1990) Endorphins and exercise: physiological mechanisms and clinical implications. Med Sci Sports Exerc 22 : 417 428.
105. Tivis R, Beatty WW, Nixon SJ, Parsons OA (1995) Patterns of cognitive impairment among alcoholics: are there subtypes? Alcohol Clin Exp Res 19 : 496 500.
106. Ussher M, Sampuran AK, Doshi R, West R, Drummond DC (2004) Acute effect of a brief bout of exercise on alcohol urges. Addiction 99 : 1542 1547.
107. 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.
108. 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.
109. Walker DW, Barnes DE, Zornetzer SF, Hunter BE, Kubanis P (1980) Neuronal loss in hippocampus induced by prolonged ethanol consumption in rats. Science 209 : 711 713.
110. West MJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231 : 482 497.
111. Widenfalk J, Olson L, Thoren P (1999) Deprived of habitual running, rats downregulate BDNF and TrkB messages in the brain. Neurosci Res 34 : 125 132.