Alcohol and adult hippocampal neurogenesis: Promiscuous drug, wanton effects

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 54, Issue , 2014, Pages 103-113

  Geil, Chelsea R ^a   Hayes, Dayna M ^a   McClain, Justin A ^a   Liput, Daniel J ^a   Marshall, S Alex ^a   Chen, Kevin Y ^a   Nixon, Kimberly ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Adult neurogenesis; Alcoholism; Ethanol; Hippocampus; Neural stem cells

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ACETYLCHOLINE; ALCOHOL; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ENDOCANNABINOID; FATTY ACID AMIDASE; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROPEPTIDE Y; SEROTONIN RECEPTOR; CENTRAL DEPRESSANT AGENT;

ALCOHOL CONSUMPTION; ALCOHOL INTOXICATION; ALCOHOL USE DISORDER; ALCOHOLISM; ASTROCYTE; BRAIN FUNCTION; CELL ACTIVATION; CELL DAMAGE; CELL DEATH; CELL DIFFERENTIATION; CELL LOSS; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; DENTATE GYRUS; EXECUTIVE FUNCTION; GRAY MATTER; HIPPOCAMPUS; HUMAN; INTRACELLULAR SIGNALING; MICROGLIA; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROPATHOLOGY; NEUROTRANSMISSION; NONHUMAN; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; REVIEW; ANIMAL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; PATHOPHYSIOLOGY; PHYSIOLOGY;

ALCOHOL-RELATED DISORDERS; ANIMALS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ETHANOL; HIPPOCAMPUS; HUMANS; NEUROGENESIS;

EID: 84902511173     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2014.05.003     Document Type: Review

References (226)

1. Aberg E., Hofstetter C.P., Olson L., Brene S. Moderate ethanol consumption increases hippocampal cell proliferation and neurogenesis in the adult mouse. Int J Neuropsychopharmacol 2005, 8:557-567.
2. Agartz I., Momenan R., Rawlings R.R., Kerich M.J., Hommer D.W. Hippocampal volume in patients with alcohol dependence. Arch Gen Psychiatry 1999, 56:356-363.
3. Agrawal R.G., Hewetson A., George C.M., Syapin P.J., Bergeson S.E. Minocycline reduces ethanol drinking. Brain Behav Immun 2011, 25(Suppl. 1):S165-S169.
4. Aguado T., Monory K., Palazuelos J., Stella N., Cravatt B., Lutz B., et al. The endocannabinoid system drives neural progenitor proliferation. FASEB J 2005, 12:1704-1706.
5. Aguado T., Romero E., Monory K., Palazuelos J., Sendtner M., Marsicano G., et al. The CB1 cannabinoid receptor mediates excitotoxicity-induced neural progenitor proliferation and neurogenesis. J Biol Chem 2007, 282:23892-23898.
6. Altman J., Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965, 124:319-335.
7. Alvarez-Buylla A., Lim D.A. For the long run: maintaining germinal niches in the adult brain. Neuron 2004, 41:683-686.
8. Anderson M.L., Nokia M.S., Govindaraju K.P., Shors T.J. Moderate drinking? Alcohol consumption significantly decreases neurogenesis in the adult hippocampus. Neuroscience 2012, 224:202-209.
9. Armstrong R.J., Barker R.A. Neurodegeneration: a failure of neuroregeneration?. Lancet 2001, 358:1174-1176.
10. Arnone M., Maruani J., Chaperon F., Thiebot M.H., Poncelet M., Soubrie P., et al. Selective inhibition of sucrose and ethanol intake by SR 141716, an antagonist of central cannabinoid (CB1) receptors. Psychopharmacology (Berl) 1997, 132:104-106.
11. Baek J.K., Heaton M.B., Walker D.W. Up-regulation of high-affinity neurotrophin receptor, TrkB-like protein on western blots of rat cortex after chronic ethanol treatment. Brain Res Mol Brain Res 1996, 40:161-164.
12. Bartels C., Kunert H.J., Stawicki S., Kroner-Herwig B., Ehrenreich H., Krampe H. Recovery of hippocampus-related functions in chronic alcoholics during monitored long-term abstinence. Alcohol Alcohol 2007, 42:92-102.
13. Battista D., Ferrari C.C., Gage F.H., Pitossi F.J. Neurogenic niche modulation by activated microglia: transforming growth factor beta increases neurogenesis in the adult dentate gyrus. Eur J Neurosci 2006, 23:83-93.
14. Baydas G., Tuzcu M. Protective effects of melatonin against ethanol-induced reactive gliosis in hippocampus and cortex of young and aged rats. Exp Neurol 2005, 194:175-181.
15. Belujon P., Grace A.A. Hippocampus, amygdala, and stress: interacting systems that affect susceptibility to addiction. Ann N Y Acad Sci 2011, 1216:114-121.
16. Bengochea O., Gonzalo L.M. Effect of chronic alcoholism on the human hippocampus. Histol Histopathol 1990, 5:349-357.
17. Beresford T.P., Arciniegas D.B., Alfers J., Clapp L., Martin B., Du Y., et al. Hippocampus volume loss due to chronic heavy drinking. Alcohol Clin Exp Res 2006, 30:1866-1870.
18. Bergmann O., Liebl J., Bernard S., Alkass K., Yeung M.S., Steier P., et al. The age of olfactory bulb neurons in humans. Neuron 2012, 74:634-639.
19. Bison S., Crews F. Alcohol withdrawal increases neuropeptide Y immunoreactivity in rat brain. Alcohol Clin Exp Res 2003, 27:1173-1183.
20. Blednov Y.A., Benavidez J.M., Geil C., Perra S., Morikawa H., Harris R.A. Activation of inflammatory signaling by lipopolysaccharide produces a prolonged increase of voluntary alcohol intake in mice. Brain Behav Immun 2011, 25(Suppl. 1):S92-S105.
21. Bonaguidi M.A., Wheeler M.A., Shapiro J.S., Stadel R.P., Sun G.J., Ming G.L., et al. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 2011, 145:1142-1155.
22. Bonaguidi M.A., Song J., Ming G.L., Song H. A unifying hypothesis on mammalian neural stem cell properties in the adult hippocampus. Curr Opin Neurobiol 2012, 22:754-761.
23. Bouchery E.E., Harwood H.J., Sacks J.J., Simon C.J., Brewer R.D. Economic costs of excessive alcohol consumption in the U.S., 2006. Am J Prev Med 2011, 41:516-524.
24. Briones T.L., Woods J. Chronic binge-like alcohol consumption in adolescence causes depression-like symptoms possibly mediated by the effects of BDNF on neurogenesis. Neuroscience 2013, 254:324-334.
25. Bruel-Jungerman E., Davis S., Rampon C., Laroche S. Long-term potentiation enhances neurogenesis in the adult dentate gyrus. J Neurosci 2006, 26:5888-5893.
26. Bruel-Jungerman E., Lucassen P.J., Francis F. Cholinergic influences on cortical development and adult neurogenesis. Behav Brain Res 2011, 221:379-388.
27. Buffo A., Rite I., Tripathi P., Lepier A., Colak D., Horn A.P., et al. Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain. Proc Natl Acad Sci U S A 2008, 105:3581-3586.
28. Cadete-Leite A., Tavares M.A., Uylings H.B., Paula-Barbosa M. Granule cell loss and dendritic regrowth in the hippocampal dentate gyrus of the rat after chronic alcohol consumption. Brain Res 1988, 473:1-14.
29. Cadete-Leite A., Tavares M.A., Alves M.C., Uylings H.B., Paula-Barbosa M.M. Metric analysis of hippocampal granule cell dendritic trees after alcohol withdrawal in rats. Alcohol Clin Exp Res 1989, 13:837-840.
30. Cameron H.A., McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 2001, 435:406-417.
31. Cameron H.A., McEwen B.S., Gould E. Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 1995, 15:4687-4692.
32. Cameron H.A., Hazel T.G., McKay R.D. Regulation of neurogenesis by growth factors and neurotransmitters. J Neurobiol 1998, 36:287-306.
33. Carlen P.L., Wortzman G., Holgate R.C., Wilkinson D.A., Rankin J.C. Reversible cerebral atrophy in recently abstinent chronic alcoholics measured by computed tomography scans. Science 1978, 200:1076-1078.
34. Chanraud S., Martelli C., Delain F., Kostogianni N., Douaud G., Aubin H.J., et al. Brain morphometry and cognitive performance in detoxified alcohol-dependents with preserved psychosocial functioning. Neuropsychopharmacology 2007, 32:429-438.
35. Clark D.B., Bukstein O., Cornelius J. Alcohol use disorders in adolescents: epidemiology, diagnosis, psychosocial interventions, and pharmacological treatment. Paediatr Drugs 2002, 4:493-502.
36. Clelland C.D., Choi M., Romberg C., Clemenson G.D., Fragniere A., Tyers P., et al. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009, 325:210-213.
37. Collins M.A., Corse T.D., Neafsey E.J. 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 1996, 20:284-292.
38. Colton C., Wilcock D.M. Assessing activation states in microglia. CNS Neurol Disord Drug Targets 2010, 9:174-191.
39. Conover J.C., Notti R.Q. The neural stem cell niche. Cell Tissue Res 2008, 331:211-224.
40. Contet C., Kim A., Le D., Iyengar S.K., Kotzebue R.W., Yuan C.J., et al. mu-Opioid receptors mediate the effects of chronic ethanol binge drinking on the hippocampal neurogenic niche. Addict Biol 2014, [in press]. 10.1111/adb.12040.
41. Corvino V., Marchese E., Giannetti S., Lattanzi W., Bonvissuto D., Biamonte F., et al. The neuroprotective and neurogenic effects of neuropeptide Y administration in an animal model of hippocampal neurodegeneration and temporal lobe epilepsy induced by trimethyltin. J Neurochem 2012, 122:415-426.
42. Costa M., Girard M., Dalmay F., Malauzat D. Brain-derived neurotrophic factor serum levels in alcohol-dependent subjects 6months after alcohol withdrawal. Alcohol Clin Exp Res 2011, 35:1966-1973.
43. Crews F.T. Alcohol and neurodegeneration. CNS Drug Rev 1999, 5:379-394.
44. Crews F.T. Immune function genes, genetics, and the neurobiology of addiction. Alcohol Res 2012, 34(3):355-361.
45. Crews F.T., Nixon K. Alcohol, neural stem cells, and adult neurogenesis. Alcohol Res Health 2003, 27:197-204.
46. Crews F.T., Nixon K. Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcohol 2009, 44:115-127.
47. Crews F.T., Braun C.J., Hoplight B., Switzer R.C., Knapp D.J. Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. Alcohol Clin Exp Res 2000, 24:1712-1723.
48. Crews F., Nixon K., Kim D., Joseph J., Shukitt-Hale B., Qin L., et al. BHT blocks NF-kappaB activation and ethanol-induced brain damage. Alcohol Clin Exp Res 2006, 30:1938-1949.
49. Crews F.T., Mdzinarishvili A., Kim D., He J., Nixon K. Neurogenesis in adolescent brain is potently inhibited by ethanol. Neuroscience 2006, 137:437-445.
50. Crews F.T., Nixon K., Kim D.H., Qin L., Shukitt-Hale B., Josephs J.A. BHT blocks NFkB activation and ethanol-induced brain damage. Alcohol Clin Exp Res 2006, 30:1938-1949.
51. Crews F.T., Zou J., Qin L. Induction of innate immune genes in brain create the neurobiology of addiction. Brain Behav Immun 2011, 25(Suppl. 1):S4-S12.
52. Dalcik H., Yardimoglu M., Filiz S., Gonca S., Dalcik C., Erden B.F. Chronic ethanol-induced glial fibrillary acidic protein (GFAP) immunoreactivity: an immunocytochemical observation in various regions of adult rat brain. Int J Neurosci 2009, 119:1303-1318.
53. Davis M.I. Ethanol-BDNF interactions: still more questions than answers. Pharmacol Ther 2008, 118:36-57.
54. De Bellis M.D., Clark D.B., Beers S.R., Soloff P.H., Boring A.M., Hall J., et al. Hippocampal volume in adolescent-onset alcohol use disorders. Am J Psychiatry 2000, 157:737-744.
55. Deboy C.A., Xin J., Byram S.C., Serpe C.J., Sanders V.M., Jones K.J. Immune-mediated neuroprotection of axotomized mouse facial motoneurons is dependent on the IL-4/STAT6 signaling pathway in CD4(+) T cells. Exp Neurol 2006, 201:212-224.
56. Decressac M., Wright B., David B., Tyers P., Jaber M., Barker R.A., et al. Exogenous neuropeptide Y promotes in vivo hippocampal neurogenesis. Hippocampus 2011, 21:233-238.
57. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999, 97:703-716.
58. Dranovsky A., Picchini A.M., Moadel T., Sisti A.C., Yamada A., Kimura S., et al. Experience dictates stem cell fate in the adult hippocampus. Neuron 2011, 70:908-923.
59. Durand D., Saint-Cyr J.A., Gurevich N., Carlen P.L. Ethanol-induced dendritic alterations in hippocampal granule cells. Brain Res 1989, 477:373-377.
60. Eckardt M.J., Martin P.R. Clinical assessment of cognition in alcoholism. Alcohol Clin Exp Res 1986, 10:123-127.
61. Eichenbaum H. The hippocampus and declarative memory: cognitive mechanisms and neural codes. Behav Brain Res 2001, 127:199-207.
62. Ekdahl C.T., Kokaia Z., Lindvall O. Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 2009, 158:1021-1029.
63. Encinas J.M., Michurina T.V., Peunova N., Park J.H., Tordo J., Peterson D.A., et al. Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 2011, 8:566-579.
64. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., et al. Neurogenesis in the adult human hippocampus. Nat Med 1998, 4:1313-1317.
65. Esposito M.S., Piatti V.C., Laplagne D.A., Morgenstern N.A., Ferrari C.C., Pitossi F.J., et al. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 2005, 25:10074-10086.
66. Evrard S.G., Duhalde-Vega M., Tagliaferro P., Mirochnic S., Caltana L.R., Brusco A. A low chronic ethanol exposure induces morphological changes in the adolescent rat brain that are not fully recovered even after a long abstinence: an immunohistochemical study. Exp Neurol 2006, 200:438-459.
67. Fadda F., Rossetti Z. Chronic ethanol consumption: from neuroadaptation to neurodegeneration. Prog Neurobiol 1998, 56:385-431.
68. Franke H. Influence of chronic alcohol treatment on the GFAP-immunoreactivity in astrocytes of the hippocampus in rats. Acta Histochem 1995, 97:263-271.
69. Gage F.H. Mammalian neural stem cells. Science 2000, 287:1433-1438.
70. Gazdzinski S., Durazzo T.C., Meyerhoff D.J. Temporal dynamics and determinants of whole brain tissue volume changes during recovery from alcohol dependence. Drug Alcohol Depend 2005, 78:263-273.
71. Ge S., Goh E.L., Sailor K.A., Kitabatake Y., Ming G.L., Song H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 2006, 439:589-593.
72. Gilbert P.E., Kesner R.P. The role of the dorsal CA3 hippocampal subregion in spatial working memory and pattern separation. Behav Brain Res 2006, 169:142-149.
73. Godsil B.P., Kiss J.P., Spedding M., Jay T.M. The hippocampal-prefrontal pathway: the weak link in psychiatric disorders?. Eur Neuropsychopharmacol 2013, 23:1165-1181.
74. Goodlett C.R., Horn K.H., Zhou F.C. Alcohol teratogenesis: mechanisms of damage and strategies for intervention. Exp Biol Med (Maywood) 2005, 230:394-406.
75. Graeber M.B., Li W., Rodriguez M.L. Role of microglia in CNS inflammation. FEBS Lett 2011, 585:3798-3805.
76. Grant B.F., Dawson D.A., Stinson F.S., Chou S.P., Dufour M.C., Pickering R.P. The 12-month prevalence and trends in DSM-IV alcohol abuse and dependence: United States, 1991-1992 and 2001-2002. Drug Alcohol Depend 2004, 74:223-234.
77. Gray W.P. Neuropeptide Y signalling on hippocampal stem cells in health and disease. Mol Cell Endocrinol 2008, 288:52-62.
78. Grobin A.C., Matthews D.B., Montoya D., Wilson W.A., Morrow A.L., Swartzwelder H.S. Age-related differences in neurosteroid potentiation of muscimol-stimulated 36Cl(-) flux following chronic ethanol treatment. Neuroscience 2001, 105:547-552.
79. Gross C.G. Neurogenesis in the adult brain: death of a dogma. Nat Rev Neurosci 2000, 1:67-73.
80. Hansson A.C., Nixon K., Rimondini R., Damadzic R., Sommer W.H., Eskay R., et al. Long-term suppression of forebrain neurogenesis and loss of neuronal progenitor cells following prolonged alcohol dependence in rats. Int J Neuropsychopharmacol 2010, 13:583-593.
81. Harding A.J., Wong A., Svoboda M., Kril J.J., Halliday G.M. Chronic alcohol consumption does not cause hippocampal neuron loss in humans. Hippocampus 1997, 7:78-87.
82. Hauser S.R., Getachew B., Taylor R.E., Tizabi Y. Alcohol induced depressive-like behavior is associated with a reduction in hippocampal BDNF. Pharmacol Biochem Behav 2011, 100:253-258.
83. Hayes D.M., Deeny M.A., Shaner C.A., Nixon K. Determining the threshold for alcohol-induced brain damage: new evidence with gliosis markers. Alcohol Clin Exp Res 2013, 37:425-434.
84. He J., Crews F.T. Increased MCP-1 and microglia in various regions of the human alcoholic brain. Exp Neurol 2008, 210:349-358.
85. He J., Nixon K., Shetty A.K., Crews F.T. Chronic alcohol exposure reduces hippocampal neurogenesis and dendritic growth of newborn neurons. Eur J Neurosci 2005, 21:2711-2720.
86. He J., Overstreet D.H., Crews F.T. Abstinence from moderate alcohol self-administration alters progenitor cell proliferation and differentiation in multiple brain regions of male and female P rats. Alcohol Clin Exp Res 2009, 33:129-138.
87. Hensler J.G., Ladenheim E.E., Lyons W.E. Ethanol consumption and serotonin-1A (5-HT1A) receptor function in heterozygous BDNF (+/-) mice. J Neurochem 2003, 85:1139-1147.
88. Herrera D.G., Yague A.G., Johnsen-Soriano S., Bosch-Morell F., Collado-Morente L., Muriach M., et al. Selective impairment of hippocampal neurogenesis by chronic alcoholism: protective effects of an antioxidant. Proc Natl Acad Sci U S A 2003, 100:7919-7924.
89. Hill M.N., Titterness A.K., Morrish A.C., Carrier E.J., Lee T.T.Y., Gil-Mohapel J., et al. Endogenous cannabinoid signaling is required for voluntary exercise-induced enhancement of progenitor cell proliferation in the hippocampus. Hippocampus 2010, 20:513-523.
90. Hoffman P.L. NMDA receptors in alcoholism. International Review of Neurobiology 2003, 35-82. Academic Press.
91. Howell O.W., Silva S., Scharfman H.E., Sosunov A.A., Zaben M., Shatya A., et al. Neuropeptide Y is important for basal and seizure-induced precursor cell proliferation in the hippocampus. Neurobiol Dis 2007, 26:174-188.
92. Hunt W.A. Are binge drinkers more at risk of developing brain damage?. Alcohol 1993, 10:559-561.
93. Hyman S.E., Malenka R.C., Nestler E.J. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 2006, 29:565-598.
94. Imayoshi I., Sakamoto M., Ohtsuka T., Takao K., Miyakawa T., Yamaguchi M., et al. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 2008, 11:1153-1161.
95. Jang M.-H., Shin M.-C., Jung S.-B., Lee T.-H., Bahn G.-H., Kwon Y.K., et al. Alcohol and nicotine reduce cell proliferation and enhance apoptosis in dentate gyrus. Neuroreport 2002, 13:1509-1513.
96. Jin K., Xie L., Kim S.H., Parmentier-Batteur S., Sun Y., Mao X.O., et al. Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Mol Pharmacol 2004, 66:204-208.
97. Johnson A., van der Meer M.A., Redish A.D. Integrating hippocampus and striatum in decision-making. Curr Opin Neurobiol 2007, 17:692-697.
98. Kalkman H.O. Altered growth factor signaling pathways as the basis of aberrant stem cell maturation in schizophrenia. Pharmacol Ther 2009, 121:115-122.
99. Kaplan M.S., Hinds J.W. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 1977, 197:1092-1094.
100. Kelso M.L., Liput D.J., Eaves D.W., Nixon K. Upregulated vimentin suggests new areas of neurodegeneration in a model of an alcohol use disorder. Neuroscience 2011, 197:381-393.
101. Kempermann G. New neurons for 'survival of the fittest'. Nat Rev Neurosci 2012, 13:727-736.
102. Kempermann G., Gage F.H. Genetic influence on phenotypic differentiation in adult hippocampal neurogenesis. Brain Res Dev Brain Res 2002, 134:1-12.
103. Kim S.H., Won S.J., Mao X.O., Ledent C., Jin K., Greenberg D.A. Role for neuronal nitric-oxide synthase in cannabinoid-induced neurogenesis. J Pharmacol Exp Ther 2006, 319:150-154.
104. King M.A., Hunter B.E., Walker D.W. Alterations and recovery of dendritic spine density in rat hippocampus following long-term ethanol ingestion. Brain Res 1988, 459:381-385.
105. Kiyota T., Ingraham K.L., Swan R.J., Jacobsen M.T., Andrews S.J., Ikezu T. AAV serotype 2/1-mediated gene delivery of anti-inflammatory interleukin-10 enhances neurogenesis and cognitive function in APP+PS1 mice. Gene Ther 2012, 19:724-733.
106. Knapp D.J., Crews F.T. Induction of cyclooxygenase-2 in brain during acute and chronic ethanol treatment and ethanol withdrawal. Alcohol Clin Exp Res 1999, 23:633-643.
107. Knapp D.J., Duncan G.E., Crews F.T., Breese G.R. Induction of Fos-like rroteins and ultrasonic vocalizations during ethanol withdrawal: further evidence for withdrawal-induced anxiety. Alcohol Clin Exp Res 1998, 22:481-493.
108. Köhler S., Klimke S., Hellweg R., Lang U.E. Serum brain-derived neurotrophic factor and nerve growth factor concentrations change after alcohol withdrawal: preliminary data of a case-control comparison. Eur Addict Res 2013, 19:98-104.
109. Koo J.W., Duman R.S. IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci U S A 2008, 105:751-756.
110. Koob G.F., Le Moal M. Drug abuse: hedonic homeostatic dysregulation. Science 1997, 278:52-58.
111. Korbo L. Glial cell loss in the hippocampus of alcoholics. Alcohol Clin Exp Res 1999, 23:164-168.
112. Laakso M.P., Vaurio O., Savolainen L., Repo E., Soininen H., Aronen H.J., et al. A volumetric MRI study of the hippocampus in type 1 and 2 alcoholism. Behav Brain Res 2000, 109:177-186.
113. Leasure J.L., Nixon K. Exercise neuroprotection in a rat model of binge alcohol consumption. Alcohol Clin Exp Res 2010, 34:404-414.
114. Lee J., Duan W., Mattson M.P. Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem 2002, 82:1367-1375.
115. Lewohl J.M., Wilson W.R., Mayfield R.D., Brozowski S.J., Morrisett R.A., Harris R.A. G-protein-coupled inwardly rectifying potassium channels are targets of alcohol action. Nat Neurosci 1999, 2:1084-1090.
116. Livy D.J., Parnell S.E., West J.R. Blood ethanol concentration profiles: a comparison between rats and mice. Alcohol 2003, 29:165-171.
117. Lovinger D.M. 5-HT3 receptors and the neural actions of alcohols: an increasingly exciting topic. Neurochem Int 1999, 35:125-130.
118. Lovinger D.M., White G., Weight F.F. Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science 1989, 243:1721-1724.
119. Lukoyanov N.V., Brandao F., Cadete-Leite A., Madeira M.D., Paula-Barbosa M.M. Synaptic reorganization in the hippocampal formation of alcohol-fed rats may compensate for functional deficits related to neuronal loss. Alcohol 2000, 20:139-148.
120. MacLennan A.J., Lee N., Walker D.W. Chronic ethanol administration decreases brain-derived neurotrophic factor gene expression in the rat hippocampus. Neurosci Lett 1995, 197:105-108.
121. Madsen T.M., Kristjansen P.E., Bolwig T.G., Wortwein G. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 2003, 119:635-642.
122. Maekawa M., Namba T., Suzuki E., Yuasa S., Kohsaka S., Uchino S. NMDA receptor antagonist memantine promotes cell proliferation and production of mature granule neurons in the adult hippocampus. Neurosci Res 2009, 63:259-266.
123. Magavi S.S., Leavitt B.R., Macklis J.D. Induction of neurogenesis in the neocortex of adult mice. Nature 2000, 405:951-955.
124. Malva J.O., Xapelli S., Baptista S., Valero J., Agasse F., Ferreira R., et al. Multifaces of neuropeptide Y in the brain-neuroprotection, neurogenesis and neuroinflammation. Neuropeptides 2012, 46:299-308.
125. Mandyam C.D., Koob G.F. The addicted brain craves new neurons: putative role for adult-born progenitors in promoting recovery. Trends Neurosci 2012, 35:250-260.
126. Mann K., Gunther A., Stetter F., Ackermann K. Rapid recovery from cognitive deficits in abstinent alcoholics: a controlled test-retest study. Alcohol Alcohol 1999, 34:567-574.
127. Mantamadiotis T., Papalexis N., Dworkin S. CREB signalling in neural stem/progenitor cells: recent developments and the implications for brain tumour biology. Bioessays 2012, 34:293-300.
128. Marchalant Y., Brothers H.M., Norman G.J., Karelina K., DeVries A.C., Wenk G.L. Cannabinoids attenuate the effects of aging upon neuroinflammation and neurogenesis. Neurobiol Dis 2009, 34:300-307.
129. Marin-Burgin A., Schinder A.F. Requirement of adult-born neurons for hippocampus-dependent learning. Behav Brain Res 2012, 227:391-399.
130. Marshall S.A., McClain J.A., Kelso M.L., Hopkins D.M., Pauly J.R., Nixon K. Microglial activation is not equivalent to neuroinflammation in alcohol-induced neurodegeneration: the importance of microglia phenotype. Neurobiol Dis 2013, 8. [00007-7].
131. Martinotti G., Di Iorio G., Marini S., Ricci V., De Berardis D., Di Giannantonio M. Nerve growth factor and brain-derived neurotrophic factor concentrations in schizophrenia: a review. J Biol Regul Homeost Agents 2012, 3:347-356.
132. Matsumoto I., Leah J., Shanley B., Wilce P. Immediate early gene expression in the rat brain during ethanol withdrawal. Mol Cell Neurosci 1993, 4:485-491.
133. McClain J.A., Hayes D.M., Morris S.A., Nixon K. Adolescent binge alcohol exposure alters hippocampal progenitor cell proliferation in rats: effects on cell cycle kinetics. J Comp Neurol 2011, 519:2697-2710.
134. McClain J.A., Morris S.A., Deeny M.A., Marshall S.A., Hayes D.M., Kiser Z.M., et al. Adolescent binge alcohol exposure induces long-lasting partial activation of microglia. Brain Behav Immun 2011, 25(Suppl. 1):S120-S128.
135. McClain J.A., Morris S.A., Marshall S.A., Nixon K. Ectopic hippocampal neurogenesis in adolescent male rats following alcohol dependence. Addict Biol 2014, [in press]. 10.1111/adb.12075.
136. Mechtcheriakov S., Brenneis C., Egger K., Koppelstaetter F., Schocke M., Marksteiner J. A widespread distinct pattern of cerebral atrophy in patients with alcohol addiction revealed by voxel-based morphometry. J Neurol Neurosurg Psychiatry 2007, 78:610-614.
137. Meshi D., Drew M.R., Saxe M., Ansorge M.S., David D., Santarelli L., et al. Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat Neurosci 2006, 9:729-731.
138. Miller H.L., Delgado P.L., Salomon R.M., Berman R., Krystal J.H., Heninger G.R., et al. Clinical and biochemical effects of catecholamine depletion on antidepressant-induced remission of depression. Arch Gen Psychiatry 1996, 53:117-128.
139. Miller R., King M.A., Heaton M.B., Walker D.W. The effects of chronic ethanol consumption on neurotrophins and their receptors in the rat hippocampus and basal forebrain. Brain Res 2002, 950:137-147.
140. Mitrirattanakul S., López-Valdés H.E., Liang J., Matsuka Y., Mackie K., Faull K.F., et al. Bidirectional alterations of hippocampal cannabinoid 1 receptors and their endogenous ligands in a rat model of alcohol withdrawal and dependence. Alcohol Clin Exp Res 2007, 31:855-867.
141. Mokdad A.H., Marks J.S., Stroup D.F., Gerberding J.L. Actual causes of death in the United States, 2000. JAMA 2004, 291:1238-1245.
142. Monje M.L., Toda H., Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003, 302:1760-1765.
143. Moonat S., Starkman B.G., Sakharkar A., Pandey S.C. Neuroscience of alcoholism: molecular and cellular mechanisms. Cell Mol Life Sci 2010, 67:73-88.
144. Morris S.A., Eaves D.W., Smith A.R., Nixon K. Alcohol inhibition of neurogenesis: a mechanism of hippocampal neurodegeneration in an adolescent alcohol abuse model. Hippocampus 2010, 20:596-607.
145. Morshead C.M., Reynolds B.A., Craig C.G., McBurney M.W., Staines W.A., Morassutti D., et al. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 1994, 13:1071-1082.
146. Murphy J.B., Sturm E. Conditions determining the transplantability of tissues in the brain. J Exp Med 1923, 38:183-197.
147. Nacher J., Rosell D.R., Alonso-Llosa G., McEwen B.S. NMDA receptor antagonist treatment induces a long-lasting increase in the number of proliferating cells, PSA-NCAM-immunoreactive granule neurons and radial glia in the adult rat dentate gyrus. Eur J Neurosci 2001, 13:512-520.
148. Nacher J., Varea E., Miguel Blasco-Ibanez J., Gomez-Climent M.A., Castillo-Gomez E., Crespo C., et al. N-methyl-d-aspartate receptor expression during adult neurogenesis in the rat dentate gyrus. Neuroscience 2007, 144:855-864.
149. Nagel B.J., Schweinsburg A.D., Phan V., Tapert S.F. Reduced hippocampal volume among adolescents with alcohol use disorders without psychiatric comorbidity. Psychiatry Res 2005, 139:181-190.
150. Nakagawa S., Kim J.E., Lee R., Chen J., Fujioka T., Malberg J., et al. Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. J Neurosci 2002, 22:9868-9876.
151. Nakagawa S., Kim J.E., Lee R., Malberg J.E., Chen J., Steffen C., et al. Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J Neurosci 2002, 22:3673-3682.
152. Nakashiba T., Cushman J.D., Pelkey K.A., Renaudineau S., Buhl D.L., McHugh T.J., et al. Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 2012, 149:188-201.
153. Neuwelt E.A., Clark W.K. Unique aspects of central nervous system immunology. Neurosurgery 1978, 3:419-430.
154. Nixon K. Alcohol and adult neurogenesis: roles in neurodegeneration and recovery in chronic alcoholism. Hippocampus 2006, 16:287-295.
155. Nixon K., Crews F.T. Binge ethanol exposure decreases neurogenesis in adult rat hippocampus. J Neurochem 2002, 83:1087-1093.
156. Nixon K., Crews F.T. Temporally specific burst in cell proliferation increases hippocampal neurogenesis in protracted abstinence from alcohol. J Neurosci 2004, 24:9714-9722.
157. Nixon K., Kim D.H., Potts E.N., He J., Crews F.T. Distinct cell proliferation events during abstinence after alcohol dependence: microglia proliferation precedes neurogenesis. Neurobiol Dis 2008, 31:218-229.
158. Nixon K., Morris S.A., Liput D.J., Kelso M.L. Roles of neural stem cells and adult neurogenesis in adolescent alcohol use disorders. Alcohol 2010, 44:39-56.
159. Nixon K., Pauly J.R., Hayes D.M. Alcohol, nicotine, and adult neurogenesis. Drug addiction and adult neurogenesis 2011, 95-119. Research Signpost, Kerala, India. M.F. Olive (Ed.).
160. Noel X., Brevers D., Bechara A. A neurocognitive approach to understanding the neurobiology of addiction. Curr Opin Neurobiol 2013, 23:632-638.
161. Obernier J.A., Bouldin T.W., Crews F.T. Binge ethanol exposure in adult rats causes necrotic cell death. Alcohol Clin Exp Res 2002, 26:547-557.
162. Obernier J.A., White A.M., Swartzwelder H.S., Crews F.T. Cognitive deficits and CNS damage after a 4-day binge ethanol exposure in rats. Pharmacol Biochem Behav 2002, 72:521-532.
163. O'Daly O.G., Trick L., Scaife J., Marshall J., Ball D., Phillips M.L., et al. Withdrawal-associated increases and decreases in functional neural connectivity associated with altered emotional regulation in alcoholism. Neuropsychopharmacology 2012, 37:2267-2276.
164. Okamoto H., Miki T., Lee K.Y., Yokoyama T., Kuma H., Gu H., et al. Effects of chronic ethanol administration on the expression levels of neurotrophic factors in the rat hippocampus. Okajimas Folia Anat Jpn 2006, 83:1-6.
165. Overstreet Wadiche L., Bromberg D.A., Bensen A.L., Westbrook G.L. GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol 2005, 94:4528-4532.
166. Ozsoy S., Durak A.C., Esel E. Hippocampal volumes and cognitive functions in adult alcoholic patients with adolescent-onset. Alcohol 2013, 47:9-14.
167. Pachter J.S., de Vries H.E., Fabry Z. The blood-brain barrier and its role in immune privilege in the central nervous system. J Neuropathol Exp Neurol 2003, 62:593-604.
168. Palazuelos J., Aguado T., Egia A., Mechoulam R., Guzmán M., Galve-Roperh I. Non-psychoactive CB2 cannabinoid agonists stimulate neural progenitor proliferation. FASEB J 2006, 20:2405-2407.
169. Palazuelos J., Ortega Z., Díaz-Alonso J., Guzmán M., Galve-Roperh I. CB2 cannabinoid receptors promote neural progenitor cell proliferation via mTORC1 signaling. J Biol Chem 2012, 287:1198-1209.
170. Palmer T.D., Takahashi J., Gage F.H. The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci 1997, 8:389-404.
171. Palmer T.D., Willhoite A.R., Gage F.H. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000, 425:479-494.
172. Pandey S.C., Zhang D., Mittal N., Nayyar D. Potential role of the gene transcription factor cyclic AMP-responsive element binding protein in ethanol withdrawal-related anxiety. J Pharmacol Exp Ther 1999, 288:866-878.
173. Parsons O.A. Impaired neuropsychological cognitive functioning in sober alcoholics. Alcohol-induced brain damage (NIAAA Research Monograph No. 22) 1993, 173-194. National Institutes of Health, Rockville, MD. W.A. Hunt, S.J. Nixon (Eds.).
174. Pava M.J., Woodward J.J. A review of the interactions between alcohol and the endocannabinoid system: implications for alcohol dependence and future directions for research. Alcohol 2012, 46:185-204.
175. Pawlak R., Skrzypiec A., Sulkowski S., Buczko W. Ethanol-induced neurotoxicity is counterbalanced by increased cell proliferation in mouse dentate gyrus. Neurosci Lett 2002, 327:83-86.
176. Pekny M., Wilhelmsson U., Bogestal Y.R., Pekna M. The role of astrocytes and complement system in neural plasticity. Int Rev Neurobiol 2007, 82:95-111.
177. Petrus D.S., Fabel K., Kronenberg G., Winter C., Steiner B., Kempermann G. NMDA and benzodiazepine receptors have synergistic and antagonistic effects on precursor cells in adult hippocampal neurogenesis. Eur J Neurosci 2009, 29:244-252.
178. Pfefferbaum A., Sullivan E.V., Mathalon D.H., Shear P.K., Rosenbloom M.J., Lim K.O. Longitudinal changes in magnetic resonance imaging brain volumes in abstinent and relapsed alcoholics. Alcohol Clin Exp Res 1995, 19:1177-1191.
179. Post R.M. Role of BDNF in bipolar and unipolar disorder: clinical and theoretical implications. J Psychiatr Res 2007, 41:979-990.
180. Qin L., He J., Hanes R.N., Pluzarev O., Hong J.S., Crews F.T. Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. J Neuroinflammation 2008, 5:10.
181. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992, 255:1707-1710.
182. Rice A.C., Bullock M.R., Shelton K.L. Chronic ethanol consumption transiently reduces adult neural progenitor cell proliferation. Brain Res 2004, 1011:94-98.
183. Richardson H.N., Chan S.H., Crawford E.F., Lee Y.K., Funk C.K., Koob G.F., et al. Permanent impairment of birth and survival of cortical and hippocampal proliferating cells following excessive drinking during alcohol dependence. Neurobiol Dis 2009, 36:1-10.
184. Robel S., Berninger B., Gotz M. The stem cell potential of glia: lessons from reactive gliosis. Nat Rev Neurosci 2011, 12:88-104.
185. Robin R.W., Long J.C., Rasmussen J.K., Albaugh B., Goldman D. Relationship of binge drinking to alcohol dependence, other psychiatric disorders, and behavioral problems in an american indian tribe. Alcohol Clin Exp Res 1998, 22:518-523.
186. Russo I., Barlati S., Bosetti F. Effects of neuroinflammation on the regenerative capacity of brain stem cells. J Neurochem 2011, 116:947-956.
187. Saxe M.D., Battaglia F., Wang J.W., Malleret G., David D.J., Monckton J.E., et al. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci U S A 2006, 103:17501-17506.
188. Scharfman H., Goodman J., Macleod A., Phani S., Antonelli C., Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp Neurol 2005, 192:348-356.
189. Schmidt H.D., Duman R.S. The role of neurotrophic factors in adult hippocampal neurogenesis, antidepressant treatments and animal models of depressive-like behavior. Behav Pharmacol 2007, 18:391-418.
190. Schuckit M.A., Monteiro M.G. Alcoholism, anxiety and depression. Br J Addict 1988, 83:1373-1380.
191. Seri B., Garcia-Verdugo J.M., McEwen B.S., Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001, 21:7153-7160.
192. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 2002, 12:578-584.
193. Sofroniew M.V. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 2009, 32:638-647.
194. Song H., Stevens C.F., Gage F.H. Astroglia induce neurogenesis from adult neural stem cells. Nature 2002, 417:39-44.
195. Sperk G., Hamilton T., Colmers W.F. Neuropeptide Y in the dentate gyrus. Progress in brain research 2007, 285-297. Elsevier. E.S. Helen (Ed.).
196. Stavro K., Pelletier J., Potvin S. Widespread and sustained cognitive deficits in alcoholism: a meta-analysis. Addict Biol 2012, 18:203-213.
197. Stephens D.N., Duka T. Cognitive and emotional consequences of binge drinking: role of amygdala and prefrontal cortex. Philos Trans R Soc Lond B Biol Sci 2008, 363:3169-3179.
198. Stevenson J.R., Schroeder J.P., Nixon K., Besheer J., Crews F.T., Hodge C.W. Abstinence following alcohol drinking produces depression-like behavior and reduced hippocampal neurogenesis in mice. Neuropsychopharmacology 2009, 34:1209-1222.
199. Stone S.S.D., Teixeira C.M., DeVito L.M., Zaslavsky K., Josselyn S.A., Lozano A.M., et al. Stimulation of entorhinal cortex promotes adult neurogenesis and facilitates spatial memory. J Neurosci 2011, 31:13469-13484.
200. Sullivan E.V., Pfefferbaum A. Neurocircuitry in alcoholism: a substrate of disruption and repair. Psychopharmacology (Berl) 2005, 180:583-594.
201. Sullivan E.V., Marsh L., Mathalon D.H., Lim K.O., Pfefferbaum A. Anterior hippocampal volume deficits in nonamnesic, aging chronic alcoholics. Alcohol Clin Exp Res 1995, 19:110-122.
202. Taffe M.A., Kotzebue R.W., Crean R.D., Crawford E.F., Edwards S., Mandyam C.D. Long-lasting reduction in hippocampal neurogenesis by alcohol consumption in adolescent nonhuman primates. Proc Natl Acad Sci U S A 2010, 107:11104-11109.
203. Tagliaferro P., Vega M.D., Evrard S.G., Ramos A.J., Brusco A. Alcohol exposure during adulthood induces neuronal and astroglial alterations in the hippocampal CA-1 area. Ann N Y Acad Sci 2002, 965:334-342.
204. Tapia-Arancibia L., Rage F., Givalois L., Dingeon P., Arancibia S., Beauge F. Effects of alcohol on brain-derived neurotrophic factor mRNA expression in discrete regions of the rat hippocampus and hypothalamus. J Neurosci Res 2001, 63:200-208.
205. Tateno M., Saito T. Biological studies on alcohol-induced neuronal damage. Psychiatry Investig 2008, 5:21-27.
206. Taupin P. Adult neural stem cells, neurogenic niches, and cellular therapy. Stem Cell Rev 2006, 2:213-219.
207. Thiele T.E., Marsh D.J., Ste Marie L., Bernstein I.L., Palmiter R.D. Ethanol consumption and resistance are inversely related to neuropeptide Y levels. Nature 1998, 396:366-369.
208. Town T., Nikolic V., Tan J. The microglial "activation" continuum: from innate to adaptive responses. J Neuroinflammation 2005, 2:24.
209. Tozuka Y., Fukuda S., Namba T., Seki T., Hisatsune T. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 2005, 47:803-815.
210. Udomuksorn W., Mukem S., Kumarnsit E., Vongvatcharanon S., Vongvatcharanon U. Effects of alcohol administration during adulthood on parvalbumin and glial fibrillary acidic protein immunoreactivity in the rat cerebral cortex. Acta Histochem 2011, 113:283-289.
211. Valles S.L., Blanco A.M., Pascual M., Guerri C. Chronic ethanol treatment enhances inflammatory mediators and cell death in the brain and in astrocytes. Brain Pathol 2004, 14:365-371.
212. Vallieres L., Campbell I.L., Gage F.H., Sawchenko P.E. Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J Neurosci 2002, 22:486-492.
213. 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.
214. Vangipuram S.D., Lyman W.D. Ethanol alters cell fate of fetal human brain-derived stem and progenitor cells. Alcohol Clin Exp Res 2010, 34:1574-1583.
215. Vengeliene V., Bilbao A., Molander A., Spanagel R. Neuropharmacology of alcohol addiction. Br J Pharmacol 2008, 154:299-315.
216. Vorel S.R., Liu X., Hayes R.J., Spector J.A., Gardner E.L. Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science 2001, 292:1175-1178.
217. Wainwright D.A., Xin J., Mesnard N.A., Beahrs T.R., Politis C.M., Sanders V.M., et al. Exacerbation of facial motoneuron loss after facial nerve axotomy in CCR3-deficient mice. ASN Neuro 2009, 1:e00024.
218. Walker D.W., Barnes D.E., Zornetzer S.F., Hunter B.E., Kubanis P. Neuronal loss in hippocampus induced by prolonged ethanol consumption in rats. Science 1980, 209:711-713.
219. Walter J., Honsek S.D., Illes S., Wellen J.M., Hartung H.P., Rose C.R., et al. A new role for interferon gamma in neural stem/precursor cell dysregulation. Mol Neurodegener 2011, 6:18.
220. Warnault V., Houchi H., Barbier E., Pierrefiche O., Vilpoux C., Ledent C., et al. The lack of CB1 receptors prevents neuroadapatations of both NMDA and GABAA receptors after chronic ethanol exposure. J Neurochem 2007, 102:741-752.
221. Whitney N.P., Eidem T.M., Peng H., Huang Y., Zheng J.C. Inflammation mediates varying effects in neurogenesis: relevance to the pathogenesis of brain injury and neurodegenerative disorders. J Neurochem 2009, 108:1343-1359.
222. Zeigler D.W., Wang C.C., Yoast R.A., Dickinson B.D., McCaffree M.A., Robinowitz C.B., et al. The neurocognitive effects of alcohol on adolescents and college students. Prev Med 2005, 40:23-32.
223. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132:645-660.
224. Zhou F.C., Balaraman Y., Teng M., Liu Y., Singh R.P., Nephew K.P. Alcohol alters DNA methylation patterns and inhibits neural stem cell differentiation. Alcohol Clin Exp Res 2011, 35:735-746.
225. Zou J., Crews F.T. Inflammasome-IL-1beta signaling mediates ethanol inhibition of hippocampal neurogenesis. Front Neurosci 2012, 6:30.
226. Zunszain P.A., Anacker C., Cattaneo A., Choudhury S., Musaelyan K., Myint A.M., et al. Interleukin-1beta: a new regulator of the kynurenine pathway affecting human hippocampal neurogenesis. Neuropsychopharmacology 2012, 37:939-949.