Effects of ethanol on hippocampal function during adolescence: A look at the past and thoughts on the future

Alcohol

Volumn 44, Issue 1, 2010, Pages 3-14

  Chin, Vivien S ^a   Van Skike, Candice E ^a   Matthews, Douglas B ^a,b  

^a BAYLOR UNIVERSITY   (United States)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Adolescents; Alcohol; GABAA; Hippocampus; Learning; Memory

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID A RECEPTOR; ALCOHOL; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ADOLESCENT DEVELOPMENT; ALCOHOL METABOLISM; AMNESIA; BRAIN DAMAGE; BRAIN MATURATION; COGNITIVE DEFECT; CONDUCT DISORDER; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; HUMAN; HYPOTHERMIA; LEARNING; LEARNING DISORDER; LONG TERM POTENTIATION; MEMORY DISORDER; MENTAL PERFORMANCE; MOOD DISORDER; MOTOR DYSFUNCTION; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; REVIEW; SPATIAL MEMORY;

ADOLESCENT; ADOLESCENT BEHAVIOR; ADOLESCENT DEVELOPMENT; AGE FACTORS; ALCOHOL DRINKING; ANIMALS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ETHANOL; HIPPOCAMPUS; HUMANS; MEMORY; RATS;

RATTUS;

EID: 76449105043     PISSN: 07418329     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.alcohol.2009.10.015     Document Type: Review

References (171)

1. Acheson S.K., Ross E.L., Swartzwelder H.S. Age-independent and dose-response effects of ethanol on spatial memory in rats. Alcohol 2001, 23:167-175.
2. Acheson S.K., Stein R.M., Swartzwelder H.S. Impairment of semantic and figural memory by acute ethanol: age-dependent effects. Alcohol. Clin. Exp. Res. 1998, 22:1437-1442.
3. Anagnostaras S.G., Maren S., Fanselow M.S. Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: within-subjects examination. J. Neurosci. 1999, 19:1106-1114.
4. Archibald, A. B., Graber, J. A., and Brooks-Gunn, J. (2003). Pubertal processes and physiological growth in adolescence. In: Adams, G. R., & Berzonsky, M. D. (Eds.), Blackwell Handbook of Adolescence, pp. 24-47.
5. Arnett J.J. Sensation seeking, aggressiveness, and adolescent reckless behavior. Pers. Individ. Dif. 1996, 20:693-702.
6. Barbaccia M.L., Scaccianoce S., Del Bianco P., Campolongo P., Trezza V., Tattoli M., et al. Cognitive impairment and increased brain neurosteroids in adult rats perinatally exposed to low millimolar blood alcohol concentrations. Psychoneuroendocrinology 2007, 32:931-942.
7. Bergstrom H.C., McDonald C.G., Smith R.F. Alcohol exposure during adolescence impairs auditory fear conditioning in adult Long-Evans rats. Physiol. Behav. 2006, 88:466-472.
8. Berry R.B., Matthews D.B. Acute ethanol administration selectively impairs spatial memory in C57BL/6J mice. Alcohol 2004, 32:9-18.
9. Blanchard B.A., Riley E.P., Hannigan J.H. Deficits on a spatial navigation task following prenatal exposure to ethanol. Neurotoxicol. Teratol. 1987, 9:253-258.
10. Blitzer R.D., Gil O., Landau E.M. Long-term potentiation in rat hippocampus is inhibited by low concentrations of ethanol. Brain Res. 1990, 537:203-208.
11. Bolhuis J.J., Stewart C.A., Forrest E.M. Retrograde amnesia and memory reactivation in rats with ibotenate lesions to the hippocampus or subiculum. Q. J. Exp. Psychol. B 1994, 47:129-150.
12. Brown S.A., Tapert S.F., Granholm E., Delis D.C. Neurocognitive functioning of adolescents: effects of protracted alcohol use. Alcohol Clin. Exp. Res. 2000, 24:164-171.
13. Brown S.A., Tapert S.F. Adolescence and the trajectory of alcohol use: basic to clinical studies. Ann. N. Y. Acad. Sci 2004, 1021:234-244.
14. Carpenter-Hyland E.P., Chandler J.L. Adaptive plasticity of NMDA receptors and dendritic spines: implications for enhanced vulnerability of the adolescent brain to alcohol addiction. Pharmacol. Biochem. Behav. 2007, 86:200-208.
15. Casey B.J., Galvan A., Hare T.A. Changes in cerebral functional organization during cognitive development. Curr. Opin. Neurobiol. 2005, 15:239-244.
16. Casey B.J., Getz S., Galvan A. The adolescent brain. Dev. Rev. 2008, 28:62-77.
17. Chang Q., Gold P.E. Intra-hippocampal lidocaine injections impair acquisition of a place task and facilitate acquisition of a response task in rats. Behav. Brain Res. 2003, 144:19-24.
18. 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.
19. Chin V.S., Berry R.B., Matthews D.B. Adolescent rats are less sensitive than adult rats to the spatial memory impairing effects of acute ethanol. Alcoholism: Clin. Exper. Res 2009, 33:216A.
20. Clark R.E., Broadbent N.J., Squire L.R. Hippocampus and remote spatial memory in rats. Hippocampus 2005, 15:260-272.
21. Clark D.B., Lesnick L., Hegedus A.M. Traumas and other adverse life events in adolescents with alcohol abuse and dependence. J. Am. Acad. Child Adolesc. Psychiatry 1997, 36:1744-1751.
22. Clark D.B., Pollock N., Bukstein O.G., Mezzich A.C., Bromberger J.T., Donovan J.E. Gender and comorbid psychopathology in adolescents with alcohol dependence. J. Am. Acad. Child Adolesc. Psychiatry 1997, 36:1195-1203.
23. Clayton N.S., Griffiths D.P., Emery N.J., Dickinson A. Elements of episodic-like memory in animals. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 2001, 356:1483-1491.
24. Cornwell B.R., Johnson L.L., Holroyd T., Carver F.W., Grillon C. Human hippocampal and parahippocampal theta during goal-directed spatial navigation predicts performance on a virtual Morris water maze. J. Neurosci. 2008, 28:5983-5990.
25. Craig L.A., Hong N.S., Kopp J., McDonald R.J. Selective lesion of medial septal cholinergic neurons followed by a mini-stroke impairs spatial learning in rats. Exp. Brain Res. 2009, 193:29-42.
26. 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.
27. Cull-Candy S., Brickley S., Farrant M. NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol. 2001, 11:327-335.
28. Czerniawski J., Yoon T., Otto T. Dissociating space and trace in dorsal and ventral hippocampus. Hippocampus 2009, 19:20-32.
29. Dahl R.E. Adolescent brain development: a period of vulnerabilities and opportunities. Keynote address. Ann. N. Y. Acad. Sci. 2004, 1021:1-22.
30. Dillon G.M., Qu X., Marcus J.N., Dodart J.C. Excitotoxic lesions restricted to the dorsal CA1 field of the hippocampus impair spatial memory and extinction learning in C57BL/6 mice. Neurobiol. Learn. Mem. 2008, 90:426-433.
31. 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.
32. De Bellis M.D., Narasimhan A., Thatcher D.L., Keshavan M.S., Soloff P., Clark D.B. Prefrontal cortex, thalamus, and cerebellar volumes in adolescents and young adults with adolescent-onset alcohol use disorders and comorbid mental disorders. Alcohol. Clin. Exp. Res. 2005, 29:1590-1600.
33. Doremus T.L., Brunell S.C., Rajendran P., Spear L.P. Factors influencing elevated ethanol consumption in adolescent relative to adult rats. Alcohol. Clin. Exp. Res. 2005, 29:1796-1808.
34. Durston S., Hulshoff Pol H.E., Casey B.J., Giedd J.N., Buitelaar J.K., van Engeland H. Anatomical MRI of the developing human brain: what have we learned?. J. Am. Acad. Child Adolesc. Psychiatry 2001, 40:1012-1020.
35. Ego-Stengel V., Wilson M.A. Spatial selectivity and theta phase precession in CA1 interneurons. Hippocampus 2007, 17:161-174.
36. Eichenbaum H. The hippocampus and mechanisms of declarative memory. Behav. Brain Res. 1999, 103:123-133.
37. Eichenbaum H., Stewart C., Morris R.G. Hippocampal representation in place learning. J. Neurosci. 1990, 10:3531-3542.
38. Ezzyat Y., Olson I.R. The medial temporal lobe and visual working memory: comparisons across tasks, delays, and visual similarity. Cogn. Affect. Behav. Neurosci. 2008, 8:32-40.
39. Farr S.A., Scherrer J.F., Banks W.A., Flood J.F., Morley J.E. Chronic ethanol consumption impairs learning and memory after cessation of ethanol. Alcohol. Clin. Exp. Res. 2005, 29:971-982.
40. Fleming R.L., Wilson W.A., Swartzwelder H.S. Magnitude and ethanol sensitivity of tonic GABAA receptor-mediated inhibition in detate gyrus changes from adolescence to adulthood. J. Neurophysiol. 2007, 97:3806-3811.
41. Fritschy J.M., Paysan J., Enna A., Mohler H. Switch in the expression of rat GABAA-receptor subtypes during postnatal development: an immunohistochemical study. J. Neurosci. 1994, 14:5302-5324.
42. Fritschy J.M., Mohler H. GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp. Neurol 2005, 359:154-194.
43. Frotscher M., Seress L. Morphological Development of the Hippocampus. The Hippocampus Book 2007, 115-131. Oxford University Press, Oxford, UK.
44. Giancola P.R., Mezzich A.C., Tarter R.E. Executive cognitive functioning, temperament, and antisocial behavior in conduct disordered adolescent females. J. Abnorm. Psychol. 1998, 107:629-641.
45. Gibson W.E. Effects of alcohol on radial maze performance in rats. Physiol. Behav. 1985, 35:1003-1005.
46. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., et al. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 1999, 2:861-863.
47. Giedd J.N., Castellanos F.X., Rajapakse J.C., Vaituzis A.C., Rapoport J.L. Sexual dimorphism of the developing human brain. Prog. Neuropsychopharmacol. Biol. Psychiatry 1997, 21:1185-1201.
48. Girard T.A., Xing H.C., Ward G.R., Wainwright P.E. Early postnatal ethanol exposure has long-term effects on the performance of male rats in a delayed matching-to-place task in the Morris water maze. Alcohol. Clin. Exp. Res. 2000, 24:300-306.
49. Givens B. Low doses of ethanol impair spatial working memory and reduce hippocampal theta activity. Alcohol. Clin. Exp. Res. 1995, 19:763-767.
50. Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:8174-8179.
51. Goodlett C.R., Johnson T.B. Neonatal binge ethanol exposure using intubation: time and dose effects on place learning. Neurotoxicol. Teratol. 1997, 19:435-446.
52. Grant K.A. Strategies for understanding the pharmacological effects of ethanol with drug discrimination procedures. Pharmacol. Biochem. Behav. 1999, 64:261-267.
53. Gulick D., Gould T.J. Acute ethanol has biphasic effects on short- and long-term memory in both foreground and background contextual fear conditioning in C57BL/6 mice. Alcohol. Clin. Exp. Res. 2007, 31:1528-1537.
54. Gutierrez A., Khan Z.U., Miralles C.P., Mehta A.K., Ruano D., Araujo F., et al. GABAA receptor subunit expression changes in the rat cerebellum and cerebral cortex during aging. Brain Res. Mol. Brain Res. 1997, 45:59-70.
55. Hargreaves G.A., Quinn H., Kashem M.A., Matsumoto I., McGregor I.S. Proteomic analysis demonstrates adolescent vulnerability to lasting hippocampal changes following chronic alcohol consumption. Alcohol. Clin. Exp. Res. 2009, 33:86-94.
56. Harper C. The neuropathology of alcohol-related brain damage. Alcohol Alcohol. 2009, 44:136-140.
57. Haut J.S., Beckwith B.E., Petros T.V., Russell S. Gender differences in retrieval from long-term memory following acute intoxication with ethanol. Physiol. Behav. 1989, 45:1161-1165.
58. Hernandez-Rabaza V., Hontecillas-Prieto L., Velazquez-Sanchez C., Ferragud A., Perez-Villaba A., Arcusa A., et al. The hippocampal dentate gyrus is essential for generating contextual memories of fear and drug-induced reward. Neurobiol. Learn. Mem. 2008, 90:553-559.
59. Hirsh R. The hippocampus and contextual retrieval of information from memory: a theory. Behav. Biol. 1974, 12:421-444.
60. Hunt P.S., Levillain M.E., Spector B.M., Kostelnik L.A. Post-training ethanol disrupts trace conditioned fear in rats: effects of timing of ethanol, dose and trace interval duration. Neurobiol. Learn. Mem. 2009, 91:73-80.
61. Jarrard L.E. Selective hippocampal lesions and behavior: efffects of kainic acid lesions on performace of place and cue tasks. Behav. Neurosci. 1993, 97:873-889.
62. Johnson T.B., Goodlett C.R. Selective and enduring deficits in spatial learning after limited neonatal binge alcohol exposure in male rats. Alcohol. Clin. Exp. Res. 2002, 26:83-93.
63. Kalluri H.S., Ticku M.K. Effect of ethanol on phosphorylation of the NMDAR2B subunit in mouse cortical neurons. Brain Res. Mol. Brain Res. 1999, 68:159-168.
64. Kanaumi T., Takashima S., Iwasaki H., Mitsudome A., Hirose S. Developmental changes in the expression of GABAA receptor alpha 1 and gamma 2 subunits in human temporal lobe, hippocampus and basal ganglia: an implication for consideration on age-related epilepsy. Epilepsy Res. 2006, 71:47-53.
65. Kennedy P.J., Shapiro M.L. Retrieving memories via internal context requires the hippocampus. J. Neurosci. 2004, 24:6979-6985.
66. Khisti R.T., Penland S.N., VanDoren M.J., Grobin A.C., Morrow A.L. GABAergic neurosteroid modulation of ethanol actions. World J. Biol. Psychiatry 2002, 3:87-95.
67. Kim J.H., Lee S., Chow J., Lau J., Tsang A., Choi J., et al. Prevalence and the factors associated with binge drinking, alcohol abuse, and alcohol dependence: a population-based study of Chinese adults in Hong Kong. Alcohol Alcohol. 2008, 43:360-370.
68. Kirwan C.B., Gilbert P.E., Kesner R.P. The role of the hippocampus in the retrieval of a spatial location. Neurobiol. Learn. Mem. 2005, 83:65-71.
69. Kumar S., Porcu P., Werner D.F., Matthews D.B., Diaz-Granados J.L., Helfand R.S., et al. The role of GABA(A) receptors in the acute and chronic effects of ethanol: a decade of progress. Psychopharmacology (Berl.) 2009, 205:529-564.
70. Lancaster F.E., Brown T.D., Coker K.L., Elliott J.A., Wren S.B. Sex differences in alcohol preference and drinking patterns emerge during the early postpubertal period. Alcohol. Clin. Exp. Res. 1996, 20:1043-1049.
71. Land C., Spear N.E. Fear conditioning is impaired in adult rats by ethanol doses that do not affect periadolescents. Int. J. Dev. Neurosci. 2004, 22:355-362.
72. Lattal K.M. Effects of ethanol on encoding, consolidation, and expression of extinction following contextual fear conditioning. Behav. Neurosci. 2007, 121:1280-1292.
73. Laurie D.J., Wisden W., Seeburg P.H. The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J. Neurosci. 1992, 12:4151-4172.
74. Laviola G., Macri S., Adriani W., Morley Fletcher S. Psychobiological determinates of risk behavior in adolescence. Ann. 1st Super Sanita. 2002, 38:279-287.
75. Li J.S., Chao Y.S. Electrolytic lesions of dorsal CA3 impair episodic-like memory in rats. Neurobiol. Learn. Mem. 2008, 89:192-198.
76. Liang J., Suryanarayanan A., Chandra D., Homanics G.E., Olsen R.W., Spigelman I. Functional consequences of GABAA receptor α4 subunit deletion on synaptic and extrasynaptic currents in mouse dentate granule cells. Alcohol. Clin. Exp. Res. 2008, 32:19-26.
77. Lim W.Y., Fong C.W., Chan J.M., Heng D., Bhalla V., Chew S.K. Trends in alcohol consumption in Singapore 1992-2004. Alcohol Alcohol. 2007, 42:354-361.
78. Lister R.G., Gorenstein C., Fisher-Flowers D., Weingartner H.J., Eckardt M.J. Dissociation of the acute effects of alcohol on implicit and explicit memory processes. Neuropsychologia 1991, 29:1205-1212.
79. Lovinger D.M., White G., Weight F.F. NMDA receptor-mediated synaptic excitation selectively inhibited by ethanol in hippocampal slice from adult rat. J. Neurosci. 1990, 10:1372-1379.
80. Maguire E.A., Gadian D.G., Johnsrude I.S., Good C.D., Ashburner J., Frackowiak R.S., et al. Navigation-related structural change in the hippocampi of taxi drivers. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:4398-4403.
81. Makris N., Oscar-Berman M., Jaffin S.K., Hodge S.M., Kennedy D.N., Caviness V.S., et al. Decreased volume of the brain reward system in alcoholism. Biol. Psychiatry 2008, 64:192-202.
82. Manns J.R., Hopkins R.O., Squire L.R. Semantic memory and the human hippocampus. Neuron 2003, 38:127-133.
83. Markwiese B.J., Acheson S.K., Levin E.D., Wilson W.A., Swartzwelder H.S. Differential effects of ethanol on memory in adolescent and adult rats. Alcohol. Clin. Exp. Res. 1998, 22:416-421.
84. Martin S.J., Clark R.E. The rodent hippocampus and spatial memory: from synapses to systems. Cell. Mol. Life Sci. 2007, 64:401-431.
85. Matthews D.B., Best P.J. Fimbria/fornix lesions facilitate the learning of a non-spatial response task. Psychon. Bull. Rev. 1995, 2:113-116.
86. Matthews D.B., Silvers J.R. The use of acute ethanol administration as a tool to investigate multiple memory systems. Neurobiol. Learn. Mem. 2004, 82:299-308.
87. Matthews D.B., Simson P.E. Prenatal exposure to ethanol disrupts spatial memory: effect of the training-testing delay period. Physiol. Behav. 1998, 64:63-67.
88. Matthews D.B., Simson P.E., Best P.J. Acute ethanol impairs the use of spatial memory but not the use of stimulus/response memory in the rat. Alcohol. Clin. Exp. Res. 1995, 19:902-909.
89. Matthews D.B., Simson P.E., Best P.J. Ethanol alters spatial processing of hippocampal place cells: a mechanism for impaired navigation when intoxicated. Alcohol. Clin. Exp. Res. 1996, 20:404-407.
90. Matthews D.B., Illgen M.A., White A.M., Best P.J. Acute ethanol administration impairs spatial performance while facilitating non-spatial performance in rats. Neurobiol. Learn. Mem. 1999, 72:169-179.
91. Matthews D.B., Morrow A.L., Tokunaga S., McDaniel J.R. Acute ethanol administration and acute allopregnanolone administration impair spatial memory in the Morris water task. Alcohol. Clin. Exp. Res. 2002, 26:1747-1751.
92. Matthews D.B., Tinsley K.L., Diaz-Granados J.L., Tokunaga S., Silvers J.M. Chronic intermittent exposure to ethanol during adolescence produces tolerance to the hypnotic effects of ethanol in male rats: a dose-dependent analysis. Alcohol 2008, 42:617-621.
93. McQweeny T., Schweinsburg B.C., Schweinsburg A.D., Jacobus J., Bava S., Frank L.R., et al. Altered white matter integrity in adolescent binge drinkers. Alcohol. Clin. Exp. Res. 2009, 33:1278-1285.
94. Medina K.L., Schweinsburg A.D., Cohen-Zion M., Nagel B.J., Tapert S.F. Effects of alcohol and combined marijuana and alcohol use during adolescence on hippocampal volume and asymmetry. Neurotoxicol. Teratol. 2007, 29:141-152.
95. Medina K.L., McQueeny T., Nagel B.J., Hanson K.L., Schweinsburg A.D., Tapert S.F. Prefrontal cortex volumes in adolescents with alcohol use disorders: unique gender effects. Alcohol. Clin. Exp. Res. 2008, 32:386-394.
96. M'Harzi M., Jarrard L.E., Willig F., Palacios A., Delacour J. Selective fimbria and thalamic lesions differentially impair forms of working memory in rats. Behav. Neural Biol. 1991, 56:221-239.
97. Miller M.E., Adesso V.J., Fleming J.P., Gino A., Lauerman R. Effects of alcohol on the storage and retrieval processes of heavy social drinkers. J. Exp. Psychol. Hum. Learn. 1978, 4:246-255.
98. Morris R.G. Spatial localisation does not depend on the presence of local cues. Learn. Motiv. 1981, 12:239-260.
99. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
100. Moss H.B., Kirisci L., Gordon H.W., Tarter R.E. A neuropsychologic profile of adolescent alcoholics. Alcohol. Clin. Exp. Res. 1994, 18:159-163.
101. Mumby D.G., Astur R.S., Weisend M.P., Sutherland R.J. Retrograde amnesia and selective damage to the hippocampal formation: memory for places and object discriminations. Behav. Brain Res. 1999, 106:97-107.
102. 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.
103. Narahashi T., Kuriyama K., Illes P., Wirkner K., Muhlberg K., Scheibler P., et al. Neuroreceptors and ion channels as targets of alcohol. Alcohol. Clin. Exp. Res. 2001, 25:182S-188S.
104. Nichols E.A., Kao Y.C., Verfaellie M., Gabrieli J.D. Working memory and long-term memory for faces: evidence from fMRI and global amnesia for involvement of the medial temporal lobes. Hippocampus 2006, 16:604-616.
105. O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971, 34:171-175.
106. O'Keefe J., Nadel L. The Hippocampus as a Cognitive Map 1978, Oxford University Press, Oxford, UK.
107. Owens J.C., Bennett B., Johnson T.E. Possible pleiotropic effects of genes specifying sedative/hypnotic sensitivity to ethanol on other alcohol-related traits. Alcohol. Clin. Exp. Res. 2002, 26:1461-1467.
108. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol. Learn. Mem. 1996, 65:65-72.
109. Pascual M., Blanco A.M., Cauli O., Minarro J., Guerri C. Intermittent ethanol exposure induces inflammatory brain damage and causes long-term behavioural alterations in adolescent rats. Eur. J. Neurosci. 2007, 25:541-550.
110. Penick S., Solomon P.R. Hippocampus, context, and conditioning. Behav. Neurosci. 1991, 105:611-617.
111. Pfefferbaum A., Mathalon D.H., Sullivan E.V., Rawles J.M., Zipursky R.B., Lim K.O. A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. Arch. Neurol. 1994, 51:874-887.
112. Pfefferbaum A., Sullivan E.V., Mathalon D.H., Lim K.O. Frontal lobe volume loss observed with magnetic resonance imaging in older chronic alcoholics. Alcohol. Clin. Exp. Res. 1997, 21:521-529.
113. Pian J.P., Criado J.R., Walker B.M., Ehlers C.L. Differential effects of acute alcohol on EEG and sedative responses in adolescent and adult Wistar rats. Brain Res. 2008, 1194:28-36.
114. Popovic M., Caballero-Bleda M., Guerri C. Adult rat's offspring of alcoholic mothers are impaired on spatial learning and object recognition in the can test. Behav. Brain Res. 2006, 174:101-111.
115. Pothuizen H.H., Zhang W.N., Jongen-Relo A.L., Feldon J., Yee B.K. Dissociation of function between the dorsal and the ventral hippocampus in spatial learning abilities of the rat: a within-subject, within-task comparison of reference and working spatial memory. Eur. J. Neurosci. 2004, 19:705-712.
116. Pyapali G.K., Turner D.A., Wilson W.A., Swartzwelder H.S. Age and dose-dependent effects of ethanol on the induction of hippocampal long-term potentiation. Alcohol 1999, 19:107-111.
117. Rajendran P., Spear L.P. The effects of ethanol on spatial and nonspatial memory in adolescent and adult rats studied using an appetitive paradigm. Ann. N. Y. Acad. Sci. 2004, 1021:441-444.
118. Ranck J.B. Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp. Neurol. 1973, 41:461-531.
119. Ranganath C., D'Esposito M. Medial temporal lobe activity associated with active maintenance of novel information. Neuron 2001, 31:865-873.
120. Redish A.D. The hippocampal debate: are we asking the right questions?. Behav. Brain Res. 2001, 127:81-98.
121. Redish A.D., Touretzky D.S. The role of the hippocampus in solving the Morris water maze. Neural Comput. 1998, 10:73-111.
122. Reyes E., Wolfe J., Savage D.D. The effects of prenatal alcohol exposure on radial arm maze performance in adult rats. Physiol. Behav. 1989, 46:45-48.
123. Ristuccia R.C., Spear L.P. Autonomic responses to ethanol in adolescent and adult rats: a dose-response analysis. Alcohol 2008, 42:623-629.
124. Roberto M., Nelson T.E., Ur C.L., Gruol D.L. Long-term potentiation in the rat hippocampus is reversibly depressed by chronic intermittent ethanol exposure. J. Neurophysiol. 2002, 87:2385-2397.
125. Rudy J.W., Sutherland R.J. The hippocampal formation is necessary for rats to learn and remember configural discriminations. Behav. Brain Res. 1989, 34:97-109.
126. Saults J.S., Cowan N., Sher K.J., Moreno M.V. Differential effects of alcohol on working memory: distinguishing multiple processes. Exp. Clin. Psychopharmacol. 2007, 15:576-587.
127. Schroeder J.P., Wingard J.C., Packard M.G. Post-training reversible inactivation of hippocampus reveals interference between memory systems. Hippocampus 2002, 12:280-284.
128. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatr. 1957, 20:11-21.
129. Shapiro M. Plasticity, hippocampal place cells, and cognitive maps. Arch. Neurol. 2001, 58:874-881.
130. Sher L. Functional magnetic resonance imaging in studies of neurocognitive effects of alcohol use on adolescents and young adults. Int. J. Adolesc. Med. Health 2006, 18:3-7.
131. Shimizu K., Matsubara K., Uezono T., Kimura K., Shiono H. Reduced dorsal hippocampal glutamate release significantly correlates with the spatial memory deficits produced by benzodiazepines and ethanol. Neuroscience 1998, 83:701-706.
132. Silveri M.M., Spear L.P. Decreased sensitivity to the hypnotic effects of ethanol early in ontogeny. Alcohol. Clin. Exp. Res. 1998, 22:670-676.
133. Silvers J.M., Tokunaga S., Berry R.B., White A.M., Matthews D.B. Impairments in spatial learning and memory: ethanol, allopregnanolone, and the hippocampus. Brain Res. Brain Res. Rev. 2003, 43:275-284.
134. Silvers J.M., Tokunaga S., Mittleman G., O'Buckley T., Morrow A.L., Matthews D.B. Chronic intermittent ethanol exposure during adolescence reduces the effect of ethanol challenge on hippocampal allopregnanolone levels and Morris water maze task performance. Alcohol 2006, 39:151-158.
135. Sinclair J.G., Lo G.F. Ethanol blocks titanic and calcium-induced long-term potentiation in the hippocampal slice. Gen. Pharmacol. 1986, 17:231-233.
136. Sircar R., Sircar D. Adolescent rats exposed to repeated ethanol treatment show lingering behavioral impairments. Alcohol. Clin. Exp. Res. 2005, 29:1402-1410.
137. Slawecki C.J., Betancourt M., Cole M., Ehlers C.L. Periadolescent alcohol exposure has lasting effects on adult neurophysiological function in rats. Brain Res. Dev. Brain Res. 2001, 128:63-72.
138. Smith D.M., Wakeman D., Patel J., Gabriel M. Fornix lesions impair context-related cingulothalamic neuronal patterns and concurrent discrimination learning in rabbits (Oryctolagus cuniculus). Behav. Neurosci. 2004, 118:1225-1239.
139. Soderlund H., Grady C.L., Easdon C., Tulving E. Acute effects of alcohol on neural correlates of episodic memory encoding. Neuroimage 2007, 35:928-939.
140. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 2000, 24:417-463.
141. Steinberg L., Albert D., Cauffman E., Banich M., Graham S., Woolard J. Age differences in sensation seeking and impulsivity as indexed by behavior and self-report: evidence for a dual systems model. Dev. Psychol. 2008, 44:1764-1778.
142. Stephens D.N., Ripley T.L., Borlikova G., Mchubert M., Albrecht D., Hogarth L., et al. Repeated ethanol exposure and withdrawal impairs human fear conditioning and depresses long-term potentiation in rat amygdala in hippocampus. Biol. Psychiatry 2005, 58:392-400.
143. Substance Abuse and Mental Health Services Administration Results from the 2005 National Survey on Drug Use and Health: National Findings 2006, Office of Applied Studies, Rockville, MD, NSDUH Series H-30, DHHS Publication No. SMA 06e4194.
144. Sundstrom-Poromaa I., Smith D.H., Gong Q.H., Sabado T.N., Li X., Light A., et al. Hormonally regulated α4β2δ GABAA receptors are a target for alcohol. Nat. Neurosci. 2002, 5:721-722.
145. Sutherland R.J., Weisend M.P., Mumby D., Astur R.S., Hanlon F.M., Koerner A., et al. Retrograde amnesia after hippocampal damage: recent vs. remote memories in two tasks. Hippocampus 2001, 11:27-42.
146. Swartzwelder H.S., Richardson R.C., Markwiese-Foerch B., Wilson W.A., Little P.J. Developmental differences in the acquisition of tolerance to ethanol. Alcohol 1998, 15:311-314.
147. Swartzwelder H.S., Wilson W.A., Tayyeb M.I. Age-dependent inhibition of long-term potentiation by ethanol in immature versus mature hippocampus. Alcohol. Clin. Exp. Res. 1995, 19:1480-1485.
148. Swartzwelder H.S., Wilson W.A., Tayyeb M.I. Differential sensitivity of NMDA receptor-mediated synaptic potentials to ethanol in immature versus mature hippocampus. Alcohol. Clin. Exp. Res. 1995, 19:320-323.
149. Talpos J.C., Dias R., Bussey T.J., Saksida L.M. Hippocampal lesions in rats impair learning and memory for locations on a touch-sensitive computer screen: the " ASAT" task. Behav. Brain Res. 2008, 192:216-225.
150. Tapert S.F., Brown S.A. Neuropsychological correlates of adolescent substance abuse: four-year outcomes. J. Int. Neuropsychol. Soc. 1999, 5:481-493.
151. Tapert S.F., Granholm E., Leedy N.G., Brown S.A. Substance use and withdrawal: neuropsychological functioning over 8 years in youth. J. Int. Neuropsychol. Soc. 2002, 8:873-883.
152. Tokunaga S., McDaniel J.R., Morrow A.L., Matthews D.B. Effect of acute ethanol administration and acute allopregnanolone administration on spontaneous hippocampal pyramidal cell neural activity. Brain Res. 2003, 967:273-280.
153. Tokunaga S., Silvers J.M., Matthews D.B. Chronic intermittent ethanol exposure during adolescence blocks ethanol-induced inhibition of spontaneously active hippocampal pyramidal neurons. Alcohol. Clin. Exp. Res. 2006, 30:1-6.
154. Tulving E., Markowitsch H.J. Episodic and declarative memory: role of the hippocampus. Hippocampus 1998, 8:198-204.
155. Vargha-Khadem F., Gadian D.G., Watkins K.E., Connelly A., Van Paesschen W., Mishkin M. Differential effects of early hippocampal pathology on episodic and semantic memory. Science 1997, 277:376-380.
156. Walker B.M., Walker J.L., Ehlers C.L. Dissociable effects of ethanol consumption during the light and dark phase in adolescent and adult Wistar rats. Alcohol 2008, 42:83-89.
157. Wang J., Carnicella S., Phamluong K., Jeanblanc J., Ronesi J.A., Chaudhri N., et al. Ethanol induces long-term facilitation of NR2B-NMDA receptor activity in the dorsal striatum: implications for alcohol drinking behavior. J. Neurosci. 2007, 27:3593-3602.
158. Wei W., Faria L.C., Mody I. Low ethanol concentrations selectively augment the tonic inhibition mediated by δ subunit-containing GABAA receptors in hippocampal neurons. J. Neurosci. 2004, 24:8379-8382.
159. White A.M., Best P.J. Effects of ethanol on hippocampal place-cell and interneuron activity. Brain Res. 2000, 876:154-165.
160. White A.M., Swartzwelder H.S. Hippocampal function during adolescence: a unique target of ethanol effects. Ann. N. Y. Acad. Sci. 2004, 1021:206-220.
161. White A.M., Swartzwelder H.S. Age-related effects of alcohol on memory and memory-related brain function in adolescents and adults. Recent Dev. Alcohol. 2005, 17:161-176.
162. White A.M., Bae J.G., Truesdale M.C., Ahmad S., Wilson W.A., Swartzwelder H.S. Chronic-intermittent ethanol exposure during adolescence prevents normal developmental changes in sensitivity to ethanol-induced motor impairments. Alcohol. Clin. Exp. Res. 2002, 26:960-968.
163. White A.M., Elek T.M., Beltz T.L., Best P.J. Spatial performance is more sensitive to ethanol than nonspatial performance regardless of cue proximity. Alcohol. Clin. Exp. Res. 1998, 22:2102-2107.
164. White A.M., Simson P.E., Best P.J. Comparison between the effects of ethanol and diazepam on spatial working memory in the rat. Psychopharmacology (Berl.) 1997, 133:256-261.
165. Wilent W.B., Nitz D.A. Discrete place fields of hippocampal formation interneurons. J. Neurophysiol. 2007, 97:4152-4161.
166. Wisden W., Laurie D.J., Monyer H., Seeburg P.H. The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telecephalon, diencephalon, mesencephalon. J. Neurosci. 1992, 12:1040-1062.
167. Wise S.P., Murray E.A. Arbitrary associations between antecedents and actions. Trends Neurosci. 2000, 23:271-276.
168. Wright J.W., Masino A.J., Reichert J.R., Turner G.D., Meighan S.E., Meighan P.C., et al. Ethanol-induced impairment of spatial memory and brain matrix metalloproteinases. Brain Res. 2003, 963:252-261.
169. Yan H., Li Q., Fleming R., Madison R.D., Wilson W.A., Swartzwelder H.S. Developmental sensitivity of hippocampal interneurons to ethanol: involvement of the hyperpolarization-activated current, Ih. J. Neurophysiol. 2009, 101:67-83.
170. Yu Z.Y., Wang W., Fritschy J.M., Witte O.W., Redecker C. Changes in neocortical and hippocampal GABAA receptor subunit distribution during brain maturation and aging. Brain Res. 2006, 1099:73-81.
171. Zhang W.N., Pothuizen H.H., Feldon J., Rawlins J.N. Dissociation of function within the hippocampus: effects of dorsal, ventral and complete excitotoxic hippocampal lesions on spatial navigation. Neuroscience 2004, 127:289-300.