Rat strain differences in brain structure and neurochemistry in response to binge alcohol

Psychopharmacology

Volumn 231, Issue 2, 2014, Pages 429-445

  Zahr, Natalie M ^a,b   Mayer, Dirk ^b,c   Rohlfing, Torsten ^b   Hsu, Oliver ^b   Vinco, Shara ^b   Orduna, Juan ^b   Luong, Richard ^d   Bell, Richard L ^e   Sullivan, Edith V ^a   Pfefferbaum, Adolf ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SRI INTERNATIONAL   (United States)

^c STANFORD UNIVERSITY   (United States)

^d STANFORD UNIVERSITY   (United States)

^e INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alcoholism; Choline; Genetics; Magnetic resonance (MR) imaging; MR spectroscopy; Selective breeding; Ventriculomegaly

Indexed keywords

ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CHANGE; BINGE DRINKING; BRAIN LEVEL; BRAIN SIZE; BRAIN VENTRICLE; CHOLINE BRAIN LEVEL; CONTROLLED STUDY; DRINKING BEHAVIOR; HISTOPATHOLOGY; LIVER; NONHUMAN; PRIORITY JOURNAL; RAT; WEIGHT GAIN; WEIGHT REDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN; COMPARATIVE STUDY; DRUG EFFECTS; INBRED RAT STRAIN; MALE; METABOLISM; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOLOGY; SPECIES DIFFERENCE; WISTAR RAT;

ALCOHOL; ASPARTIC ACID; N-ACETYLASPARTATE;

ANIMALS; ASPARTIC ACID; BINGE DRINKING; BRAIN; BRAIN CHEMISTRY; CEREBRAL VENTRICLES; ETHANOL; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NEUROIMAGING; RATS; RATS, INBRED STRAINS; RATS, WISTAR; SPECIES SPECIFICITY;

EID: 84892794475     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-013-3253-z     Document Type: Article

References (109)

1. Adalsteinsson E, Hurd RE, Mayer D, Sailasuta N, Sullivan EV, Pfefferbaum A (2004) In vivo 2D J-resolved magnetic resonance spectroscopy of rat brain with a 3-T clinical human scanner. Neuroimage 22:381-386
2. Alfonso-Loeches S, Pascual M, Gomez-Pinedo U, Pascual-Lucas M, Renau-Piqueras J, Guerri C (2012) Toll-like receptor 4 participates in the myelin disruptions associated with chronic alcohol abuse. Glia 60:948-964
3. Altura BM, Altura BT (1999) Association of alcohol in brain injury, headaches, and stroke with brain-tissue and serum levels of ionized magnesium: a review of recent findings and mechanisms of action. Alcohol 19:119-130
4. Annweiler C, Montero-Odasso M, Hachinski V, Seshadri S, Bartha R, Beauchet O (2013) Vitamin D concentration and lateral cerebral ventricle volume in older adults. Mol Nutr Food Res 57:267-276
5. Baslow MH, Suckow RF, Hungund BL (2000) Effects of ethanol and of alcohol dehydrogenase inhibitors on the reduction of N-acetylaspartate levels of brain in mice in vivo: a search for substances that may have therapeutic value in the treatment of Canavan disease. J Inherit Metab Dis 23:684-692
6. Baslow MH, Suckow RF, Sapirstein V, Hungund BL (1999) Expression of aspartoacylase activity in cultured rat macroglial cells is limited to oligodendrocytes. J Mol Neurosci 13:47-53
7. Bates TE, Strangward M, Keelan J, Davey GP, Munro PMG, Clark JB (1996) Inhibition of N-acetylaspartate production: Implications for H-1 MRS studies in vivo. Neuroreport 7:1397-1400
8. Becker HC (2000) Animal models of alcohol withdrawal. Alcohol Res Health 24:105-113
9. Bell RL, Rodd ZA, Boutwell CL, Hsu CC, Lumeng L, Murphy JM, Li TK, McBride WJ (2004) Effects of long-term episodic access to ethanol on the expression of an alcohol deprivation effect in low alcohol-consuming rats. Alcohol Clin Exp Res 28:1867-1874
10. Bell RL, Rodd ZA, Lumeng L, Murphy JM, McBride WJ (2006a) The alcohol-preferring P rat and animal models of excessive alcohol drinking. Addict Biol 11:270-288
11. Bell RL, Rodd ZA, Sable HJ, Schultz JA, Hsu CC, Lumeng L, Murphy JM, McBride WJ (2006b) Daily patterns of ethanol drinking in peri-adolescent and adult alcohol-preferring (P) rats. Pharmacol Biochem Behav 83:35-46
12. Bell RL, Rodd ZA, Schultz JA, Peper CL, Lumeng L, Murphy JM, McBride WJ (2008) Effects of short deprivation and re-exposure intervals on the ethanol drinking behavior of selectively bred high alcohol-consuming rats. Alcohol 42:407-416
13. Bell RL, Sable HJ, Colombo G, Hyytia P, Rodd ZA, Lumeng L (2012) Animal models for medications development targeting alcohol abuse using selectively bred rat lines: neurobiological and pharmacological validity. Pharmacol Biochem Behav 103:119-155
14. Bell RL, Stewart RB, Woods JE 2nd, Lumeng L, Li TK, Murphy JM, McBride WJ (2001) Responsivity and development of tolerance to the motor impairing effects of moderate doses of ethanol in alcohol-preferring (P) and -nonpreferring (NP) rat lines. Alcohol Clin Exp Res 25:644-650
15. Berrettini M, Fedeli D, Falcioni G, Bevilacqua C, Massi M, Polidori C (2004) Hippocampal and striated skeletal muscle changes in fatty acid composition induced by ethanol in alcohol-preferring rats. Toxicology 199:161-168
16. Bluml S, Seymour KJ, Ross BD (1999) Developmental changes in choline- and ethanolamine-containing compounds measured with proton-decoupled (31)P MRS in in vivo human brain. Magn Reson Med 42:643-654
17. Boulanger Y, Labelle M, Khiat A (2000) Role of phospholipase A(2) on the variations of the choline signal intensity observed by 1H magnetic resonance spectroscopy in brain diseases. Brain Res Brain Res Rev 33:380-389
18. Brenner RE, Munro PM, Williams SC, Bell JD, Barker GJ, Hawkins CP, Landon DN, McDonald WI (1993) The proton NMR spectrum in acute EAE: the significance of the change in the Cho:Cr ratio. Magn Reson Med 29:737-745
19. Ciccia RM, Langlais PJ (2000) An examination of the synergistic interaction of ethanol and thiamine deficiency in the development of neurological signs and long-term cognitive and memory impairments. Alcohol Clin Exp Res 24:622-634
20. Cicero TJ, Snider SR, Perez VJ, Swanson LW (1971) Physical dependence on and tolerance to alcohol in the rat. Physiol Behav 6:191-198
21. Colombo G, Agabio R, Carai MA, Lobina C, Pani M, Reali R, Vacca G, Gessa GL (2000) Different sensitivity to ethanol in alcohol-preferring sP and -nonpreferring sNP rats. Alcohol Clin Exp Res 24:1603-1608
22. Colombo G, Lobina C, Carai MA, Gessa GL (2006) Phenotypic characterization of genetically selected Sardinian alcohol-preferring (sP) and -non-preferring (sNP) rats. Addict Biol 11:324-338
23. Crews FT, Braun CJ (2003) Binge ethanol treatment causes greater brain damage in alcohol-preferring P rats than in alcohol-nonpreferring NP rats. Alcohol Clin Exp Res 27:1075-1082
24. Crews FT, Braun CJ, Ali R, Knapp DJ (2001) Interaction of nutrition and binge ethanol treatment on brain damage and withdrawal. J Biomed Sci 8:134-142
25. Ding ZM, Rodd ZA, Engleman EA, Bailey JA, Lahiri DK, McBride WJ (2013) Alcohol drinking and deprivation alter basal extracellular glutamate concentrations and clearance in the mesolimbic system of alcohol-preferring (P) rats. Addict Biol 18:297-306
26. Djuricic B, Olson SR, Assaf HM, Whittingham TS, Lust WD, Drewes LR (1991) Formation of free choline in brain tissue during in vitro energy deprivation. J Cereb Blood Flow Metab 11:308-313
27. Dreher W, Leibfritz D (1999) Detection of homonuclear decoupled in vivo proton NMR spectra using constant time chemical shift encoding: CT-PRESS. Magn Reson Imaging 17:141-150
28. Ehlers CL, Chaplin RI, Wall TL, Lumeng L, Li TK, Owens MJ, Nemeroff CB (1992) Corticotropin releasing factor (CRF): studies in alcohol preferring and non-preferring rats. Psychopharmacology (Berl) 106:359-364
29. Ehlers CL, Li TK, Lumeng L, Hwang BH, Somes C, Jimenez P, Mathe AA (1998) Neuropeptide Y levels in ethanol-naive alcohol-preferring and nonpreferring rats and in Wistar rats after ethanol exposure. Alcohol Clin Exp Res 22:1778-1782
30. Ehlers CL, Somes C, Lumeng L, Li TK (1999) Electrophysiological response to neuropeptide Y (NPY): in alcohol-naive preferring and non-preferring rats. Pharmacol Biochem Behav 63:291-299
31. Enzmann DR, Lane B (1977) Cranial computed tomography findings in anorexia nervosa. J Comput Assist Tomogr 1:410-414
32. Fitzgerald GJ, Liu H, Morzorati SL (2012) Decreased sensitivity of NMDA receptors on dopaminergic neurons from the posterior ventral tegmental area following chronic nondependent alcohol consumption. Alcohol Clin Exp Res 36:1710-1719
33. Golden NH, Ashtari M, Kohn MR, Patel M, Jacobson MS, Fletcher A, Shenker IR (1996) Reversibility of cerebral ventricular enlargement in anorexia nervosa, demonstrated by quantitative magnetic resonance imaging. J Pediatr 128:296-301
34. Goldstein D (1983) Pharmacology of alcohol. Oxford University Press, Oxford
35. Gozzi A, Agosta F, Massi M, Ciccocioppo R, Bifone A (2013) Reduced limbic metabolism and fronto-cortical volume in rats vulnerable to alcohol addiction. Neuroimage 69:112-119
36. Grant BF, Stinson FS, Dawson DA, Chou SP, Dufour MC, Compton W, Pickering RP, Kaplan K (2004) Prevalence and co-occurrence of substance use disorders and independent mood and anxiety disorders: results from the National Epidemiologic Survey on Alcohol and Related Conditions. Arch Gen Psychiatry 61:807-816
37. Gunston GD, Burkimsher D, Malan H, Sive AA (1992) Reversible cerebral shrinkage in kwashiorkor: an MRI study. Arch Dis Child 67:1030-1032
38. Gupta RK, Sinha U, Cloughesy TF, Alger JR (1999) Inverse correlation between choline magnetic resonance spectroscopy signal intensity and the apparent diffusion coefficient in human glioma. Magn Reson Med 41:2-7
39. Harding AJ, Halliday GM, Ng JL, Harper CG, Kril JJ (1996) Loss of vasopressin-immunoreactive neurons in alcoholics is dose-related and time-dependent. Neuroscience 72:699-708
40. He J, Crews FT (2008) Increased MCP-1 and microglia in various regions of the human alcoholic brain. Exp Neurol 210:349-358
41. Hwang BH, Lumeng L, Wu JY, Li TK (1990) Increased number of GABAergic terminals in the nucleus accumbens is associated with alcohol preference in rats. Alcohol Clin Exp Res 14:503-507
42. Hwang BH, Stewart R, Zhang JK, Lumeng L, Li TK (2004a) Corticotropin-releasing factor gene expression is down-regulated in the central nucleus of the amygdala of alcohol-preferring rats which exhibit high anxiety: a comparison between rat lines selectively bred for high and low alcohol preference. Brain Res 1026:143-150
43. Hwang BH, Suzuki R, Lumeng L, Li TK, McBride WJ (2004b) Innate differences in neuropeptide Y (NPY) mRNA expression in discrete brain regions between alcohol-preferring (P) and -nonpreferring (NP) rats: a significantly low level of NPY mRNA in dentate gyrus of the hippocampus and absence of NPY mRNA in the medial habenular nucleus of P rats. Neuropeptides 38:359-368
44. Institute of Laboratory Animal Resources Commission on Life Sciences National Research Council (1996) Guide for the Care and Use of Laboratory Animals. National Academy Press, Washington, D.C.
45. Jones AE, McBride WJ, Murphy JM, Lumeng L, Li T, Shekhar A, McKinzie DL (2000) Effects of ethanol on startle responding in alcohol-preferring and -non-preferring rats. Pharmacol Biochem Behav 67:313-318
46. Kampov-Polevoy AB, Matthews DB, Gause L, Morrow AL, Overstreet DH (2000) P rats develop physical dependence on alcohol via voluntary drinking: changes in seizure thresholds, anxiety, and patterns of alcohol drinking. Alcohol Clin Exp Res 24:278-284
47. Kelso ML, Liput DJ, Eaves DW, Nixon K (2011) Upregulated vimentin suggests new areas of neurodegeneration in a model of an alcohol use disorder. Neuroscience 197:381-393
48. Kennedy GC (1967) Ontogeny of mechanisms controlling food and water intake. In: Code CF (ed) Handbook of physiology: alimentary canal. Control of food and water intake. American Physiological Society, Washington, D.C., pp 337-352
49. Langlais PJ, Zhang SX (1997) Cortical and subcortical white matter damage without Wernicke's encephalopathy after recovery from thiamine deficiency in the rat. Alcohol Clin Exp Res 21:434-443
50. Lankford MF, Roscoe AK, Pennington SN, Myers RD (1991) Drinking of high concentrations of ethanol versus palatable fluids in alcohol-preferring (P) rats: valid animal model of alcoholism. Alcohol 8:293-299
51. Lee DW, Kim SY, Kim JH, Lee T, Yoo C, Nam YK, Jung JY, Shin HC, Kim HY, Kim DJ, Choe BY (2013) Quantitative assessment of neurochemical changes in a rat model of long-term alcohol consumption as detected by in vivo and ex vivo proton nuclear magnetic resonance spectroscopy. Neurochem Int 62:502-509
52. Lee H, Holburn GE, Price RR (2001) In vivo and in vitro proton NMR spectroscopic studies of thiamine-deficient rat brains. J Magn Reson Imaging 13:163-166
53. Lester D, Freed EX (1973) Criteria for an animal model of alcoholism. Pharmacol Biochem Behav 1:103-107
54. Lewohl JM, Wixey J, Harper CG, Dodd PR (2005) Expression of MBP, PLP, MAG, CNP, and GFAP in the human alcoholic brain. Alcohol Clin Exp Res 29:1698-1705
55. Li TK, Lumeng L, McBride WJ, Murphy JM (1987) Rodent lines selected for factors affecting alcohol consumption. Alcohol Alcohol Suppl 1:91-96
56. Lieber CS (1991) Perspectives: do alcohol calories count? Am J Clin Nutr 54:976-982
57. Lien YH, Shapiro JI, Chan L (1990) Effects of hypernatremia on organic brain osmoles. J Clin Invest 85:1427-1435
58. Likar B, Viergever MA, Pernus F (2001) Retrospective correction of MR intensity inhomogeneity by information minimization. IEEE Trans Med Imaging 20:1398-1410
59. Lumeng L, Hawkins TD, Li TK (1977) New strains of rats with alcohol preference and nonpreference. In: Thurman RG, Williamson JR, Drott HR, Chance B (eds) Alcohol and aldehyde metabolizing systems. Academic, New York, pp 537-544
60. Mader I, Rauer S, Gall P, Klose U (2008) (1)H MR spectroscopy of inflammation, infection and ischemia of the brain. Eur J Radiol 67:250-257
61. Majchrowicz E (1975) Induction of physical dependence upon ethanol and the associated behavioral changes in rats. Psychopharmacologia 43:245-254
62. Mann K, Mundle G, Langle G, Petersen D (1993) The reversibility of alcoholic brain damage is not due to rehydration: a CT study. Addiction 88:649-653
63. Mayer D, Spielman DM (2005) Detection of glutamate in the human brain at 3 T using optimized constant time point resolved spectroscopy. Magn Reson Med 54:439-442
64. McBride WJ, Chernet E, Dyr W, Lumeng L, Li TK (1993) Densities of dopamine D2 receptors are reduced in CNS regions of alcohol-preferring P rats. Alcohol 10:387-390
65. McBride WJ, Kimpel MW, McClintick JN, Ding ZM, Hyytia P, Colombo G, Edenberg HJ, Lumeng L, Bell RL (2012) Gene expression in the ventral tegmental area of 5 pairs of rat lines selectively bred for high or low ethanol consumption. Pharmacol Biochem Behav 102:275-285
66. McBride WJ, Li TK (1998) Animal models of alcoholism: neurobiology of high alcohol-drinking behavior in rodents. Crit Rev Neurobiol 12:339-369
67. Miguel-Hidalgo JJ (2005) Lower packing density of glial fibrillary acidic protein-immunoreactive astrocytes in the prelimbic cortex of alcohol-naive and alcohol-drinking alcohol-preferring rats as compared with alcohol-nonpreferring and Wistar rats. Alcohol Clin Exp Res 29:766-772
68. Moffett JR, Ross B, Arun P, Madhavarao CN, Namboodiri AM (2007) N-Acetylaspartate in the CNS: from neurodiagnostics to neurobiology. Prog Neurobiol 81:89-131
69. Murphy JM, McBride WJ, Lumeng L, Li TK (1987) Contents of monoamines in forebrain regions of alcohol-preferring (P) and -nonpreferring (NP) lines of rats. Pharmacol Biochem Behav 26:389-392
70. Murphy JM, Stewart RB, Bell RL, Badia-Elder NE, Carr LG, McBride WJ, Lumeng L, Li TK (2002) Phenotypic and genotypic characterization of the Indiana University rat lines selectively bred for high and low alcohol preference. Behav Genet 32:363-388
71. Murphy JM, Waller MB, Gatto GJ, McBride WJ, Lumeng L, Li TK (1988) Effects of fluoxetine on the intragastric self-administration of ethanol in the alcohol preferring P line of rats. Alcohol 5:283-286
72. Oscar-Berman M, Marinkovic K (2007) Alcohol: effects on neurobehavioral functions and the brain. Neuropsychol Rev 17:239-257
73. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates. Elsevier Academic, San Diego
74. Pfefferbaum A, Adalsteinsson E, Bell RL, Sullivan EV (2007) Development and resolution of brain lesions caused by pyrithiamine- and dietary-Induced thiamine deficiency and alcohol exposure in the alcohol-preferring rat: a longitudinal magnetic resonance imaging and spectroscopy study. Neuropsychopharmacology 32:1149-1177
75. Pfefferbaum A, Rosenbloom M, Rohlfing T, Sullivan EV (2009) Degradation of association and projection white matter systems in alcoholism detected with quantitative fiber tracking. Biol Psychiatry 65:680-690
76. Pfefferbaum A, Rosenbloom M, Serventi KL, Sullivan EV (2002) Corpus callosum, pons, and cortical white matter in alcoholic women. Alcohol Clin Exp Res 26:400-406
77. Pfefferbaum A, Sullivan EV, Mathalon DH, Shear PK, Rosenbloom MJ, Lim KO (1995) Longitudinal changes in magnetic resonance imaging brain volumes in abstinent and relapsed alcoholics. Alcohol Clin Exp Res 19:1177-1191
78. Pfefferbaum A, Zahr NM, Mayer D, Vinco S, Orduna J, Rohlfing T, Sullivan EV (2008) Ventricular expansion in wild-type Wistar rats after alcohol exposure by vapor chamber. Alcohol Clin Exp Res 32:1459-1467
79. Pitkin SR, Savage LM (2001) Aging potentiates the acute and chronic neurological symptoms of pyrithiamine-induced thiamine deficiency in the rodent. Behav Brain Res 119:167-177
80. Rivier C, Vale W (1983) Influence of ethanol on reproductive functions of the adult male rat as a function of body weight. Alcohol Clin Exp Res 7:210-212
81. Roberts AJ, Cole M, Koob GF (1996) Intra-amygdala muscimol decreases operant ethanol self-administration in dependent rats. Alcohol Clin Exp Res 20:1289-1298
82. Rodd-Henricks ZA, McKinzie DL, Murphy JM, McBride WJ, Lumeng L, Li TK (2000) The expression of an alcohol deprivation effect in the high-alcohol-drinking replicate rat lines is dependent on repeated deprivations. Alcohol Clin Exp Res 24:747-753
83. Ross B, Bluml S (2001) Magnetic resonance spectroscopy of the human brain. Anat Rec 265:54-84
84. Ruiz SM, Oscar-Berman M, Sawyer KS, Valmas MM, Urban T, Harris GJ (2013) Drinking history associations with regional white matter volumes in alcoholic men and women. Alcohol Clin Exp Res 37:110-122
85. Sartorius A, Lugenbiel P, Mahlstedt MM, Ende G, Schloss P, Vollmayr B (2008) Proton magnetic resonance spectroscopic creatine correlates with creatine transporter protein density in rat brain. J Neurosci Methods 172:215-219
86. Sasaki O, Hattori N, Nakahama H, Inoue N, Nakamura S, Inenaga T, Kohno S, Sawada T, Kawano Y (2006) Positive correlations between cerebral choline and renal dysfunction in chronic renal failure. Neuroradiology 48:300-306
87. Silva SM, Madeira MD, Ruela C, Paula-Barbosa MM (2002) Prolonged alcohol intake leads to irreversible loss of vasopressin and oxytocin neurons in the paraventricular nucleus of the hypothalamus. Brain Res 925:76-88
88. Sim E, Pasternak CA (1976) The metabolism of the phosphonium analogue of choline in cultured cells. A useful nuclear-magnetic-resonance probe for membrane phosphatidylcholine. Biochem J 154:105-111
89. Smith DG, Learn JE, McBride WJ, Lumeng L, Li TK, Murphy JM (2001) Alcohol-naive alcohol-preferring (P) rats exhibit higher local cerebral glucose utilization than alcohol-nonpreferring (NP) and Wistar rats. Alcohol Clin Exp Res 25:1309-1316
90. Sonn J, Mayevsky A (2001) The effect of ethanol on metabolic, hemodynamic and electrical responses to cortical spreading depression. Brain Res 908:174-186
91. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417-463
92. Strother WN, Chernet EJ, Lumeng L, Li TK, McBride WJ (2001) Regional central nervous system densities of delta-opioid receptors in alcohol-preferring P, alcohol-nonpreferring NP, and unselected Wistar rats. Alcohol 25:31-38
93. Sullivan EV, Pfefferbaum A (2005) Neurocircuitry in alcoholism: a substrate of disruption and repair. Psychopharmacology (Berl)
94. Tedeschi G, Lundbom N, Raman R, Bonavita S, Duyn J, Alger J, Di Chiro G (1997) Increased choline signal coinciding with malignant degeneration of cerebral gliomas: a serial proton magnetic resonance spectroscopy imaging study. J Neurosurg 87:516-524
95. Thielen RJ, McBride WJ, Chernet E, Lumeng L, Li TK (1997) Regional densities of benzodiazepine sites in the CNS of alcohol-naive P and NP rats. Pharmacol Biochem Behav 57:875-882
96. Thielen RJ, McBride WJ, Lumeng L, Li TK (1993) Housing conditions alter GABAA receptor of alcohol-preferring and -nonpreferring rats. Pharmacol Biochem Behav 46:723-727
97. Trovarelli G, De Medio GE, Montanini I (1982) The influence of CDP-choline on brain lipid metabolism during ischemia. Farmaco [Sci] 37:663-668
98. Waller MB, McBride WJ, Lumeng L, Li TK (1983) Initial sensitivity and acute tolerance to ethanol in the P and NP lines of rats. Pharmacol Biochem Behav 19:683-686
99. Weiss F, Lorang MT, Bloom FE, Koob GF (1993) Oral alcohol self-administration stimulates dopamine release in the rat nucleus accumbens: genetic and motivational determinants. J Pharmacol Exp Ther 267:250-258
100. Witzmann FA, Li J, Strother WN, McBride WJ, Hunter L, Crabb DW, Lumeng L, Li TK (2003) Innate differences in protein expression in the nucleus accumbens and hippocampus of inbred alcohol-preferring and -nonpreferring rats. Proteomics 3:1335-1344
101. Yaksh TL, Kohl RL, Rudy TA (1977) Induction of tolerance and withdrawal in rats receiving morphine in the spinal subarachnoid space. Eur J Pharmacol 42:275-284
102. Zahr NM, Luong R, Sullivan EV, Pfefferbaum A (2010a) Measurement of serum, liver, and brain cytokine induction, thiamine levels, and hepatopathology in rats exposed to a 4-day alcohol binge protocol. Alcohol Clin Exp Res 34:1858-1870
103. Zahr NM, Mayer D, Rohlfing T, Hasak M, Hsu O, Vinco S, Orduna J, Luong R, Sullivan EV, Pfefferbaum A (2010b) Brain injury and recovery following binge ethanol: evidence from in vivo magnetic resonance spectroscopy. Biol Psychiatry 67:846-854
104. Zahr NM, Mayer D, Rohlfing T, Orduna J, Luong R, Sullivan EV, Pfefferbaum A (2013) A mechanism of rapidly reversible cerebral ventricular enlargement independent of tissue atrophy. Neuropsychopharmacology 38:1121-1129
105. Zahr NM, Mayer D, Vinco S, Orduna J, Luong R, Sullivan EV, Pfefferbaum A (2009) In vivo evidence for alcohol-induced neurochemical changes in rat brain without protracted withdrawal, pronounced thiamine deficiency, or severe liver damage. Neuropsychopharmacology 34:1427-1442
106. Zawada ET, Jr. (1996) Malnutrition in the elderly. Is it simply a matter of not eating enough? Postgrad Med 100: 207-8, 211-4, 220-2 passim
107. Zhou FC, Bledsoe S, Lumeng L, Li TK (1991) Immunostained serotonergic fibers are decreased in selected brain regions of alcohol-preferring rats. Alcohol 8:425-431
108. Zhou FC, Zhang JK, Lumeng L, Li TK (1995) Mesolimbic dopamine system in alcohol-preferring rats. Alcohol 12:403-412
109. Zipursky RB, Lim KO, Pfefferbaum A (1989) MRI study of brain changes with short term abstinence from alcohol. Alcohol Clin Exp Res 13:664-666