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

Volumn 32, Issue 5, 2007, Pages 1159-1177

  Pfefferbaum, Adolf ^a,b   Adalsteinsson, Elfar ^c,d   Bell, Richard L ^e   Sullivan, Edith V ^b  

^a SRI INTERNATIONAL   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d Department of Electrical Engineering and Computer Science   (United States)

^e INDIANA UNIVERSITY   (United States)

Author keywords

Alcohol; Longitudinal; MRI; MRS; Pyrithiamine; Rat; Thiamine

Indexed keywords

ALCOHOL; CHOLINE; CREATINE; GLUTAMIC ACID; N ACETYLASPARTIC ACID; PYRITHIAMINE; THIAMINE; WATER;

ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; BRAIN FOURTH VENTRICLE; BRAIN GROWTH; BRAIN LEVEL; BRAIN NERVE CELL; CLUSTER ANALYSIS; CONTROLLED STUDY; CORPUS CALLOSUM; DATA ANALYSIS; HIPPOCAMPUS; IN VIVO STUDY; INFERIOR COLLICULUS; LATERAL BRAIN VENTRICLE; MAMMILLARY BODY; METABOLITE; NEUROLOGIC DISEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARENCHYMA; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPECTROSCOPY; THALAMUS; THIAMINE DEFICIENCY; WERNICKE ENCEPHALOPATHY;

ALCOHOL-INDUCED DISORDERS, NERVOUS SYSTEM; ALCOHOLISM; ANIMALS; ANTIMETABOLITES; BIOLOGICAL MARKERS; BRAIN; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DISEASE MODELS, ANIMAL; ETHANOL; KORSAKOFF SYNDROME; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NERVE DEGENERATION; PYRITHIAMINE; RATS; RATS, WISTAR; SURVIVAL RATE; THIAMINE; THIAMINE DEFICIENCY;

EID: 34247345425     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1301107     Document Type: Article

References (132)

1. Acara M, Alletto JJ, Dlugos C, Pentney R (1995). Small animal MRI. Alcohol Health Res World 4: 321-324.
2. 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 3T clinical human scanner. Neuroimage 22: 381-386.
3. 1H magnetic resonance spectroscopic imaging (abs). Presented at Alzheimer's Imaging Consortium, Washington, DC, July 8.
4. Adalsteinsson E, Sullivan EV, Mayer D, Pfefferbaum A (2006). In vivo quantification of ethanol kinetics in rat brain. Neuropsychopharmacology [Epub ahead of print January 11].
5. Agartz I, Momenan R, Rawlings RR, Kerich MJ, Hommer DW (1999). Hippocampal volume in patients with alcohol dependence. Arch Gen Psychiatry 56: 356-363.
6. Baker K, Harding A, Halliday G, Kril J, Harper C (1999). Neuronal loss in functional zones of the cerebellum of chronic alcoholics with and without Wernicke's encephalopathy. Neuroscience 91: 429-438.
7. Bell RL, Rodd ZA, Murphy JM, McBride WJ (2005). Use of selectively bred alcohol-preferring rats to study alcohol abuse, relapse and craving. In: Preedy VR, Watson RR (eds). Comprehensive Handbook of Alcohol Related Pathology, Vol 3. New York: Academic Press, Elsevier Science. pp 1515-1533.
8. Bender L, Schilder P (1933). Encphalopathia alcoholica: polioencephalitis haemorrhagica superior of Wernicke. Arch Neurol Psychiatry 29: 990-1053.
9. Bendszus M, Weijers HG, Wiesbeck G, Warmuth-Metz M, Bartsch AJ, Engels S et al (2001). Sequential MR imaging and proton MR spectroscopy in patients who underwent recent detoxification for chronic alcoholism: correlation with clinical and neuropsychological data. Am J Neuroradiol 22: 1926-1932.
10. Blansjaar B, Vielvoye G, van Dijk J, Rijnders R (1992). Similar brain lesions in alcoholics and Korsakoff patients: MRI, psychometric and clinical findings. Clin Neurol Neurosurg 93: 197-203.
11. Bloom FE, Hoffer BJ, Siggins GR, Barker JL, Nicoll RA (1972). Effects of serotonin on central neurons: microiontophoretic administration. Fed Proc 31: 97-106.
12. Butters N, Cermak LS (1980). Alcoholic Korsakoff's Syndrome: An Information Processing Approach to Amnesia. Academic Press Inc.: New York.
13. Butterworth RF (1993). Pathophysiology of cerebellar dysfunction in the Wernicke-Korsakoff syndrome. Can J Neurol Sci 20: S123-S126.
14. Caine D, Halliday GM, Kril JJ, Harper CG (1997). Operational criteria for the classification of chronic alcoholics: identification of Wernicke's encephalopathy. J Neurol Neurosurg Psychiatry 62: 51-60.
15. Cardenas VA, Studholme C, Meyerhoff DJ, Song E, Weiner MW (2005). Chronic active heavy drinking and family history of problem drinking modulate regional brain tissue volumes. Psychiatry Res 138: 115-130.
16. Carlen PL, Wortzman G, Holgate RC, Wilkinson DA, Rankin JG (1978). Reversible cerebral atrophy in recently abstinent chronic alcoholics measured by computed tomography scans. Science 200: 1076-1078.
17. Charness ME (1993). Brain lesions in alcoholics. Alcohol Clin Exp Res 17: 2-11.
18. Charness ME (1999). Intracranial voyeurism: revealing the mammillary bodies in alcoholism. Alcohol Clin Exp Res 23: 1941-1944.
19. Charness ME, DeLaPaz RL (1987). Mammillary body atrophy in Wernicke's encephalopathy: antemortem identification using magnetic resonance imaging. Ann Neurol 22: 595-600.
20. Chu K, Kang DW, Kim HJ, Lee YS, Park SH (2002). Diffusion-weighted imaging abnormalities in wernicke encephalopathy: reversible cytotoxic edema? Arch Neurol 59: 123-127.
21. 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.
22. Davila MD, Shear PK, Lane B, Sullivan EV, Pfefferbaum A (1994). Mammillary body and cerebellar shrinkage in chronic alcoholics: an MRI and neuropsychological study. Neuropsychology 8: 433-444.
23. De Bellis MD, Narasimhan A, Thatcher DL, Keshavan MS, Soloff P, Clark DB (2005). 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 29: 1590-1600.
24. Dixon G, Harper CG (2001). Quantitative analysis of glutamic acid decarboxylase-immunoreactive neurons in the anterior thalamus of the human brain. Brain Res 923: 39-44.
25. Dlugos CA, Pentney RJ (1997). Morphometric evidence that the total number of synapses on Purkinje neurons of old F344 rats is reduced after long-term ethanol treatment and restored to control levels after recovery. Alcohol Alcoholism 32: 161-172.
26. Doraiswamy PM, Massey EW, Enright K, Palese VJ, Lamonica D, Boyko O (1994). Wernicke-Korsakoff syndrome caused by psychogenic food refusal - MR findings. Am J Neuroradiol 15: 594-596.
27. Dreher W, Leibfritz D (1995). On the use of two-dimensional-J NMR measurements for in vivo proton MRS: measurement of homonuclear decoupled spectra without the need for short echo times. Magn Reson Med 34: 331-337.
28. Durazzo TC, Gazdzinski S, Banys P, Meyerhoff DJ (2004). Cigarette smoking exacerbates chronic alcohol-induced brain damage: a preliminary metabolite imaging study. Alcoholism Clin Exp Res 28: 1849-1860.
29. Eckardt M, File S, Gessa G, Grant K, Guerri C, Hoffman P et al (1998). Effects of moderate alcohol consumption on the central nervous system. Alcohol Clin Exp Res 22: 351-359.
30. Ende G, Welzel H, Walter S, Weber-Fahr W, Diehl A, Hermann D et al (2005). Monitoring the effects of chronic alcohol consumption and abstinence on brain metabolism: a longitudinal proton magnetic resonance spectroscopy study. Biol Psychiatry 58: 974-980.
31. Fein G, Bachman L, Fisher S, Davenport L (1990). Cognitive impairments in abstinent alcoholics. Western J Med 152: 531-537.
32. Fein G, Di Sclafani V, Cardenas VA, Goldmann H, Tolou-Shams M, Meyerhoff DJ (2002). Cortical gray matter loss in treatment-naive alcohol dependent individuals. Alcohol Clin Exp Res 26: 558-564.
33. Fein G, Meyerhoff D, Di Sclafani V, Ezekiel F, Poole N, MacKay S et al (1994). H magnetic resonance spectroscopic imaging separates neuronal from glial changes in alcohol-related brain atrophy. In: Lancaster F (ed). Alcohol and Glial Cells NIAAA Research Monograph # 27. US Government Printing Office: Bethesda, MD. pp 227-241.
34. Gazdzinski S, Durazzo TC, Meyerhoff DJ (2005). Temporal dynamics and determinants of whole brain tissue volume changes during recovery from alcohol dependence. Drug Alcohol Depend 78: 263-273.
35. Haase A, Frahm J, Hanicke W, Matthaei D (1985). H NMR chemical shift selective (CHESS) imaging. Phys Med Biol 30: 341-344.
36. Halliday G, Baker K, Harper C (1995). Serotonin and alcohol-related brain damage. Metab Brain Dis 10: 25-30.
37. Harper C, Butterworth R (1997). Nutritional and metabolic disorders. In: Graham DI, Lantos PL (eds). Greenfield's Neuropathology. London: Arnold. pp 601-642.
38. Harper C, Fornes P, Duyckaerts C, Lecomte D, Hauw JJ (1995). An international perspective on the prevalence of the Wernicke-Korsakoff syndrome. Metab Brain Dis 10: 17-24.
39. Harper CG, Kril JJ (1988). Corpus callosal thickness in alcoholics. Br J Addict 83: 577-580.
40. Harper CG, Kril JJ (1990). Neuropathology of alcoholism. Alcohol Alcohol 25: 207-216.
41. Harper CG, Sheedy DL, Lara AI, Garrick TM, Hilton JM, Raisanen J (1998). Prevalence of Wernicke-Korsakoff syndrome in Australia: has thiamine fortification made a difference? Med J Aust 168: 542-545.
42. Hurd RE (2000). Magnetic resonance spectroscopic imaging having reduced parasitic side band signals. United States patent no. 6,069,478, May 30, 2000.
43. Hurd RE, Gurr D, Sailasuta N (1998). Proton spectroscopy without water suppression: the oversampled J-resolved experiment. Magn Reson Med 40: 343-347.
44. Irle E, Markowitsch HJ (1983). Widespread neuroanatomical damage and learning deficits following chronic alcohol consumption or vitamin-B1 (thiamine) deficiency in rats. Behav Brain Res 9: 277-294.
45. Jagannathan NR, Desai NG, Raghunathan P (1996). Brain metabolite changes in alcoholism: an in vivo proton magnetic resonance spectroscopy (MRS) study. Magn Reson Imaging 14: 553-557.
46. Jernigan TL, Butters N, DiTraglia G, Schafer K, Smith T, Irwin M et al (1991). Reduced cerebral grey matter observed in alcoholics using magnetic resonance imaging. Alcohol Clin Exp Res 15: 418-427.
47. Jolliffe N, Wortis H, Fein HD (1941). The Wernicke syndrome. Arch Neurol Psychiatry 46: 569-597.
48. Jordan LR, Zelaya FO, Rose SE, Bower AJ, Galloway G, Wholohan T et al (1998). Changes in the hippocampus induced by glucose in thiamine deficient rats detected by MRI. Brain Res 791: 347-351.
49. Kopelman MD (1995). The Korsakoff syndrome. Br J Psychiatry 166: 154-173.
50. Kril JJ, Halliday GM, Svoboda MD, Cartwright H (1997). The cerebral cortex is damaged in chronic alcoholics. Neuroscience 79: 983-998.
51. Langlais PJ, Mair RG, Anderson CD, McEntee WJ (1988). Longlasting changes in regional brain amino acids and monoamines in recovered pyrithiamine treated rats. Neurochem Res 13: 1199-1206.
52. Langlais PJ, Savage LM (1995). Thiamine deficiency in rats produces cognitive and memory deficits on spatial tasks that correlate with tissue loss in diencephalon, cortex and white matter. Behav Brain Res 68: 75-89.
53. 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.
54. 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.
55. Lee H, Holburn GH, Price RR (2003). Proton MR spectroscopic studies of chronic alcohol exposure on the rat brain. J Magn Reson Imaging 18: 147-151.
56. Lee H, Tarter J, Holbourn GE, Price RR, Weinstein DD, Martin PR (1995). In vivo localized proton NMR spectroscopy of thiamine-deficient rat brain. Magn Reson Med 34: 313-318.
57. Li TK, Lumeng L, McBride WJ, Waller MB (1979). Progress toward a voluntary oral consumption model of alcoholism. Drug Alcohol Depend 4: 45-60.
58. Lieber CS (2003a). Relationships between nutrition, alcohol and liver disease. Alcohol Res Health 27: 220-231.
59. Lieber CS (2003b). Relationships between nutrition, alcohol use, and liver disease. Alcohol Res Health 27: 220-231.
60. Lu W, Jaatinen P, Rintala J, Sarviharju M, Kiianmaa K, Hervonen A (1997). Effects of lifelong ethanol consumption on rat locus coeruleus. Alcohol Alcohol 32: 463-470.
61. Mann K, Gunther A, Stetter F, Ackermann K (1999). Rapid recovery from cognitive deficits in abstinent alcoholics: a controlled test-retest study. Alcohol Alcohol 34: 567-574.
62. Martin PR, Gibbs SJ, Nimmerrichter AA, Riddle WR, Welch LW, Willcott MR (1995). Brain proton magnetic resonance spectroscopy studies in recently abstinent alcoholics. Alcohol Clin Exp Res 19: 1078-1082.
63. Martin PR, Rio D, Adinoff B, Johnson JL, Bisserbe J-C, Rawlings RR et al (1992). Regional cerebral glucose utilization in chronic organic mental disorders associated with alcoholism. J Neuropsychiatry Clin Neurosci 4: 159-167.
64. Martin PR, Singleton CK, Hiller-Sturmhofel S (2003). The role of thiamine deficiency in alcoholic brain disease. Alcohol Res Health 27: 134-142.
65. Mason GF, Petrakis IL, de Graaf RA, Gueorguieva R, Guidone E, Coric V et al (2006). Cortical gamma-aminobutyric acid levels and the recovery from ethanol dependence: preliminary evidence of modification by cigarette smoking. Biol Psychiatry 59: 85-93.
66. Mayer D, Zahr NM, Sullivan EV, Pfefferbaum A (2006). Differences in cerebellar and striatal metabolite ratios in rat brain detected in vivo with optimized CT-PRESS at 3T (abs). Presented at International Society for Magnetic Resonance in Medicine, Seattle, WA, May.
67. McBride WJ, Li TK (1998). Animal models of alcoholism: neurobiology of high alcohol-drinking behavior in rodents. Crit Rev Neurobiol 12: 339-369.
68. McBride WJ, Murphy JM, Gatto GJ, Levy AD, Lumeng L, Li TK (1991). Serotonin and dopamine systems regulating alcohol intake. Alcohol Alcohol 1: 411-416.
69. Meyerhoff DJ, Blumenfeld R, Truran D, Lindgren J, Flenniken D, Cardenas V et al (2004). Effects of heavy drinking, binge drinking, and family history of alcoholism on regional brain metabolites. Alcohol Clin Exp Res 28: 650-661.
70. Mulholland PJ, Self RL, Stepanyan TD, Little HJ, Littleton JM, Prendergast MA (2005). Thiamine deficiency in the pathogenesis of chronic ethanol-associated cerebellar damage in vitro. Neuroscience 135: 1129-1139.
71. Murata T, Fujito T, Kimura H, Omori M, Itoh H, Wada Y (2001). Serial MRI and (1)H-MRS of Wernicke's encephalopathy: report of a case with remarkable cerebellar lesions on MRI. Psychiatry Res 108: 49-55.
72. Murphy JM, Stewart RB, Bell RL, Badia-Elder NE, Carr LG, McBride WJ et al (2002). Phenotypic and genotypic characterization of the Indiana University rat lines selectively bred for high and low alcohol preference. Behavior Genetics 32: 363-388.
73. Nixon K, Crews FT (2002). Binge ethanol exposure decreases neurogenesis in adult rat hippocampus. J Neurochem 83: 1087-1093.
74. Nixon K, Crews FT (2004). Temporally specific burst in cell proliferation increases hippocampal neurogenesis in protracted abstinence from alcohol. J Neurosci 24: 9714-9722.
75. O'Neill J, Cardenas VA, Meyerhoff DJ (2001). Effects of abstinence on the brain: quantitative magnetic resonance imaging and magnetic resonance spectroscopic imaging in chronic alcohol abuse. Alcohol Clin Exp Res 25: 1673-1682.
76. Papez JW (1937). A proposed mechanism of emotion. Arch Neurol 38: 725-743.
77. Parks MH, Dawant BM, Riddle WR, Hartmann SL, Dietrich MS, Nickel MK et al (2002). Longitudinal brain metabolic characterization of chronic alcoholics with proton magnetic resonance spectroscopy. Alcohol Clin Exp Res 26: 1368-1380.
78. Parsons O (1993). Impaired neuropsychological cognitive functioning in sober alcoholics. In: Hunt WA, Nixon SJ (eds). Alcohol Induced Brain Damage, NIAAA Research Monograph No. 22 National Institutes of Health: Rockville, MD. pp 173-194.
79. Pentney RJ, Alletto JJ, Acara MA, Dlugos CA, Fiel RJ (1993). Small animal magnetic resonance imaging: a means of studying the development of structural pathologies in the rat brain. Alcohol Clin Exp Res 17: 1301-1308.
80. Pentney RJ, Dlugos CA (2000). Cerebellar Purkinje neurons with altered terminal dendritic segments are present in all lobules of the cerebellar vermis of ageing, ethanol-treated F344 rats. Alcohol Alcohol 35: 35-43.
81. Pentney RJ, Quackenbush LJ (1990). Dendritic hypertrophy in Purkinje neurons of old Fischer 344 rats after long-term ethanol treatment. Alcohol Clin Exp Res 14: 878-886.
82. Petroff O, Ogino T, Alger J, Prichard J (1991). Regional variation in metabolite concentration and the effect of post-mortem autolysis: a magnetic resonance spectroscopy study of brain biopsy material. Society of Magnetic Resonance in Medicine Conference Abstracts Vol 61.
83. Petroff OAC, Pleban LA, Spencer DD (1995). Symbiosis between in vivo and in vitro NMR spectroscopy: the creatine, N-acetylaspartate, glutamate and GABA content of the epileptic human brain. Magn Reson Imaging 13: 1197-1211.
84. Pfefferbaum A, Adalsteinsson E, Sood R, Mayer D, Bell RL, McBride WJ et al (2006). Part II: longitudinal brain MRI study of the alcohol-preferring (P) rat: effects of voluntary chronic alcohol consumption. Alcohol Clin Exp Res (in press).
85. Pfefferbaum A, Adalsteinsson E, Spielman D, Sullivan EV, Lim KO (1999a). In vivo brain concentrations of N-acetyl compounds, creatine and choline in Alzheimer's disease. Arch Gen Psychiatry 56: 185-192.
86. Pfefferbaum A, Adalsteinsson E, Spielman D, Sullivan EV, Lim KO (1999b). In vivo spectroscopic quantification of the N-acetyl moiety, creatine and choline from large volumes of gray and white matter: effects of normal aging. Magn Reson Med 41: 276-284.
87. Pfefferbaum A, Adalsteinsson E, Sullivan EV (2004a). In vivo structural imaging of the rat brain with a 3T clinical human scanner. J Magn Reson Imaging 20: 779-785.
88. Pfefferbaum A, Adalsteinsson E, Sullivan EV (2005). Cortical NAA deficits in HIV infection without dementia: influence of alcoholism comorbidity. Neuropsychopharmacology 30: 1392-1399.
89. Pfefferbaum A, Lim KO, Zipursky RB, Mathalon DH, Lane B, Ha CN et al (1992). Brain gray and white matter volume loss accelerates with aging in chronic alcoholics: a quantitative MRI study. Alcohol Clin Exp Res 16: 1078-1089.
90. Pfefferbaum A, Rosenbloom MJ, Serventi KL, Sullivan EV (2004b). Brain volumes, RBC status, and hepatic function in alcoholics after 1 and 4 weeks of sobriety: predictors of outcome. Am J Psychiatry 161: 1190-1196.
91. Pfefferbaum A, Sullivan EV, Mathalon DH, Lim KO (1997). Frontal lobe volume loss observed with magnetic resonance imaging in older chronic alcoholics. Alcohol Clin Exp Res 21: 521-529.
92. 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.
93. Pfefferbaum A, Sullivan EV, Rosenbloom MJ, Mathalon DH, Lim KO (1998). A controlled study of cortical gray matter and ventricular changes in alcoholic men over a five year interval. Arch Gen Psychiatry 55: 905-912.
94. 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.
95. Plaitakis A, Nicklas WJ, Berl S (1978). Thiamine deficiency: selective impairment of the cerebellar serotonergic system. Neurology 28: 691-698.
96. Riley JN, Walker DW (1978). Morphological alterations in hippocampus after long-term alcohol consumption in mice. Science 201: 646-648.
97. Rintala J, Jaatinen P, Lu W, Sarviharju M, Eriksson CJ, Laippala P et al (1997). Effects of lifelong ethanol consumption on cerebellar layer volumes in AA and ANA rats. Alcohol Clin Exp Res 21: 311-317.
98. 1H MRS to study biochemical changes in the thiamine deficient rat brain under glucose load. NMR Biomed 6: 324-328.
99. Savage LM, Candon PM, Hohmann HL (2000). Alcohol-induced brain pathology and behavioral dysfunction: using an animal model to examine sex differences. Alcohol Clin Exp Res 24: 465-475.
100. Schroth G, Naegele T, Klose U, Mann K, Petersen D (1988). Reversible brain shrinkage in abstinent alcoholics, measured by MRI. Neuroradiology 30: 385-389.
101. Schroth G, Wichmann W, Valavanis A (1991). Blood-brain-barrier disruption in acute Wernicke encephalopathy: MR findings. J Comput Assist Tomogr 15: 1059-1061.
102. Schweinsburg B, Taylor M, Videen J, Alhassoon O, Patterson T, Grant I (2000). Elevated myo-inositol in gray matter of recently detoxified but not long-term abstinent alcoholics: a preliminary MR spectroscopy study. Alcohol Clin Exp Res 24: 699-705.
103. Schweinsburg BC, Alhassoon OM, Taylor MJ, Gonzalez R, Videen JS, Brown GG et al (2003). Effects of alcoholism and gender on brain metabolism. Am J Psychiatry 160: 1180-1183.
104. 1H magnetic resonance spectroscopy investigation of alcohol-associated frontal lobe injury. Alcohol Clin Exp Res 25: 924-934.
105. Seitz D, Widmann U, Seeger U, Nagele T, Klose U, Mann K et al (1999). Localized proton magnetic resonance spectroscopy of the cerebellum in detoxifying alcoholics. Alcohol Clin Exp Res 23: 158-163.
106. Shear PK, Sullivan EV, Lane B, Pfefferbaum A (1996). Mammillary body and cerebellar shrinkage in chronic alcoholics with and without amnesia. Alcohol Clin Exp Res 20: 1489-1495.
107. Sullivan EV (2000). Human brain vulnerability to alcoholism: evidence from neuroimaging studies. In: Noronha A, Eckardt M, Warren K (eds). Review of NIAAA's Neuroscience and Behavioral Research Portfolio NIAAA Research Monograph No. 34. National Institutes of Health: Bethesda, MD. pp 473-508.
108. Sullivan EV, Adalsteinsson E, Sood R, Mayer D, Bell RL, McBride WJ et al (2006). Part I: longitudinal brain MRI brain study of the alcohol-preferring (P) rat: adult brain growth. Alcohol Clin Exp Res (in press).
109. Sullivan EV, Deshmukh A, Desmond JE, Lim KO, Pfefferbaum A (2000a). Cerebellar volume decline in normal aging, alcoholism, and Korsakoff's syndrome: relation to ataxia. Neuropsychology 14: 341-352.
110. Sullivan EV, Deshmukh A, Desmond JE, Mathalon DH, Rosenbloom MJ, Lim KO et al (2000b). Contribution of alcohol abuse to cerebellar volume deficits in men with schizophrenia. Arch Gen Psychiatry 57: 894-902.
111. Sullivan EV, Lane B, Rosenbloom MJ, Deshmukh A, Desmond J, Lim KO et al (1999). In vivo mammillary body volume deficits in amnesic and nonamnesic alcoholics. Alcohol Clin Exp Res 23: 1629-1636.
112. Sullivan EV, Marsh L (2003). Hippocampal volume deficits in alcoholic Korsakoff's syndrome. Neurology 61: 1716-1719.
113. Sullivan EV, Marsh L, Mathalon DH, Lim KO, Pfefferbaum A (1995). Anterior hippocampal volume deficits in nonamnesic, aging chronic alcoholics. Alcohol Clin Exp Res 19: 110-122.
114. Sullivan EV, Rosenbloom MJ, Lim KO, Pfefferbaum A (2000c). Longitudinal changes in cognition, gait, and balance in abstinent and relapsed alcoholic men: relationships to changes in brain structure. Neuropsychology 14: 178-188.
115. Sullivan EV, Rosenbloom MJ, Serventi KL, Deshmukh A, Pfefferbaum A (2003). The effects of alcohol dependence comorbidity and anti-psychotic medication on volumes of the thalamus and pons in schizophrenia. Am J Psychiatry 160: 1110-1116.
116. Talland GA (1965). Deranged Memory; A Psychonomic Study of the Amnesic Syndrome. Academic Press: New York.
117. Thomson AD, Jeyasingham MD, Pratt OE, Shaw GK (1987). Nutrition and alcoholic encephalopathies. Acta Med Scand Suppl 717: 55-65.
118. Todd K, Butterworth RF (1999). Mechanisms of selective neuronal cell death due to thiamine deficiency. Ann NY Acad Sci 893: 404-411.
119. Torvik A, Lindboe CF, Rodge S (1982). Brain lesions in alcoholics: a neuropathological study with clinical correlations. J Neurol Sci 56: 233-248.
120. Torvik A, Torp S, Lindboe CF (1986). Atrophy of the cerebellar vermis in aging: a morphometric and histologic study. J Neurol Sci 76: 283-294.
121. Unlu E, Cakir B, Asil T (2006). MRI findings of Wernicke encephalopathy revisited due to hunger strike. Eur J Radiol 57: 43-53.
122. Victor M, Adams RD, Collins GH (1971). The Wernicke-Korsakoff Syndrome. Davis Co.: Philadelphia, PA.
123. Victor M, Adams RD, Collins GH (1989). The Wernicke-Korsakoff Syndrome and Related Neurologic Disorders Due to Alcoholism and Malnutrition, 2nd edn. Davis Co.: Philadelphia, PA.
124. Victor M, Herman K, White EE (1959). A psychological study of the Wernicke-Korsakoff syndrome. Results of Wechsler-Bellevue intelligence scale and Wechsler memory scale testing at different stages in the disease. Quart J Stud Alcohol 20: 467-479.
125. Webb P, Sailasuta N, Kohler S, Raidy T, Moats R, Hurd R (1994). Automated single-voxel proton MRS: technical development and multisite verification. Magn Reson Med 31: 365-373.
126. Wiggins RC, Gorman A, Rolsten C, Samorajski T, Ballinger WE, Freund G (1988). Effects of aging and alcohol on the biochemical composition of histologically normal human brain. Metab Brain Dis 3: 67-80.
127. Witt E (1985). Neuroanatomical consequences of thiamine deficiency: a comparative analysis. Alcohol Alcohol 20: 201-221.
128. Zelaya FO, Rose SE, Nixon PF, Wholohan BT, Bower AJ, Zimitat C et al (1995). MRI demonstration of impairment of the blood-CSF barrier by glucose administration to the thiamine-deficient rat brain. Magn Reson Imaging 13: 555-561.
129. Zhong C, Jin L, Fei G (2005). MR imaging of nonalcoholic Wernicke encephalopathy: a follow-up study. AJNR Am J Neuroradiol 26: 2301-2305.
130. Zhou FC, Lumeng L, Li TK (1995). Quantitative immunocytochemical evaluation of serotonergic innervation in alcoholic rat brain. Neurochem Int 26: 135-143.
131. Zimatkin SM, Zimatkina TI (1996). Thiamine deficiency as predisposition to, and consequence of, increased alcohol consumption. Alcohol Alcohol 31: 421-427.
132. Zimitat C, Kril J, Harper CG, Nixon PF (1990). Progression of neurological disease in thiamine-deficient rats is enhanced by ethanol. Alcohol 7: 493-501.