Thiamine deficiency decreases glutamate uptake in the prefrontal cortex and impairs spatial memory performance in a water maze test

Pharmacology Biochemistry and Behavior

Volumn 83, Issue 4, 2006, Pages 481-489

  Carvalho, Fabiana M ^a   Pereira, Silvia R C ^a   Pires, Rita G W ^a   Ferraz, Vany P ^a   Romano Silva, Marco Aurélio ^a   Oliveira Silva, Ieda F ^a   Ribeiro, Angela M ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Chronic ethanol; Glutamate uptake; Prefrontal cortex; Rat; Spatial learning; Spatial memory; Thiamine deficiency

Indexed keywords

ALCOHOL; GLUTAMATE TRANSPORTER;

ALCOHOL CONSUMPTION; AMINO ACID TRANSPORT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; BRAIN DYSFUNCTION; BRAIN REGION; CONTROLLED STUDY; MALE; MAZE TEST; MEMORY DISORDER; METABOLIC TRANSPORT DISORDER; NEUROCHEMISTRY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; TASK PERFORMANCE; THIAMINE DEFICIENCY; VITAMIN DEFICIENCY; WERNICKE KORSAKOFF SYNDROME;

ANIMALS; ETHANOL; GLUTAMIC ACID; MALE; MAZE LEARNING; MEMORY DISORDERS; PREFRONTAL CORTEX; RATS; RATS, WISTAR; SPACE PERCEPTION; THIAMINE DEFICIENCY;

ANIMALIA;

EID: 33746854610     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2006.03.004     Document Type: Article

References (93)

1. Antzoulatos E.G., and Byrne J.H. Learning insights transmitted by glutamate. Trends Neurosci 27 (2004) 555-560
2. Aoki C., and Kabak S. Cholinergic terminals in the cat visual cortex: ultrastructural basis for interaction with glutamate-immunoreactive neurons and other cells. Vis Neurosci 8 (1992) 177-191
3. Astur R.S., Taylor L.B., Mamelak A.N., Philpott L., and Sutherland R.J. Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behav Brain Res 132 (2002) 77-84
4. Ba A., Seri B., and Han S. Thiamine administration during chronic alcohol intake in pregnant and lactating rats: effects on the offspring neurobehavioural development. Alcohol Alcohol 31 (1996) 27-40
5. Bouton M.E. Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biol Psychiatry 52 (2002) 976-986
6. Brandeis R., Brandys Y., and Yehuda S. The use of the Morris water maze in the study of memory and learning. Int J Neurosci 48 (1989) 29-69
7. Brokate B., Hildebrandt H., Eling P., Fichtner H., Runge K., and Timm C. Frontal lobe dysfunctions in Korsakoff's Syndrome and chronic alcoholism: continuity or discontinuity?. Neuropsychology 17 (2003) 420-428
8. Butterworth R.F. Pathophysiology of cerebellar dysfunction in the Wernicke-Korsakoff syndrome. Can J Neurol Sci 20 (1993) 123-126
9. Butterworth R.F. Pathophysiology of alcoholic brain damage: synergistic effects of ethanol, thiamine deficiency and alcoholic liver disease. Metab Brain Dis 10 (1995) 1-8
10. Caulo M., Van Hecke J., Toma L., Ferretti A., Tartaro A., Colosimo C., et al. Functional MRI study of diencephalic amnesia in Wernicke-Korsakoff syndrome. Brain 128 (2005) 1584-1594
11. Chakkalakal D.A., Jerzy R., Novak J.R., Fritz E.D., Mollner T.J., McVicker D.L., et al. Chronic ethanol consumption results in deficient bone repair in rats. Alcohol Alcohol 37 (2002) 13-20
12. Ciccia R.M., and Langlais P.J. 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 (2000) 622-634
13. 1 vitamin deficiency and neuropsychiatric syndromes in alcohol misuse. Alcohol Alcohol 33 (1998) 317-336
14. Danbolt N.C. Glutamate uptake. Prog Neurobiol 65 (2001) 1-105
15. Degenetais E., Thierry A.M., Glowinski J., and Gioanni Y. Synaptic influence of hippocampus on pyramidal cells of the rat prefrontal cortex: an in vivo intracellular recording study. Cereb Córtex 13 (2003) 782-792
16. Delatour B., and Gisquet-Verrier P. Functional role of rat prelimbic-infralimbic cortices in spatial memory: evidence for their involvement in attention and behavioral flexibility. Behav Brain Res 109 (2000) 195-206
17. Devaud L.L. Ethanol dependence has limited effects on GABA or glutamate transporters in rat brain. Alcohol Clin Exp Res 25 (2001) 606-611
18. Dias R., and Aggleton J.P. Effects of selective excitotoxic prefrontal lesions on acquisition of nonmatching- and matching-to-sample in the T-maze in the rat: differential involvement of the prelimbic-infralimbic and anterior cingulate cortices in providing behavioural flexibility. Eur J Neurosci 12 (2000) 4457-4466
19. Doyère V., Burette F., Negro C.R., and Laroche S. Long-term potentiation of hippocampal afferents and efferents to prefrontal cortex: implications for associative learning. Neuropsychologia 31 (1993) 1031-1053
20. Dunkley P.R., Heath J.W., Harrison S.M., Javie P.E., Glenfield P.J., and Rostas J.Á. A rapid percoll gradient procedure for isolation of synaptosomes directly from an S1 fraction: homogeneity and morphology of subcellular fractions. Brain Res 441 (1988) 59-71
21. Férino F., Thierry A.M., and Glowinski J. Anatomical and electrophysiological evidence for a direct projection from Ammon's horn to the medial prefrontal cortex in the rat. Exp Brain Res 65 (1987) 421-426
22. Granon S., and Poucet B. Medial prefrontal lesions in the rat and spatial navigation: evidence for impaired planning. Behav Neurosci 109 (1995) 474-484
23. Granon S., Save E., Buhot M.C., and Poucet B. Effortful information processing in a spontaneous spatial situation by rats with medial prefrontal lesions. Behav Brain Res 78 (1996) 147-154
24. Hakim A.M., and Pappius H.M. Sequence of metabolic, clinical and histological events in experimental thiamin deficiency. Ann Neurol 13 (1983) 365-375
25. Halliday G., Cullen K., and Harding A. Neuropathological correlates of memory dysfunction in the Wernicke-Korsakoff syndrome. Alcohol Alcohol Suppl 2 (1994) 245-251
26. Harper C.G., and Butterworth R.F. Nutritional and metabolic disorders. In: Graham D.I., and Lantos P.L. (Eds). Greensfild's neuropathology (1997), Arnold, London 601-655
27. Hazell A.S., Rao K.V., Danbolt N.C., Pow D.V., and Butterworth R.F. Selective down-regulation of the astrocyte glutamate transporters GLT-1 and GLAST within the medial thalamus in experimental Wernicke's encephalopathy. J Neurochem 78 (2001) 560-568
28. Hazell A.S., Pannunzio P., Rama Rao K.V., Pow D.V., and Rambaldi A. Thiamine deficiency results in downregulation of the GLAST glutamate transporter in cultured astrocytes. Glia 43 (2003) 175-184
29. Hildebrandt H., Brokate B., Eling P., and Lanz M. Response shifting and inhibition, but not working memory, are impaired after long-term heavy alcohol consumption. Neuropsychology 18 (2004) 203-211
30. Homewood J.M., Bond N.W., and Mackenzie A. The effects of single and repeated episodes of thiamin deficiency on memory in alcohol-consuming rat. Alcohol 14 (1997) 81-91
31. Hyde L.A., Stavnezer A.J., Bimonte H.A., Sherman G.F., and Denenberg V.H. Spatial and nonspatial Morris maze learning: impaired behavioral flexibility in mice with ectopias located in the prefrontal cortex. Behav Brain Res 133 (2002) 247-259
32. Janowsky J.S., Shimamura A.P., Kritchevsky M., and Squire L.R. Cognitive impairment following frontal lobe damage and its relevance to human amnesia. Behav Neurosci 103 (1989) 548-560
33. Joyce E.M., and Robbins T.W. Frontal lobe function in Korsakoff and non-Korsakoff alcoholics: planning and spatial working memory. Neuropsychologia 29 (1991) 709-723
34. Keller E., Cummins J.T., and von Hungen K. Regional effects of ethanol on glutamate levels, uptake and release in slice and synaptosome preparations from rat brain. Subst Alcohol Actions/Misuse 4 (1983) 383-392
35. Kim J.H., Lim Y.J., Ro Y.J., Min S.W., Kim C.S., Do S.H., et al. Effects of ethanol on the rat glutamate excitatory amino Acid transporter type 3 expressed in Xenopus oocytes: role of protein kinase C and phosphatidylinositol 3-kinase. Alcohol Clin Exp Res 27 (2003) 1548-1553
36. Kolb B., Sutherland R.J., and Whishaw I.Q. A comparison of the contributions of the frontal and parietal association cortex to spatial localization in rats. Behav Neurosci 97 (1983) 13-27
37. Kopelman M.D. The Korsakoff syndrome. Br J Psychiatry 166 (1995) 154-173
38. Kril J.J., Halliday G.M., Svoboda M.D., and Cartwright H. The cerebral cortex is damaged in chronic alcoholics. Neurosciences 79 (1997) 983-998
39. Kruse M., Navarro D., Desjardins P., and Butterworth R.F. Increased brain endothelial nitric oxide synthase expression in thiamine deficiency: relationship to selective vulnerability. Neurochem Int 45 (2004) 49-56
40. Kubowitz F., and Ott C. Isolierung and Krystallisation eines Garugferments aus Tumoren. Biochem Z 319 (1943) 94-117
41. Kyd R.J., and Bilkey D.K. Prefrontal cortex lesions modify the spatial properties of hippocampal place cells. Cereb Cortex 13 (2003) 444-451
42. Lambe E.K., Picciotto M.R., and Aghajanian G.K. Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex. Neuropsychopharmacology 28 (2003) 216-225
43. Langlais P.J. Alcohol-related thiamine deficiency: impact on memory and cognitive functioning. Alcohol Health Res World 19 (1995) 113-121
44. Langlais P.J., and Savage L.M. 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 (1995) 75-89
45. Langlais P.J., and Zhang S.X. Extracellular glutamate is increased in thalamus during thiamine deficiency-induced lesions and is blocked by MK-801. Neurochemistry 61 (1993) 2175-2182
46. Langlais P.J., and Zhang S.X. Cortical and subcortical white matter damage without Wernicke's encephalopathy after recovery from thiamine deficiency in the rat. Alcohol Clin Exp Res 21 (1997) 434-443
47. Langlais P.J., Mair R.G., Anderson C.D., and McEntee W.J. Monoamines and metabolites in cortex and subcortical structures: normal regional distribution and the effects of thiamine deficiency in the rat. Brain Res 421 (1987) 140-149
48. Langlais P.J., Zhang S.X., and Savage L.M. Neuropathology of thiamine deficiency: an update on the comparative analysis of human disorders and experimental models. Metab Brain Dis 11 (1996) 19-37
49. Lee I., and Kesner R.P. Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. J Neurosci 23 (2003) 1517-1523
50. Linden D.J. The return of the spike: postsynaptic action potentials and the induction of LTP and LTD. Neuron 22 (1999) 661-666
51. Lishman W.A. Alcohol and the brain. Br J Psychiatry 156 (1990) 635-644
52. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 193 (1951) 265-275
53. Mafra R.A., de Oliveira L.C., Ferreira C.A., De Lima M.E., Beirão P.S., and Cruz J.S. Regulation of the glutamate uptake by extracellular calcium. Brain Res 936 (2002) 21-26
54. Mair R.G., Anderson C.D., Langlais P.J., and McEntee W.J. Behavioral impairments, brain lesions and monoaminergic activity in the rat following recovery from a bout of thiamine deficiency. Behav Brain Res 27 (1988) 223-239
55. Mair R.G., Knoth R.L., Rabchenuk S.A., and Langlais P.J. Impairment of olfactory, auditory, and spatial serial reversal learning in rats recovered from pyrithiamine-induced thiamine deficiency. Behav Neurosci 105 (1991) 360-374
56. Mason S.T. The neurochemistry and pharmacology of extinction behavior. Neurosci Biobehav Rev 7 (1983) 325-347
57. Meldrum B., and Garthwaite J. Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Pharmacol Sci 11 (1990) 379-387
58. Miguel-Hidalgo J.J., Wei J., Andrew M., Overholser J.C., Jurjus G., Stockmeier C.A., et al. Glia pathology in the prefrontal cortex in alcohol dependence with and without depressive symptoms. Biol Psychiatry 52 (2002) 1121-1133
59. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11 (1984) 47-60
60. Mumby D.G., Cameli L., and Glenn M.J. Impaired allocentric spatial working memory and intact retrograde memory after thalamic damage caused by thiamine deficiency in rats. Behav Neurosci 113 (1999) 42-50
61. Murata T., Fujito T., Kimura H., Omori M., Itoh H., and Wada Y. Serial MRI and (1)H-MRS of Wernicke's encephalopathy: report of a case with remarkable cerebellar lesions on MRI. Psychiatry Res 108 (2001) 49-55
62. National Research Council. Guide for the care and use of laboratory animals: a report of the Institute of Laboratory Animal Resources Committee on Care and Use of Laboratory Animals (1985), U.S. Department of Health and Human Services, Washington (DC)
63. Othman T., Sinclair C.J., Haughey N., Geiger J.D., and Parkinson F.E. Ethanol alters glutamate but not adenosine uptake in rat astrocytes: evidence for protein kinase C involvement. Neurochem Res 27 (2002) 289-296
64. O'Shea R.D. Roles and regulation of glutamate transporters in the central nervous system. Clin Exp Pharmacol Physiol 29 (2002) 1018-1023
65. Palencia G., Teixeira F., Ortiz A., Perez R., Rios C., and Sotelo J. Detrimental effects of malnutrition on the damage induced by alcoholism: a study of animal models the simulate chronic alcoholism and malnutrition of large human groups. J Stud Alcohol 55 (1994) 113-120
66. Pereira S.R.C., Menezes G.A., Franco G.C., Costa A.E.B., and Ribeiro A.M. Chronic ethanol consumption impairs spatial remote memory in rats but does not affect cortical cholinergic parameters. Pharmacol Biochem Behav 60 (1998) 305-311
67. 3H]glutamate binding sites in brain in thiamine deficiency: results of a quantitative autoradiographic study. Neurochem Res 20 (1995) 1155-1160
68. Pires R.G.W., Pereira S.R.C., Oliveira-Silva I.F., Franco G.C., and Ribeiro A.M. Cholinergic parameters and the retrieval of learned and re-learned spatial information: a study using a model of Wernicke-Korsakoff Syndrome. Behav Brain Res 162 (2005) 11-21
69. Plaitakis A., Hwang E.C., Van Woert M.H., Szilagyi P.I.A., and Berl S. Effect of thiamin deficiency on brain neurotransmitter systems. Ann N Y Acad Sci 378 (1982) 367-381
70. Pronko P., Bardina L., Satanovskaya V., Kuzmich A., and Zimatkin S. Effect of chronic alcohol consumption on the ethanol and acetaldehyde metabolizing systems in the rat gastrointestinal tract. Alcohol Alcohol 37 (2002) 229-335
71. Ragozzino M.E., Wilcox C., Raso M., and Kesner R.P. Involvement of rodent prefrontal cortex subregions in strategy switching. Behav Neurosci 113 (1999) 32-41
72. Rao T.S., Correa L.D., Adams P., Santori E.M., and Sacaan A.I. Pharmacological characterization of dopamine, norepinephrine and serotonin release in the rat prefrontal cortex by neuronal nicotinic acetylcholine receptor agonists. Brain Res 990 (2003) 203-208
73. Reed L.J., Lasserson D., Marsden P., Stanhope N., Stevens T., Bello F., et al. FDG-PET findings in the Wernicke-Korsakoff syndrome. Cortex 39 (2003) 1027-1045
74. Robbins T.W. Arousal systems and attentional processes. Biol Psychol 45 (1997) 57-71
75. Santín L.J., Rubio S., Begega A., and Arias J.L. Effects of chronic alcohol consumption on spatial reference and working memory tasks. Alcohol 20 (2000) 149-159
76. Savage L.M., Pitkin S.R., and Knitowski K.M. Rats exposed to acute pyrithiamine-induced thiamine deficiency are more sensitive to the amnestic effects of scopolamine and MK-801: examination of working memory, response selection, and reinforcement contingencies. Behav Brain Res 104 (1999) 13-26
77. Savage L.M., Chang Q., and Gold P.E. Diencephalic damage decreases hippocampal acetylcholine release during spontaneous alternation testing. Learn Mem 10 (2003) 242-246
78. Sher E., Chen Y., Sharples T.J., Broad L.M., Benedetti G., Zwart R., et al. Physiological roles of neuronal nicotinic receptor subtypes: new insights on the nicotinic modulation of neurotransmitter release, synaptic transmission and plasticity. Curr Top Med Chem 4 (2004) 283-297
79. Smith T.L. Regulation of glutamate uptake in astrocytes continuously exposed to ethanol. Life Sci 61 (1997) 2499-2505
80. Squire L.R. The hippocampus and spatial memory. Trends Neurosci 16 (1993) 56-57
81. Steckler T., Oliveira A.F.M., Dyck C.V., Craenendonck H.V., Mateus A.M.A., Langlois X., et al. Metabotropic glutamate receptor 1 blockade impairs acquisition and retention in a spatial Water maze task. Behav Brain Res 164 14 (2005) 52-60
82. Takita M., Izaki Y., Jay T.M., Kaneko H., and Suzuki S.S. Induction of stable long-term depression in vivo in the hippocampal-prefrontal cortex pathway. Eur J Neurosci 11 (1999) 4145-4148
83. Todd K.G., and Butterworth R.F. Evaluation of the role of NMDA-mediated excitotoxicity in the selective neuronal loss in experimental wernicke encephalopathy. Exp Neurol 149 (1998) 130-138
84. Todd K.G., and Butterworth R.F. In vivo microdialysis in an animal model of neurological disease: thiamine deficiency (Wernicke) encephalopathy. Methods 23 (2001) 55-61
85. Troncoso J.C., Johnston M.V., Hess K.M., Griffin J.W., and Price D.L. Model of Wernicke's encephalopathy. Arch Neurol 38 (1981) 350-354
86. Thomson A.D. Mechanisms of vitamin deficiency in chronic alcohol misusers and the development of the Wernicke-Korsakoff syndrome. Alcohol Alcohol Suppl 35 (2000) 2-7
87. Vickery R.M., Morris S.H., and Bindman L.J. Metabotropic glutamate receptors are involved in long-term potentiation in isolated slices of rat medial frontal cortex. J Neurophysiol 78 (1997) 3039-3046
88. Vidal C. Nicotinic potentiation of glutamatergic synapses in the prefrontal cortex: new insight into analysis of the role of nicotine receptors in cognitive function. Drug Dev Res 31 (1994) 120-126
89. Visser P.J., Krabbendam L., Verhey F.R.J., Hofman P.A.M., Verhoeven W.M.A., Tuinier S., et al. Brain correlates of memory dysfunction in alcoholic Korsakoff's syndrome. J Neurol Neurosurg Psychiatry 67 (1999) 774-778
90. Wenisch S., Fortmann B., Steinmetz T., Leiser R., and Bitsch I. Neuroprotective effects of thiamine-megadoses after long-term ethanol application in the rat brain. A structural investigation of hippocampal CA1 pyramidal and cerebellar Purkinje neurons. J Hirnforsch 37 (1996) 377-387
91. Winer B.J. Statistical principles in experimental design (1962), McGraw-Hill, New York
92. Witt E.D. Neuroanatomical consequences of thiamine deficiency: a comparative analysis. Alcohol Alcohol 20 (1985) 201-221
93. Zhao M.-G., Toyoda H., Lee Y.-S., Wu L.-J., Ko S., Zhang X.-H., et al. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 4 (2005) 859-872