Translational rodent models of Korsakoff syndrome reveal the critical neuroanatomical substrates of memory dysfunction and recovery

Neuropsychology Review

Volumn 22, Issue 2, 2012, Pages 195-209

  Savage, Lisa M ^a   Hall, Joseph M ^a   Resende, Leticia S ^b  

^a BINGHAMTON UNIVERSITY   (United States)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Cortex; Hippocampus; Korsakoff syndrome; Memory; Rodent; Thalamus; Thiamine deficiency

Indexed keywords

ANIMAL; BRAIN; COGNITIVE DEFECT; DISEASE MODEL; HUMAN; KORSAKOFF PSYCHOSIS; METHODOLOGY; NEUROANATOMY; PATHOLOGY; PATHOPHYSIOLOGY; REVIEW; THIAMINE DEFICIENCY;

ANIMALS; BRAIN; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; HUMANS; KORSAKOFF SYNDROME; NEUROANATOMY; THIAMINE DEFICIENCY;

EID: 84863844213     PISSN: 10407308     EISSN: 15736660     Source Type: Journal    
DOI: 10.1007/s11065-012-9194-1     Document Type: Review

References (111)

1. Aggleton, J. P. (2008). Understanding anterograde amnesia: disconnections and hidden lesions. The Quarterly Journal of Experimental Psychology, 61, 1441-1471.
2. Aggleton, J. P., & Brown, M. W. (1999). Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behavioral Brain Research, 22, 425-489.
3. Aggleton, J. P., Dumont, J. R., & Warburton, E. C. (2011). Unraveling the contributions of the diencephalon to recognition memory: a review. Learning & Memory, 18, 384-400.
4. Anzalone, S., Vetreno, R. P., Ramos, R. L., & Savage, L. M. (2010). Cortical cholinergic abnormalities contribute to the amnesic state induced by pyrithiamine-induced thiamine deficiency in the rat. European Journal of Neuroscience, 32, 847-858.
5. Arendt, T., Bigl, V., Arendt, A., & Tennstedt, A. (1983). Loss of neurons in the nucleus basalis of Meynert in Alzheimer's disease, paralysis agitans and Korskaoff's disease. Acta Neuropathologica, 61, 101-108.
6. Armstrong-James, M., Ross, D. T., Chen, F., & Ebner, F. F. (1988). The effect of thiamine deficiency on the structure and physiology of the rat forebrain. Metabolic Brain Disease, 3, 91-124.
7. Baker, K. G., Harding, A. J., Halliday, G. M., Kril, J. J., & Harper, C. G (1999). Neuronal loss in functional zones of the cerebellum of chronic alcoholics with and without Wernicke's encephalopathy. Neuroscience, 91, 429-438.
8. Béracochéa, D. (2005). Interaction between emotion and memory: importance of mammillary body damage in a mouse model of the alcoholic Korsakoff syndrome. Neural Plasticity, 12, 275-287.
9. Burk, J. A., & Mair, R. G (2001). Effects of intralaminar thalamic lesions on sensory attention and motor intention in the rat: a comparison with lesions involving frontal cortex and hippocampus. Behavioural Brain Research, 123, 49-63.
10. Butterworth, R. F., & Héroux, M. (1989). Effect of pyrithiamine treatment and subsequent thiamine rehabilitation on regional cerebral amino acids and thiamine-dependent enzymes. Journal of Neurochemistry, 52, 1079-1084.
11. Carvalho, F. M., Pereira, S. R. C, Pires, R. G W., Ferraz, V. P., Romano-Silva, M. A., Oliveira-Silva, I. F., & Ribeiro, A. M. (2006). Thiamine deficiency decreases glutamate uptake in the prefrontal cortex and impairs performance in a water maze test. Pharmacology Biochemistry and Behavior, 83, 481-489.
12. Christie, J. E., Kean, D. M., Douglas, R. H, Engleman, H. M., St Clair, D., & Blackburn, I. M. (1988). Magnetic resonance imaging in pre-senile dementia of the Alzheimer-type, multi-infarct dementia and Korsakoff's syndrome. Psychological Medicine, 18, 319-329.
13. Ciccia, R. M., & Langlais, P. J. (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. Alcoholism, Clinical and Experimental Research, 24, 622-634.
14. Cochrane, M., Cochrane, A., Jauhar, P., & Ashton, E. (2005). Acetylcholinesterase inhibitors for the treatment of Wernicke-Korsakoff syndrome- three further cases show response to donepezil. Alcohol and Alcoholism, 40, 151-154.
15. Cotman, C. W., & Berchtold, N. C. (2002). Exercise: a behavioral intervention to enhance brain health and plasticity. Trends in Neuroscience, 25, 295-301.
16. Crews, F. T, Nixon, K, & Wilkie, M. E. (2004). Exercise reverses ethanol inhibition of neural stem cell proliferation. Alcohol, 33, 63-71.
17. Dirksen, C. L., Howard, J. A., Cronin-Golomb, A., & Oscar-Berman, M. (2006). Patterns of prefrontal dysfunction in alcoholics with and without Korsakoff's syndrome, patients with Parkinson's disease, and patients with rupture and repair of the anterior communicating artery. Neuropsychiatric Disease and Treatment, 2, 327-339.
18. Fabel, K, Wolf, S. A., Ehninger, D., Babu, H, Leal-Galicia, P., & Kemperman, G (2009). Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice. Frontiers in Neuroscience, 3, 1-7.
19. Fama, R., Marsh, L., & Sullivan, E. V. (2004). Dissociation of remote and anterograde memory impairment and neural correlates in alcoholic Korsakoff syndrome. Journal of International Neuropsychological Society, 10, 427-441.
20. Gansler, D. A., Harris, G. J., Oscar-Berman, M., Streeter, C., Lewis, R. F., Ahmed, I., & Achong, D. (2000). Hypoperfusion of inferior frontal brain regions in abstinent alcoholics: a pilot SPECT study. Journal of Studies on Alcohol, 61, 32-37.
21. Gibson, G. E., Ksiezak-Reding, H., Sheu, K. F. R., Mykytyn, V., & Blass, J. P. (1984). Correlation of enzymatic metabolic and behavioral deficits in thiamine deficiency and its reversal. Neurochemistry Research, 9, 803-814.
22. Gibson, G. E., Park, L. C. H., Sheu, K. F. R., Blass, J. P., & Calingasan, N. Y. (1999). The α-ketoglutarate dehydrogenase complex in neurodegeneration. Neurochemistry International, 36, 97-112.
23. Griesbach, G. S., Hovda, D. A., Molteni, R., Wu, A., & Gomez-Pinilla, F. (2004). Voluntary exercise following traumatic brain injury: brain-derived neurotrophic factor upregulation and recovery of function. Neuroscience, 125, 129-139.
24. Griesbach, G. S., Hovda, D. A., & Gomez-Pinilla, F. (2009). Exercise-induced improvement in cognitive performance after traumatic brain injury in rats is dependent on BDNF activation. Brain Research, 1228, 105-115.
25. Harding, A. J., Halliday, G., Caine, D., & Kril, J. J. (2000). Degeneration of anterior thalamic nuclei differentiates alcoholics with amnesia. Brain, 123, 141-154.
26. Harper, C. G., & Kril, J. J. (1993). Neuropathological changes in alcoholics. Research Monograph: Alcohol-induced Brain Damage, 22, 39-70.
27. Hazell, A. S., & Butterworth, R. F. (2009). Update of cell damage mechanisms in thiamine deficiency: focus on oxidative stress, excitotoxicity and inflammation. Alcohol and Alcoholism, 44, 141-147.
28. Hazell, A. S., Butterworth, R. F., & Hakim, A. M. (1993). Cerebral vulnerability is associated with selective increase in extracellular glutamate concentration in experimental thiamine deficiency. Journal of Neurochemistry, 61, 1155-1158.
29. He, X., Sullivan, E. V., Stankovic, R. K., Harper, C. G., & Pfefferbaum, A. (2007). Interaction of thiamine deficiency and voluntary alcohol consumption disrupts rat corpus callosum ultrastructure. Neuropsy- chopharmacology, 32, 2207-2216.
30. Héroux, M., & Butterworth, R. F. (1988). Reversible alterations of cerebral α-aminobutyric acid in pyrithiamine-treated rats: implications for the pathogenesis Wernicke's encephalopathy. Journal of Neurochemistry, 51, 1221-1226.
31. Héroux, M., & Butterworth, R. F. (1995). Regional alterations of thiamine phosphate esters and of thiamine diphosphate-dependent enzymes in relation to function in experimental Wernicke's en-cephalopathy. Neurochemical Research, 20, 87-93.
32. Heyn, P., Abreau, B. C., & Ottenbacher, K. J. (2004). The effects of exercise training on elderly persons with cognitive impairment and dementia: a meta-analysis. Archives of Physical Medicine and Rehabilitation, 85, 1694-1704.
33. Hochhalter, A. K., Sweeney, W. A., Savage, L. M., Bakke, B. L., & Overmier, J. B. (2001). Using animal models to address the memory deficits of Wernicke-Korsakoff syndrome. In M. E. Carroll & J. B. Overmier (Eds.), Animal research and human health: Advancing human welfare through behavioral science (pp. 281-292). Washington, DC: American Psychological Association.
34. Homewood, J., Bond, N. W., & Mackenzie, A. (1997). The effects of single and repeated episodes of thiamin deficiency on memory in alcohol-consuming rats. Science, 14, 81-91.
35. Iga, J. I., Araki, M., Ishimoto, Y., & Ohmori, T. (2001). A case of Korsakoff's syndrome improved by high doses of donepezil. Alcohol and Alcoholism, 36, 553-555.
36. Irle, E., & Markowitsch, H. J. (1983). Widespread neuroanatomical damage and learning deficits following chronic alcohol consumption or vitamin-B1 (thiamine) deficiency in rats. Behavioural Brain Research, 9, 277-294.
37. Ke, Z. J., Wang, X., Fan, Z., & Luo, J. (2009). Ethanol promotes thiamine deficiency-induced neuronal death: involvement of double-stranded RNA-activated protein kinase. Alcohol Clinical Experimental Research, 33, 1097-1103.
38. Kopelman, M. D., Thomson, A. D., Guerrini, I., & Marshall, E. J. (2009). The Korskakoff syndrome: clinical aspects, psychology and treatment. Alcohol and Alcoholism, 44, 148-154.
39. Kril, J. J., & Homewood, J. (1993). Neuronal changes in the cerebral cortex of the rat following alcohol treatment and thiamine deficiency. Journal of Neuropathology and Experimental Neuro-pathology, 52, 586-593.
40. Langlais, P. J., & Mair, R. G. (1990). Protective effects of the glutamate antagonist MK-801 on pyrithiamine-induced lesions and amino acid changes in rat brain. Journal of Neuroscience, 10, 1664-1674.
41. Langlais, P. J., & Zhang, S. X. (1993). Extracellular glutamate is increased in thalamus during thiamine deficiency-induced lesions and is blocked by MK-801. Journal of Neurochemistry, 61, 2175-2182.
42. Langlais, P. J., & Savage, L. M. (1995). Thiamine deficiency in rats produces cognitive and memory deficits on spatial tasks that correlate with tissue loss in diencephalon, cortex and white matter. Behavioural Brain Research, 68, 75-89.
43. Langlais, P. J., & Zhang, S. X. (1997). Cortical and subcortical white matter damage without Wernicke's encephalopathy after recovery from thiamine deficiency in the rat. Alcoholism, Clinical and Experimental Research, 21, 434-443.
44. Langlais, P. J., Mair, R. G., Anderson, C. D., & McEntee, W. J. (1988). Long-lasting changes during thiamine deficiency-induced lesions and amino acid changes in the rat brain. Neurochemistry Research, 13, 1199-1206.
45. Langlais, P. J., Mandel, R. J., & Mair, R. G. (1992). Diencephalic lesions, learning impairments, and intact retrograde memory following acute thiamine deficiency in the rat. Behavioural Brain Research, 48, 177-185.
46. Langlais, P. J., Anderson, G., Guo, S. X., & Bondy, S. C. (1996a). Increased cerebral free radical production during thiamine deficiency. Metabolic Brain Disease, 12, 137-143.
47. Langlais, P. J., Zhang, S. X., & Savage, L. M. (1996b). Neuropathol-ogy of thiamine deficiency: an update on the comparative analysis of human disorders and experimental models. Metabolic Brain Disease, 11, 19-35.
48. Lee, J., Duan, W., & Mattson, M. P. (2002). Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. Journal of Neuro-chemistry, 82, 1367-1375.
49. Le Roch, K., Riche, D., & Sara, S. J. (1987). Persistence of habituation deficits after neurological recovery from severe thiamine deprivation. Behavioural Brain Research, 26, 37-46.
50. Leasure, J. L., & Nixon, K. (2010). Exercise neuroprotection in a rat model of binge alcohol consumption. Alcoholism, Clinical and Experimental Research, 34, 404-414.
51. Loukavenko, E. A., Ottley, M. C., Morgan, J. P., Wolff, M., & Dairymple-Alford, J. C. (2007). Towards therapy to relieve memory impairments after anterior thalamic lesions: improved spatial working memory after immediate and delayed postoperative enrichment. European Journal of Neuroscience, 26, 3267-3276.
52. Mair, R. G. (1994). On the role of thalamic pathology in diencephalic amnesia. Reviews in Neuroscience, 5, 105-140.
53. Mair, R. G., Anderson, C. D., Langlais, P. J., & McEntee, W. J. (1985). Thiamine deficiency depletes cortical norepinephrine and impairs learning processes in the rat. Brain Research, 360, 273-284.
54. Mair, R. G., Anderson, C. D., Langlais, P. J., & McEntee, W. J. (1988). Behavioral impairments, brain lesions, and monoaminergic activity in the rat following recovery from a bout of thiamine deficiency. Behavioural Brain Research, 27, 223-239.
55. Mair, R. G., Knoth, R. L., Rabchenuk, S. A., & Langlais, P. J. (1991a). Impairment of olfactory, auditory, and spatial serial reversal learning in rats recovered from pyrithiamine-induced thiamine deficiency. Behavioral Neuroscience, 105, 360-374.
56. Mair, R. G., Otto, T. A., Knoth, R. L., Rabchenuk, S. A., & Langlais, P. J. (1991b). Analysis of aversively conditioned learning and memory in rats recovered from pyrithiamine-induced thiamine deficiency. Behavioral Neuroscience, 105, 351-359.
57. Mair, R. G., Burk, J. A., & Porter, M. C. (1998). Lesions of the frontal cortex, hippocampus, and intralaminar thalamic nuclei have distinct effects on remembering in rats. Behavioral Neuroscience, 112, 772-792.
58. Mitchell, A. S., & Dalrymple-Alford, J. C. (2005). Dissociable memory effects after medial thalamus lesions in the rat. European Journal of Neuroscience, 22, 973-985.
59. Mitchell, A. S., & Dalrymple-Alford, J. C. (2006). Lateral and anterior thalamic lesions impair independent memory systems. Learning & Memory, 13, 388-396.
60. Nakagawasai, O. (2005). Behavioral and neurochemical alterations following thiamine deficiency in rodents: relationship to functions of cholinergic neurons. The Pharmaceutical Society of Japan, 125, 549-554.
61. Nakagawasai, O., Tadano, T., Hozumi, S., Tan-No, K., Niijima, F., & Kisara, K. (2000). Immunohistochemical estimation of brain choline acetyltransferase and somatostatin related to the impairment of avoidance learning induced by thiamine deficiency. Brain Research Bulletin, 52, 189-196.
62. Nakagawasai, O., Tadano, T., Hozumi, S., Taniguchi, R., Yamadera, F., Tan-No, F., Niijima, H., Arai, H., Yasuhara, H., Kinemuchi, H., & Kisara, K. (2001). Inolvement of muscarinic receptor on the impairment of avoidance learning in mice fed a thiamine-deficient diet. Biogenic Amines, 16, 199-210.
63. Nonner, D., Barrett, E. F., & Barrett, J. N. (1996). Neurotrophin effects on survival and expression of cholinergic properties in cultured rat septal neurons under normal and stress conditions. The Journal of Neuroscience, 16, 6665-6675.
64. Oscar-Berman, M., & Evert, D. (1997). Alcoholic Korsakoff's syndrome. In P. D. Nussbaum (Ed.), Handbook of neuropsychology and aging (pp. 201-215). New York: Plenum.
65. Oscar-Berman, M., Kirkley, S. M., Gansler, D. A., & Couture, A. (2004). Comparisons of Korsakoff and non-Korsakoff alcoholics on neuropsychological tests of prefrontal brain functioning. Alcoholism, Clinical and Experimental Research, 28, 667-675.
66. Paller, K. A., Acharya, A., Richardson, A. P., Plaisant, O., Shimamura, A. P., Reed, B. R., & Jagust, W. J. (1997). Functional neuroimaging of cortical dysfunction in alcoholic Korsakoff's syndrome. Journal of Cognitive Neuroscience, 9, 277-293.
67. Pannunzio, P., Hazell, A. S., Pannunzio, M., Rao, K. V., & Butterworth, R. F. (2000). Thiamine deficiency results in metabolic acidosis and energy failure in cerebellar granule cells: an in vitro model for the study of cell death mechanisms in Wernicke's encephalopathy. Journal of Neuroscience Research, 62, 286-292.
68. Pfefferbaum, A., Adalsteinsson, E., Bell, R. L., & Sullivan, E. V. (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. Neuropsy-chopharmacology, 32, 1159-1177.
69. Philips, S. C., Harper, C., & Kril, J. (1987). A quantitative histological study of the cerebellar vermis in alcoholic patients. Brain, 110, 301-314.
70. Pires, R. G. W., Pereira, S. R. C., Pittella, J. E. H., Franco, G. C., Ferreira, C. L. M., Fernandes, P. A., & Ribeiro, A. M. (2001). The contribution of mild thiamine deficiency and ethanol consumption to central cholinergic dysfunction and rats' open-field performance impairment. Pharmacology Biochemistry and Behavior, 70, 227-235.
71. Pires, R. G. W., Pereira, S. R. C., Oliveira-Silva, I., Franco, G. C., & Ribeiro, A. M. (2005). Cholinergic parameters and the retrieval of learned and re-learned spatial information: a study using a model of Wernicke-Korsakoff Syndrome. Behavioural Brain Research, 162, 11-21.
72. Pitkin, S. R., & Savage, L. M. (2001). Aging potentiates the acute and chronic neurological symptoms of pyrithiamine-induced thiamine deficiency in the rodent. Behavioural Brain Research, 119, 167-177.
73. Pitkin, S. R., & Savage, L. M. (2004). Age-related vulnerability to diencephalic amnesia produced by thiamine deficiency: the role of time of insult. Behavioural Brain Research, 148, 93-105.
74. Reed, L. J., Lasserson, D., Marsden, P., Stanhope, N., Stevens, T., Bello, F., Kingsley, D., Colchester, A., & Kopelman, M. D. (2003). FDG-PET findings in the Wernicke-Korsakoff syndrome. Cortex, 39, 1027-1045.
75. Robinson, J. K., & Mair, R. G. (1992). MK-801 prevents brain lesions and delayed-nonmatching-to-sample deficits produced by pyrithiamine-induced encephalopathy in rats. Behavioral Neuroscience, 106, 623-633.
76. Roland, J. J., & Savage, L. M. (2007). Blunted hippocampal, but not striatal, acetylcholine efflux parallels learning impairment in diencephalic-lesioned rats. Neurobiology of Learning and Memory, 87, 123-132.
77. Roland, J. J., & Savage, L. M. (2009). The role of cholinergic and GABAergic medial septal/diagonal band cell populations in the emergence of diencephalic amnesia. Neuroscience, 160, 32-41.
78. Roland, J. J., Mark, K., Vetreno, R. P., & Savage, L. M. (2008). Increasing hippocampal acetylcholine levels enhance behavioral performance in an animal model of diencephalic amnesia. Brain Research, 1234, 116-127.
79. Roland, J. J., Levinson, M., Vetreno, R. P., & Savage, L. M. (2010). Differential effects of systemic and intraseptal administration of the acetylcholinesterase inhibitor tacrine on the recovery of spatial behavior in an animal model of diencephalic amnesia. European Journal of Pharmacology, 629, 31-39.
80. Sairanen, M., Lucas, G., Emfors, P., Castren, M., & Castren, E. (2005). Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. The Journal of Neuroscience, 25, 1089-1094.
81. Savage, L. M. (2012). Sustaining high acetylcholine levels in the frontal cortex, but not retrosplenial cortex, recovers spatial memory performance in a rodent model of diencephalic amnesia. Behavioral Neuroscience, 126, 226-236.
82. Savage, L. M., & Guarino, S. (2010). Memory for reward location is enhanced even though acetylcholine efflux within the amygdala is impaired in rats with damage to the diencephalon produced by thiamine deficiency. Neurobiology of Learning and Memory, 94, 554-560.
83. Savage, L. M., & Ramos, R. L. (2009). Reward expectation alters learning and memory: the impact of the amygdala on appetitive-driven behaviors. Behavioural Brain Research, 198, 1-12.
84. Savage, L. M., Castillo, R., & Langlais, P. J. (1998). Effects of lesions of thalamic intralaminar and midline nuclei and internal medual-lary lamina on spatial memory and object discrimination. Behavioral Neuroscience, 112, 1339-1352.
85. Savage, L. M., Pitkin, S. R., & Knitowski, K. M. (1999). 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. Behavioural Brain Research, 104, 13-26.
86. Savage, L. M., Chang, Q., & Gold, P. E. (2003). Diencephalic damage decreases hippocampal acetylcholine release during spontaneous alternation testing. Learning & Memory, 10, 242-246.
87. Savage, L. M., Roland, J. J., & Klintsova, A. (2007). Selective septohippocampal-but not forebrain amygdalar-cholinergic dysfunction in diencephalic amnesa. Brain Research, 1139, 210-219.
88. Savage, L. M., Hall, J. M., & Vetreno, R. P. (2011). Anterior thalamic lesions alter both hippocampal-dependent behavior and hippocampal acetylcholine release in the rat. Learning & Memory, 18, 751-758.
89. Savage, L. M., Sweet, A. J., Castillo, R., & Langlais, P. J. (1997). The effects of lesions to the thalamic lateral internal medullary lamina nuclei and posterior nuclei on learning, memory, and habituation in the rat. Behavioural Brain Research, 82, 133-147.
90. Squire, L. R. (1980). Specifying the defect in human amnesia: storage, retrieval and semantics. Neuropsychologia, 18, 369-372.
91. Squire, L. R. (1982). The neuropsychology of human memory. Annual Review of Neuroscience, 5, 241-273.
92. Squire, L. R., Amaral, D. G., & Press, G. A. (1990). Magnetic resonance imaging of the hippocampal formation and mammillary nuclei distinguish medial temporal lobe and diencephalic amnesia. Journal of Neuroscience, 10, 3106-3117.
93. Sullivan, E. V., & Marsh, L. (2003). Hippocampal volume deficits in alcoholic Korsakoff's syndrome. Neurology, 61, 1716-1719.
94. Sullivan, E. V., & Pfefferbaum, A. (2009). Neuroimaging of the Wernicke-Korsakoff syndrome. Alcohol and Alcoholism, 44, 155-165.
95. Takahashi, H., Nakazawa, S., Yoshino, Y., & Shimura, T. (1988). Metabolic studies of the edematous cerebral cortex of the pyrithiamine-treated thiamine deficient rat. Brain Research, 441, 202-208.
96. Todd, K. G., & Butterworth, R. F. (1999). Mechanisms of selective neuronal cell death due to thiamine deficiency. Annals of the New York Academy of Sciences, 893, 404-411.
97. Troncoso, J. C., Johnston, M. V., Hess, K. M., Griffin, J. W., & Price, D. L. (1981). Model of Wernicke's encephalopathy. Archives of Neurology, 38, 350-354.
98. Vann, S. D. (2010). Re-evaluating the role of the mammillary bodies in memory. Neuropsychologia, 48, 2316-2327.
99. Van Tilborg, I. A., Kessels, R. P., Kruijt, P., Wester, A. J., & Hulstijn, W. (2011). Spatial and nonspatial implicit motor learning in Korsakoff's amnesia: evidence for selective deficits. Experimental Brain Research, 214, 427-435.
100. Vetreno, R. P., Anzalone, S. J., & Savage, L. M. (2008). Impaired, spared, and enhanced ACh efflux across the hippocampus and striatum in diencephalic amnesia is dependent on task demands. Neurobiology of Learning and Memory, 90, 237-244.
101. Vetreno, R. P., Hall, J. M., & Savage, L. M. (2011a). Alcohol-related amnesia and dementia: animal models have revealed the contributions of different etiological factors on neuropathology, neuro-chemical dysfunction and cognitive impairment. Neurobiology of Learning and Memory, 96, 596-608.
102. Vetreno, R. P., Klintsova, A., & Savage, L. M. (2011b). Stage-dependent alterations of progenitor cell proliferation and neuro-genesis in an animal model of Wernicke-Korsakoff syndrome. Brain Research, 1391, 132-146.
103. Vetreno, R. P., Ramos, R. L., Anzalone, S., & Savage, L. M. (2012). Brain and behavioral pathology in an animal model of Wernicke's encephalopathy and Wernicke-Korsakoff syndrome. Brain Research, 1436, 178-192.
104. Vigil, A. F. B., Oliveira-silva, I. F., Ferreira, L. F., Pereira, S. R. C., & Ribeiro, A. M. (2010). Spatial memory deficits and thalamic serotonergic metabolite change in thiamine deficient rats. Behavioural Brain Research, 210, 140-142.
105. Volterra, A., Trotti, D., Tromba, C., Floridi, S., & Racagni, G. (1994). Glutamate uptake inhibition by oxygen free radicals in rat cortical astrocytes. The Journal of Neuroscience, 14, 2924-2932.
106. Watanabe, I. (1978). Pyrithiamine-induced acute thiamine-deficient encephalopathy in the mouse. Experimental and Molecular Pathology, 28, 381-394.
107. Witt, E. D. (1985). Neuroanatomical consequences of thiamine deficiency: a comparative analysis. Alcohol and Alcoholism, 20, 201-221.
108. Wolff, M., Loukavenko, E. A., Will, B. E., & Dalrymple-Alford, J. C. (2008). The extended hippocampal-diencephalic memory system: enriched housing promotes recovery of the flexible use of spatial representations after anterior thalamic lesions. Hippocampus, 18, 996-1007.
109. Zhang, S. X., Weilersbacher, G. S., Henderson, S. W., Corso, T., Olney, J. W., & Langlais, P. J. (1995). Excitotoxic cytopathology, progression, and reversibility of thiamine deficiency-induced di-encephalic lesions. Journal of Neuropathology and Experimental Neurology, 54, 255-267.
110. Zhao, N., Zhong, C., Wang, Y., Zhao, Y., Gong, N., Zhou, G., Xu, T., & Hong, Z. (2008). Impaired hippocampal neurogenesis is involved in cognitive dysfunction induced by thiamine deficiency at early pre-pathological lesion stage. Neurobiology of Disease, 29, 176-185.
111. Zimitat, C., Kril, J., Harper, C., & Nixon, P. (1990). Progression of neurological disease in thiamine-deficient rats is enhanced by ethanol. Alcohol, 7, 493-501.