Vitamin B1-deficient mice show impairment of hippocampus-dependent memory formation and loss of hippocampal neurons and dendritic spines: potential microendophenotypes of Wernicke–Korsakoff syndrome

References

• Suzuki U, Shimamura T, Odake S. Über Oryzanin, ein Bestandteil der Reiskleie und seine physiologische Bedeutung [Over Oryzanin, a component of the rice bran and its physiological meaning]. Imp. Univ. Tokyo; 1913.
   Google Scholar
• Singleton CK, Martin PR. Molecular mechanisms of thiamine utilization. Curr. Mol. Med. 2001;1:197–207.10.2174/1566524013363870
   PubMedGoogle Scholar
• Devlin TM. Textbook of biochemistry. Hoboken: Wiley; 2011.
   Google Scholar
• Butterworth RF, Kril JJ, Harper CG. Thiamine-dependent enzyme changes in the brains of alcoholics: relationship to the Wernicke–Korsakoff syndrome. Alcohol. Clin. Exp. Res. 1993;17:1084–1088.10.1111/acer.1993.17.issue-5
   PubMed Web of Science ®Google Scholar
• Halliday G, Cullen K, Harding A. Neuropathological correlates of memory dysfunction in the Wernicke–Korsakoff syndrome. Alcohol Alcohol Suppl. 1994;2:245–251.
   PubMedGoogle Scholar
• Thomson AD. Mechanisms of vitamin deficiency in chronic alcohol misusers and the development of the Wernicke–Korsakoff syndrome. Alcohol Alcohol Suppl. 2000;35:2–7.
   PubMedGoogle Scholar
• Fattal-Valevski A, Azouri-Fattal I, Greenstein YJ, et al. Delayed language development due to infantile thiamine deficiency. Dev. Med. Child Neurol. 2009;51:629–634.10.1111/dmcn.2009.51.issue-8
   PubMed Web of Science ®Google Scholar
• Caine D, Halliday GM, Kril JJ, et al. Operational criteria for the classification of chronic alcoholics: identification of Wernicke’s encephalopathy. J. Neurol. Neurosurg. Psychiatry. 1997;62:51–60.10.1136/jnnp.62.1.51
   PubMed Web of Science ®Google Scholar
• Victor M, Adams RD, Collins GH. The Wernicke–Korsakoff syndrome. A clinical and pathological study of 245 patients, 82 with post-mortem examinations. Contemporary Neurology Series. Oxford: Oxford University Press; 1971.
   Google Scholar
• Victor M, Adams RD, Collins GH. The Wernicke–Korsakoff Syndrome: and related neurologic disorders due to alcoholism and malnutrition. Philadelphia (PA): FA Davis Company; 1989.
   Google Scholar
• Victor M, Herman K, White EE. 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. Q. J. Stud. Alcohol. 1959;20:467–479.
   PubMedGoogle Scholar
• Butters N, Cermak LS. Alcoholic Korsakoff’s syndrome: an information-processing approach to amnesia. San Diego (CA): Academic Press; 2014.
   Google Scholar
• Kopelman MD. The Korsakoff syndrome. Br. J. Psychiatry. 1995;166:154–173.10.1192/bjp.166.2.154
   PubMed Web of Science ®Google Scholar
• Talland G. Deranged memory: a psychonomic study of the amnesic syndrome. San Diego (CA): Academic Press; 1965.
   Google Scholar
• Langlais PJ, Zhang SX, Savage LM. Neuropathology of thiamine deficiency: an update on the comparative analysis of human disorders and experimental models. Metab. Brain Dis. 1996;11:19–37.10.1007/BF02080929
   PubMed Web of Science ®Google Scholar
• Wang X, Wang B, Fan Z, et al. Thiamine deficiency induces endoplasmic reticulum stress in neurons. Neuroscience. 2007;144:1045–1056.10.1016/j.neuroscience.2006.10.008
   PubMed Web of Science ®Google Scholar
• Calingasan NY, Gandy SE, Baker H, et al. Novel neuritic clusters with accumulations of amyloid precursor protein and amyloid precursor-like protein 2 immunoreactivity in brain regions damaged by thiamine deficiency. Am. J. Pathol. 1996;149:1063–1071.
   PubMed Web of Science ®Google Scholar
• Eliash S, Dror V, Cohen S, et al. Neuroprotection by rasagiline in thiamine deficient rats. Brain Res. 2009;1256:138–148.10.1016/j.brainres.2008.11.097
   PubMed Web of Science ®Google Scholar
• Dror V, Eliash S, Rehavi M, et al. Neurodegeneration in thiamine deficient rats-A longitudinal MRI study. Brain Res. 2010;1308:176–184.10.1016/j.brainres.2009.10.032
   PubMed Web of Science ®Google Scholar
• Watanabe I. Pyrithiamine-induced acute thiamine-deficient encephalopathy in the mouse. Exp. Mol. Pathol. 1978;28:381–394.10.1016/0014-4800(78)90012-6
   PubMed Web of Science ®Google Scholar
• Troncoso JC, Johnston MV, Hess KM, et al. Model of Wernicke’s encephalopathy. Arch. Neurol. 1981;38:350–354.10.1001/archneur.1981.00510060052007
   PubMedGoogle Scholar
• Langlais PJ, Savage LM. 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. 1995;68:75–89.10.1016/0166-4328(94)00162-9
   PubMed Web of Science ®Google Scholar
• Abel T, Lattal KM. Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr. Opin. Neurobiol. 2001;11:180–187.10.1016/S0959-4388(00)00194-X
   PubMed Web of Science ®Google Scholar
• McGaugh JL. Memory–a century of consolidation. Science. 2000;287:248–251.10.1126/science.287.5451.248
   PubMed Web of Science ®Google Scholar
• Silva AJ, Kogan JH, Frankland PW, et al CREB and memory. Annu. Rev. Neurosci. 1998;21:127–148.10.1146/annurev.neuro.21.1.127
   PubMed Web of Science ®Google Scholar
• Burgess N, Maguire EA, O’Keefe J. The human hippocampus and spatial and episodic memory. Neuron. 2002;35:625–641.10.1016/S0896-6273(02)00830-9
   PubMed Web of Science ®Google Scholar
• Squire LR, Wixted JT. The cognitive neuroscience of human memory since H.M. Annu. Rev. Neurosci. 2011;34:259–288.10.1146/annurev-neuro-061010-113720
   PubMed Web of Science ®Google Scholar
• Squire LR. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 1992;99:195–231.10.1037/0033-295X.99.2.195
   PubMed Web of Science ®Google Scholar
• Carvalho FM, Pereira SRC, Pires RGW, et al. Thiamine deficiency decreases glutamate uptake in the prefrontal cortex and impairs spatial memory performance in a water maze test. Pharmacol. Biochem. Behav. 2006;83:481–489.10.1016/j.pbb.2006.03.004
   PubMed Web of Science ®Google Scholar
• Nakagawasai O, Tadano T, Niijima F, et al. Immunohistochemical estimation of rat brain somatostatin on avoidance learning impairment induced by thiamine deficiency. Brain Res. Bull. 2000;51:47–55.10.1016/S0361-9230(99)00201-4
   PubMed Web of Science ®Google Scholar
• Langlais PJ, Mandel RJ, Mair RG. Diencephalic lesions, learning impairments, and intact retrograde memory following acute thiamine deficiency in the rat. Behav. Brain Res. 1992;48:177–185.10.1016/S0166-4328(05)80155-X
   PubMed Web of Science ®Google Scholar
• Kida S, Kato T. Microendophenotypes of psychiatric disorders: phenotypes of psychiatric disorders at the level of molecular dynamics, synapses, neurons, and neural circuits. Curr. Mol. Med. 2015;15:111–118.10.2174/1566524015666150303002128
   PubMed Web of Science ®Google Scholar
• Feng G, Mellor RH, Bernstein M, et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron. 2000;28:41–51.10.1016/S0896-6273(00)00084-2
   PubMed Web of Science ®Google Scholar
• Pfefferbaum A, Adalsteinsson E, Bell RL, et al. 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. 2007;32:1159–1177.10.1038/sj.npp.1301107
   PubMed Web of Science ®Google Scholar
• Hasegawa S, Furuichi T, Yoshida T, et al. Transgenic up-regulation of alpha-CaMKII in forebrain leads to increased anxiety-like behaviors and aggression. Mol. Brain. 2009;2:6.10.1186/1756-6606-2-6
   PubMed Web of Science ®Google Scholar
• Inaba H, Tsukagoshi A, Kida S. PARP-1 activity is required for the reconsolidation and extinction of contextual fear memory. Mol. Brain. 2015;8:63.10.1186/s13041-015-0153-7
   PubMed Web of Science ®Google Scholar
• Mamiya N, Fukushima H, Suzuki A, et al. Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory. J. Neurosci. 2009;29:402–413.10.1523/JNEUROSCI.4639-08.2009
   PubMed Web of Science ®Google Scholar
• Suzuki A, Josselyn SA, Frankland PW, et al. Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J. Neurosci. 2004;24:4787–4795.10.1523/JNEUROSCI.5491-03.2004
   PubMed Web of Science ®Google Scholar
• Anagnostaras SG, Josselyn SA, Frankland PW, et al. Computer-assisted behavioral assessment of pavlovian fear conditioning in mice. Learn. Mem. 2000;7:58–72.10.1101/lm.7.1.58
   PubMed Web of Science ®Google Scholar
• Ishikawa R, Kim R, Namba T, et al. Time-dependent enhancement of hippocampus-dependent memory after treatment with memantine: implications for enhanced hippocampal adult neurogenesis. Hippocampus. 2014;24:784–793.10.1002/hipo.22270
   PubMed Web of Science ®Google Scholar
• Kim R, Moki R, Kida S. Molecular mechanisms for the destabilization and restabilization of reactivated spatial memory in the Morris water maze. Mol. Brain. 2011;4:9.10.1186/1756-6606-4-9
   PubMed Web of Science ®Google Scholar
• Suzuki A, Fukushima H, Mukawa T, et al. Upregulation of CREB-mediated transcription enhances both short- and long-term memory. J. Neurosci. 2011;31:8786–8802.10.1523/JNEUROSCI.3257-10.2011
   PubMed Web of Science ®Google Scholar
• Fukushima H, Maeda R, Suzuki R, et al. Upregulation of calcium/calmodulin-dependent protein kinase iv improves memory formation and rescues memory loss with aging. J. Neurosci. 2008;28:9910–9919.10.1523/JNEUROSCI.2625-08.2008
   PubMed Web of Science ®Google Scholar
• Nomoto M, Takeda Y, Uchida S, et al. Dysfunction of the RAR/RXR signaling pathway in the forebrain impairs hippocampal memory and synaptic plasticity. Mol. Brain. 2012;5:8.10.1186/1756-6606-5-8
   PubMed Web of Science ®Google Scholar
• Thor DH, Holloway WR. Social memory of the male laboratory rat. J. Comp. Physiol. Psychol. 1982;96:1000–1006.10.1037/0735-7036.96.6.1000
   Web of Science ®Google Scholar
• Kida S, Josselyn S A, de Ortiz SP, et al. CREB required for the stability of new and reactivated fear memories. Nat. Neurosci. 2002;5:348–355.10.1038/nn819
   PubMed Web of Science ®Google Scholar
• Fukushima H, Zhang Y, Archbold G, et al. Enhancement of fear memory by retrieval through reconsolidation. Elife. 2014;3:e02736.
   Google Scholar
• Paxinos G, Franklin KB. The mouse brain in stereotaxic coordinates. San Diego (CA): Academic Press; 1997.
   Google Scholar
• Fitzgerald PJ, Pinard CR, Camp MC, et al. Durable fear memories require PSD-95. Mol. Psychiatry. 2015;20:901–912.10.1038/mp.2014.161
   PubMed Web of Science ®Google Scholar
• Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods. 1984;11:47–60.10.1016/0165-0270(84)90007-4
   PubMed Web of Science ®Google Scholar
• Stubley-Weatherly L, Harding JW, Wright JW. Effects of discrete kainic acid-induced hippocampal lesions on spatial and contextual learning and memory in rats. Brain Res. 1996;716:29–38.10.1016/0006-8993(95)01589-2
   PubMed Web of Science ®Google Scholar
• Phillips RG, LeDoux JE. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 1992;106:274–285.10.1037/0735-7044.106.2.274
   PubMed Web of Science ®Google Scholar
• Kogan JH, Franklandand PW, Silva AJ. Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus. 2000;10:47–56.10.1002/(ISSN)1098-1063
   PubMed Web of Science ®Google Scholar
• Berman DE, Dudai Y. Memory extinction, learning anew, and learning the new: dissociations in the molecular machinery of learning in cortex. Science. 2001;291:2417–2419.10.1126/science.1058165
   PubMed Web of Science ®Google Scholar
• Josselyn SA, Kida S, Silva AJ. Inducible repression of CREB function disrupts amygdala-dependent memory. Neurobiol. Learn. Mem. 2004;82:159–163.10.1016/j.nlm.2004.05.008
   PubMed Web of Science ®Google Scholar
• Hausser M. Diversity and dynamics of dendritic signaling. Science. 2000;290:739–744.10.1126/science.290.5492.739
   PubMed Web of Science ®Google Scholar
• Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat. Rev. Neurosci. 2008;9:206–221.10.1038/nrn2286
   PubMed Web of Science ®Google Scholar
• Lefebvre JL, Sanes JR, Kay JN. Development of dendritic form and function. Annu. Rev. Cell Dev. Biol. 2015;31:741–777.10.1146/annurev-cellbio-100913-013020
   PubMed Web of Science ®Google Scholar
• Segal M. Dendritic spines, synaptic plasticity and neuronal survival: activity shapes dendritic spines to enhance neuronal viability. Eur. J. Neurosci. 2010;31:2178–2184.10.1111/(ISSN)1460-9568
   PubMed Web of Science ®Google Scholar
• Parkin AJ, Leng NR. Neuropsychology of the amnesic syndrome. Hove: Psychology Press; 1993.
   Google Scholar
• Kopelman MD, Thomson AD, Guerrini I, et al. The Korsakoff syndrome: clinical aspects, psychology and treatment. Alcohol Alcohol. 2009;44:148–154.10.1093/alcalc/agn118
   PubMed Web of Science ®Google Scholar
• Langlais PJ, Zhang SX. Cortical and subcortical white matter damage without Wernicke’s encephalopathy after recovery from thiamine deficiency in the rat. Alcohol Clin. Exp. Res. 1997;21:434–443.
   PubMed Web of Science ®Google Scholar
• Ikarashi Y, Iizuka S, Imamura S, et al. Effects of Yokukansan, a traditional Japanese medicine, on memory disturbance and behavioral and psychological symptoms of dementia in thiamine-deficient rats. Biol. Pharm. Bull. 2009;32:1701–1709.10.1248/bpb.32.1701
   PubMed Web of Science ®Google Scholar
• Greenamyre JT, Young AB, Penney JB. Quantitative autoradiographic distribution of L-[3H]glutamate-binding sites in rat central nervous system. J. Neurosci. 1984;4:2133–2144.
   PubMed Web of Science ®Google Scholar
• Monaghan DT, Cotman CW. Distribution of N-methyl-D-aspartate-sensitive L-[3H]glutamate-binding sites in rat brain. J. Neurosci. 1985;5:2909–2919.
   PubMed Web of Science ®Google Scholar
• Nadler JV, Perry BW, Cotman CW. Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature. 1978;271:676–677.10.1038/271676a0
   PubMed Web of Science ®Google Scholar
• Choi DW. Glutamate neurotoxicity and diseases of the nervous system. Neuron. 1988;1:623–634.10.1016/0896-6273(88)90162-6
   PubMed Web of Science ®Google Scholar
• Tejada J, Garcia-Cairasco N, Roque AC. Combined role of seizure-induced dendritic morphology alterations and spine loss in newborn granule cells with mossy fiber sprouting on the hyperexcitability of a computer model of the dentate gyrus. PLoS Comput. Biol. 2014;10:e1003601.10.1371/journal.pcbi.1003601
   Google Scholar
• Singh SP, He X, McNamara JO, et al. Morphological changes among hippocampal dentate granule cells exposed to early kindling-epileptogenesis. Hippocampus. 2013;23:1309–1320.10.1002/hipo.22169
   PubMed Web of Science ®Google Scholar
• Roy DS, Arons A, Mitchell TI, et al. Memory retrieval by activating engram cells in mouse models of early Alzheimer’s disease. Nature. 2016;531:508–512.10.1038/nature17172
   PubMed Web of Science ®Google Scholar
• Baddeley AD, Warrington EK. Amnesia and the distinction between long- and short-term memory. J. Verbal Learn. Verbal Behav. 1970;9:176–189.10.1016/S0022-5371(70)80048-2
   Google Scholar
• Lishman WA. Organic psychiatry: the psychological consequences of cerebral disorder. Hoboken (NJ): Wiley-Blackwell; 1987.
   Google Scholar
• Zubaran C, Fernandes JG, Rodnight R. Wernicke–Korsakoff syndrome. Postgrad. Med. J. 1997;73:27–31.10.1136/pgmj.73.855.27
   PubMed Web of Science ®Google Scholar
• Day E, Bentham P, Callaghan R, et al. Thiamine for Wernicke–Korsakoff syndrome in people at risk from alcohol abuse. Cochrane Database Syst. Rev. 2004;1; CD004033.
   PubMedGoogle Scholar
• Harris KM. Structure, development, and plasticity of dendritic spines. Curr. Opin. Neurobiol. 1999;9:343–348.10.1016/S0959-4388(99)80050-6
   PubMed Web of Science ®Google Scholar
• Teyler TJ, Discenna P. Long-term potentiation as a candidate mnemonic device. Brain Res. 1984;7:15–28.10.1016/0165-0173(84)90027-4
   Web of Science ®Google Scholar
• Bliss TV, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 1993;361:31–39.10.1038/361031a0
   PubMed Web of Science ®Google Scholar
• Serenó L, Coma M, Rodríguez M, et al. A novel GSK-3beta inhibitor reduces Alzheimer’s pathology and rescues neuronal loss in vivo. Neurobiol. Dis. 2009;35:359–367.10.1016/j.nbd.2009.05.025
   PubMed Web of Science ®Google Scholar
• Tomiyama T, Matsuyama S, Iso H, et al. A mouse model of amyloid beta oligomers: their contribution to synaptic alteration, abnormal tau phosphorylation, glial activation, and neuronal loss in vivo. J. Neurosci. 2010;30:4845–4856.10.1523/JNEUROSCI.5825-09.2010
   PubMed Web of Science ®Google Scholar
• Lanz TA, Carter DB, Merchant KM. Dendritic spine loss in the hippocampus of young PDAPP and Tg2576 mice and its prevention by the ApoE2 genotype. Neurobiol. Dis. 2003;13:246–253.10.1016/S0969-9961(03)00079-2
   PubMed Web of Science ®Google Scholar
• Jacobsen JS, Wu CC, Redwine JM, et al. Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer’s disease. Proc. Natl. Acad. Sci. 2006;103:5161–5166.10.1073/pnas.0600948103
   PubMed Web of Science ®Google Scholar
• Perez-Cruz C, Nolte MW, van Gaalen MM, et al. Reduced spine density in specific regions of CA1 pyramidal neurons in two transgenic mouse models of Alzheimer’s disease. J. Neurosci. 2011;31:3926–3934.10.1523/JNEUROSCI.6142-10.2011
   PubMed Web of Science ®Google Scholar
• Matsuzaki M, Ellis-Davies GC, Nemoto T, et al. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2001;4:1086–1092.10.1038/nn736
   PubMed Web of Science ®Google Scholar
• Nimchinsky EA, Yasuda R, Oertner TG, et al. The number of glutamate receptors opened by synaptic stimulation in single hippocampal spines. J. Neurosci. 2004;24:2054–2064.10.1523/JNEUROSCI.5066-03.2004
   PubMed Web of Science ®Google Scholar
• Ashby MC, Maier SR, Nishimune A, et al. Lateral diffusion drives constitutive exchange of ampa receptors at dendritic spines and is regulated by spine morphology. J. Neurosci. 2006;26:7046–7055.10.1523/JNEUROSCI.1235-06.2006
   PubMed Web of Science ®Google Scholar
• Kasai H, Matsuzaki M, Noguchi J, et al. Structure-stability-function relationships of dendritic spines. Trends Neurosci. 2003;26:360–368.10.1016/S0166-2236(03)00162-0
   PubMed Web of Science ®Google Scholar
• Bourne J, Harris KM. Do thin spines learn to be mushroom spines that remember? Curr. Opin. Neurobiol. 2007;17:381–386.10.1016/j.conb.2007.04.009
   PubMed Web of Science ®Google Scholar
• Zhang Y, Fukushima H, Kida S. Induction and requirement of gene expression in the anterior cingulate cortex and medial prefrontal cortex for the consolidation of inhibitory avoidance memory. Mol. Brain. 2011;4:4.10.1186/1756-6606-4-4
   PubMed Web of Science ®Google Scholar