Maternal thiamine restriction during lactation induces cognitive impairments and changes in glutamate and GABA concentrations in brain of rat offspring

Behavioural Brain Research

Volumn 211, Issue 1, 2010, Pages 33-40

  de Freitas Silva, Danielle Marra ^a   Resende, Letícia de Souza ^a   Pereira, Silvia Rejane Castanheira ^a   Franco, Glaura Conceição ^a   Ribeiro, Angela Maria ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Brain regions; GABA; Glutamate; Learning and memory; Maternal thiamine restriction; Wistar rats

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; THIAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; BRAIN REGION; COGNITIVE DEFECT; DIET RESTRICTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; LACTATION; LEARNING; MALE; NEUROMODULATION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROGENY; RAT; SPATIAL MEMORY; TASK PERFORMANCE; THALAMUS; THIAMINE RESTRICTION; WEIGHT GAIN; WORKING MEMORY;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, SUCKLING; BRAIN; COGNITION DISORDERS; ENERGY METABOLISM; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HIPPOCAMPUS; LACTATION; MALE; MAZE LEARNING; MILK; NUTRITIVE VALUE; PREFRONTAL CORTEX; RATS; REACTION TIME; THALAMUS; THIAMINE; THIAMINE DEFICIENCY; TIME FACTORS;

EID: 77952323312     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.03.002     Document Type: Article

References (78)

1. Bâ A., N'Douba V., D'Almeida M.A., Seri B.V. Effects of the maternal thiamine deficiencies on the pyramidal and granule cells of the hippocampus of rat pups. Acta Neurobiol Exp 2005, 65(4):387-398.
2. Bâ A., Seri B.V., Aka K.J., Glin L., Tako A. Comparative effects of developmental thiamine deficiencies and ethanol exposure on the morphometry of the CA3 pyramidal cells. Neurotoxicol Teratol 1999, 21(5):579-586.
3. Baydas G., Koz S.T., Tuzcu M., Nedzvetsky V.S., Etem E. Effects of maternal hyperhomocysteinemia induced by high methionine diet on the learning and memory performance in offspring. Int J Dev Neurosci 2007, 25(3):133-139.
4. Bellingham-Young D.A., Adamson-Macedo E.N. Foetal origins theory: links with adult depression and general self-efficacy. Neuro Endocrinol Lett 2003, 24(6):412-416.
5. Berg J.M., Tymoczko J.L., Stryer L. Biochemistry 2004, W.H. Freeman and Company, New York. fifth ed.
6. Bredy T.W., Grant R.J., Champagne D.L., Meaney M.J. Maternal care influences neuronal survival in the hippocampus of the rat. Eur J Neurosci 2003, 18(10):2903-2909.
7. Bussey T.J., Muir J.L., Aggleton J.P. Functionally dissociating aspects of event memory: the effects of combined perirhinal and postrhinal cortex lesions on object and place memory in the rat. J Neurosci 1999, 19(1):495-502.
8. Butterworth R.F., Hamel E., Landreville F., Barbeau A. Amino acid changes in thiamine-deficient encephalopathy: some implications for the pathogenesis of Friedreich's ataxia. Can J Neurol Sci 1979, 6(2):217-222.
9. Butterworth R.F. Effects of thiamine deficiency on brain metabolism: implications for the pathogenesis of the Wernicke-Korsakoff syndrome. Alcohol Alcohol 1989, 24(4):271-279.
10. Carvalho F.M., Pereira S.R., Pires R.G., Ferraz V.P., Romano-Silva M.A., Oliveira-Silva I.F., Ribeiro A.M. Thiamine deficiency decreases glutamate uptake in the prefrontal cortex and impairs spatial memory performance in a water maze test. Pharmacol Biochem Behav 2006, 83(4):481-489.
11. Chapillon P., Patin V., Roy V., Vincent A., Caston J. Effects of pre- and Postnatal stimulation on developmental, emotional, and cognitive aspects in rodents: a review. Dev Psychobiol 2002, 41:373-387.
12. Cooper R.L., Goldman J.M., Vanderbergh J.G. Monitoring of the estrus cycle in the laboratory rodent by vaginal lavage. Methods in Toxicology: Female Reproductive Toxicology 1993, vol. 3:45-56. Academic Press, San Diego.
13. Davison A.N., Dobbing J. Myelination as a vulnerable period in brain development. Br Med Bull 1966, 22(1):40-44.
14. Del Arco A., Mora F. Prefrontal cortex-nucleus accumbens interaction: in vivo modulation by dopamine and glutamate in the prefrontal cortex. Pharmacol Biochem Behav 2008, 90(2):226-235.
15. Foster A.C., Kemp J.A. Glutamate- and GABA-based CNS therapeutics. Curr Opin Pharmacol 2006, 6(1):7-17.
16. Fournier H., Butterworth R.F. Effects of thiamine deficiency on thiamine-dependent enzymes in regions of the brain of pregnant rats and their offspring. Metab Brain Dis 1990, 5(2):77-84.
17. Freitas-Silva D.M., Ferraz V.P., Ribeiro A.M. Improved high-performance liquid chromatographic method for GABA and Glutamate determination in regions of the rodent brain. J Neurosci Methods 2009, 177(2):289-293.
18. Ge S., Yang C., Hsu K., Ming G., Song H. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 2007, 54(4):559-566.
19. Getova D.P., Dimitrova D.D. Effects of GABAB receptor antagonists CGP63360, CGP76290A and CGP76291A on learning and memory processes in rodents. CEJ Med 2007, 2(3):280-293.
20. Godfrey K.M., Barker D.J. Fetal programming and adult health. Public Health Nutr 2001, 4(2B):611-624.
21. Gorji H.M., Rashid-Pour A., Fathollahi Y. Effects of morphine dependence on the performance of rats in reference and working versions of the water maze. Physiol Behav 2008, 93(3):622-627.
22. Greenwood CE, Craig REA. Dietary influences on brain function: implications during periods of neuronal maturation. In: Basic and Clinical Aspects of Nutrition and Brain Development. Curr Top Nutr Dis, vol. 16, Alan R. Liss Inc., New York 1987;159-216.
23. Greenwood J., Pratt O.E., Thomson A.D. Thiamine, malnutrition and alcohol related damage to the central nervous system. Alcohol Nutrition and the Nervous System. Progress in Alcohol Research 1985, vol. 1:287-310. VNU Science Press, Utrecht.
24. Gurden H., Tassin J.P., Jay T.M. Integrity of the mesocortical dopaminergic system is necessary for complete expression of in vivo hippocampal-prefrontal cortex long-term potentiation. Neuroscience 1999, 94(4):1019-1027.
25. Kutlán D., Molnár-Perl I. New aspects of the simultaneous analysis of amino acids and amines as their o-phthaldialdehyde derivatives by high-performance liquid chromatography. Analysis of wine, beer and vinegar. J Chromatogr A 2003, 987(1-2):311-322.
26. Langlais P.J., Mandel R.J., Mair R.G. Diencephalic lesions, learning impairments and intact retrograde memory following acute thiamine deficiency in the rat. Behav Brain Res 1992, 48(2):177-185.
27. Langlais P.J., 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 1995, 68(1):75-89.
28. Lesage J., Del-Favero F., Leonhardt M., Louvart H., Maccari S., Vieau D., Darnaudery M. Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. J Endocrinol 2004, 181(2):291-296.
29. Lesage J., Hahn D., Leéonhardt M., Blondeau B., Bréant B., Dupouy J.P. Maternal undernutrition during late gestation-induced intrauterine growth restriction in the rat is associated with impaired placental GLUT3 expression, but does not correlate with endogenous corticosterone levels. J Endocrinol 2002, 174(1):37-43.
30. Liu D., Diorio J., Day J.C., Francis D.D., Meaney M.J. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci 2000, 3(8):799-806.
31. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277(5332):1659-1662.
32. Losa R., Sierra M.I., Fernández A., Blanco D., Buesa J.M. Determination of thiamine and its phosphorylated forms in human plasma, erythrocytes and urine by HPLC and fluorescence detection: a preliminary study on cancer patients. J Pharm Biomed Anal 2005, 37:1025-1029.
33. Lucas A. Programming by early nutrition in man. In: The Childhood Environment and Adult Disease. CIBA Foundation Symposium 1991, Wiley, Chichester, UK.
34. Lucas A. Programming by Early nutrition: an experimental approach. in: the effects of childhood diet on adult health and disease. J Nutr 1998, 128:401S-406S.
35. Mair R.G., Otto T.A., Knoth R.L., Rabchenuk S.A., Langlais P.J. Analysis of aversively conditioned learning and memory in rats recovered from pyrithiamine-induced thiamine deficiency. Behav Neurosci 1991, 105(3):351-359.
36. Maruki K., Izaki Y., Hori K., Nomura M., Yamauchi T. Effects of rat ventral and dorsal hippocampus temporal inactivation on delayed alternation task. Brain Res 2001, 895(1-2):273-276.
37. Matsumoto M., Togashi H., Konno K., Koseki H., Hirata R., Izumi T., Yamaguchi T., Yoshioda M. Early postnatal stress alters the extinction of context-dependent conditioned fear in adult rats. Pharmacol Biochem Behav 2008, 89(3):247-252.
38. McKay B.E., Lado W.E., Martin L.J., Galic M.A., Fournier N.M. Learning and memory in agmatine-treated rats. Pharmacol Biochem Behav 2002, 72(3):551-557.
39. McNally G.P., Augustyn K.A., Richardson R. GABA (A) receptors determine the temporal dynamics of memory retention. Learn Mem 2008, 15(3):106-111.
40. Mengerink Y., Kutlán D., Tóth F., Csámpai A., Molnár-Perl I. Advances in the evaluation of the stability and characteristics of the amino acid and amine derivates obtained with the o-phthaldialdehyde/3-mercaptopropionic acid and o-phthaldialdehyde/N-acetyl-L-cysteine reagents high-performance liquid chromatography-mass spectrometry study. J Chromatogr A 2002, 949(1-2):99-124.
41. Miller M.W. Generation of neurons in the rat dentate gyrus and hippocampus: effects of prenatal and postnatal treatment with ethanol. Alcohol Clin Exp Res 1995, 19(6):1500-1509.
42. Mora F., Segovia G., Del Arco A. Glutamate-dopamine-GABA interactions in the aging basal ganglia. Brain Res Rev 2008, 58(2):340-353.
43. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984, 11(1):47-60.
44. Mumby D.G., Cameli L., Glenn M.J. Impaired allocentric spatial working memory and intact retrograde memory after thalamic damage caused by thiamine deficiency in rats. Behav Neurosci 1999, 113(1):42-50.
45. Myhrer T. Neurotransmitter systems involved in learning and memory in the rat: a meta-analysis based on studies of four behavioral tasks. Brian Res Rev 2003, 41(2-3):268-287.
46. Nagahara A.H., McGaugh J.L. Muscimol infused into the medial septal area impairs long-term memory but not short-term memory in inhibitory avoidance, water maze place learning and rewarded alternation tasks. Brain Res 1992, 591(1):54-61.
47. Nakagawasai O., Murata A., Arai Y., Ohba A., Wakui K., Mitazaki S., Niijima F., Tan-No K., Tadano T. Enhanced head-twitch response to 5-HT related agonists in thiamine deficient mice. J Neural Transm 2007, 114(8):1003-1010.
48. Nakagawasai O., Yamadera F., Iwasaki K., Asao T., Tan-No K., Niijima F., Arai H., Tadano T. Preventive effect of kami-untan-to on performance in the forced swimming test in thiamine-deficient mice: relationship to functions of catecholaminergic neurons. Behav Brain Res 2007, 177(2):315-321.
49. 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. Washington (DC): U.S. Department of Health and Human Services 1985.
50. Nilsson C., Jennische E., Ho H.P., Eriksson E., Björntorp P., Holmäng A. Increased insulin sensitivity and decreased body weight in female rats after postnatal corticosterone exposure. Eur J Endocrinol 2002, 146(6):847-854.
51. Nunez J.F., Ferre P., Garcia E., Escorihuela R.M., Fernandez-Teruel A., Tobena A. Postnatal handling reduces emotionality ratings and accelerates two-way active avoidance in female rats. Physiol Behav 1995, 57:831-835.
52. Nutt D.J., Malizia A.L. New insights into the role of the GABA (A)-benzodiazepine receptor in psychiatric disorder. Br J Psychiatry 2001, 179:390-396.
53. Oliveira F.A., Galan D.T., Ribeiro A.M., Santos Cruz J. Thiamine deficiency during pregnancy leads to cerebellar neuronal death in rat offspring: role of voltage-dependent K+ channels. Brain Res 2007, 1134(1):79-86.
54. Oliveira-Silva I.F., Pinto L., Pereira S.R.C., Ferraz V.P., Barbosa A.J.A., Coelho V.A.A., Gualberto F.F.A.S., Souza V.F., Faleiro R.R.M., Franco G.C., Ribeiro A.M. Age-related deficit in behavioural extinction is counteracted by long-term ethanol consumption: Correlation between 5-HIAA/5HT ratio in dorsal raphe nucleus and cognitive parameters. Behav Brain Res 2007, 180:226-234.
55. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2004, Academy Press, London. fifth ed.
56. Pires R.G., Pereira S.R., Oliveira-Silva I.F., Franco G.C., 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 2005, 162(1):11-21.
57. Pires R.G., Pereira S.R., Pittella J.E., Franco G.C., Ferreira C.L., Fernendez P.A., Ribeiro A.M. The contribution of mild thiamine deficiency and ethanol consumption to central cholinergic parameter dysfunction and rat's open-field performance impairment. Pharmacol Biochem Behav 2001, 70(2-3):227-235.
58. Pitkin S.R., Savage L.M. Age-related vulnerability to diencephalic amnesia produced by thiamine deficiency: the role of time of insult. Behav Brain Res 2004, 148(1-2):93-105.
59. Ramakrishnan U., Manjrekar R., Rivera J., Gonzales-Cossio T., Martorell R. Micronutrients and pregnancy outcome: a review of the literature. Nutr Res 1999, 19(1):103-159.
60. Rinaldi A., Mandillo S., Oliverio A., Mele A. D1 and D2 receptor antagonist injections in the prefrontal córtex selectively impair spatial learning in mice. Neuropsychopharmacology 2007, 32(2):309-319.
61. Savage L.M., Pitkin S.R., 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 1999, 104(1-2):13-26.
62. Schneider M., Koch M. Behavioral and morphological alterations following neonatal excitotoxic lesions of the medial prefrontal cortex in rats. Exp Neurol 2005, 195(1):185-198.
63. Schulz D., Topic B., De Souza Silva M.A., Huston J.P. Extinction-induced immobility in the water maze and its neurochemical concomitants in aged and adult rats: a possible model for depression?. Neurobiol Learn Mem 2004, 82(2):128-141.
64. Shahidi S., Komaki A., Mahmoodi M., Lashgari R. The role of GABAergic transmission in the dentate gyrus on acquisition, consolidation and retrieval of an inhibitory avoidance learning and memory task in the rat. Brain Res 2008, 1204:87-93.
65. Spanis C.W., Bianchin M.M., Izquierdo I., McGaugh J.L. Excitotoxic basolateral amygdala lesions potentiate the memory impairment effect of muscimol injected into the medial septal area. Brain Res 1999, 816(2):329-336.
66. Todd K., Butterworth R.F. Mechanisms of selective neuronal cell death due to thiamine deficiency. Ann NY Acad Sci 1999, 893:404-411.
67. Toso L., Johnson A., Bissell S., Roberson R., Abebe D., Spong C.Y. Understanding the mechanism of learning enhancement: NMDA and GABA receptor expression. Am J Obstet Gynecol 2007, 197(3). 267e1-4.
68. Trostler N., Guggenheim K., Havivi E., Sklan D. Effect of thiamine deficiency in pregnancy and lactating rats on the brain of their offspring. Nutr Metab 1977, 21(5):294-304.
69. Trostler N., Sklan D. Milk composition and thiamine transfer in thiamine deficient rats. Am J Clin Nutr 1977, 30(5):681-685.
70. Valls F., Checa M.A., Fernández-Muinõ A., Sancho T. Determination of thiamin in cooked sausages. J Agric Food Chem 1999, 47(1):170-173.
71. Van de Weerd H.A., Van Loo P.L., Van Zutphen L.F., Koolhaas J.M., Baumans V. Nesting material as environmental enrichment has no adverse effects on behavior and physiology of laboratory mice. Physiol Behav 1997, 62:1019-1028.
72. Vetreno R.P., Anzalone S.J., Savage L.M. Impaired, spared and enhanced ACh efflux across the hippocampus and striatum in diencephalic amnesia is dependent on task demands. Neurobiol Learn Mem 2008, 90(1):237-244.
73. Weinberg J., Sliwowska J.H., Lan N., Hellemans K.G. Prenatal alcohol exposure: foetal programming the hypothalamic-pituitary-adrenal axis and sex differences in outcome. J Neuroendocrinol 2008, 20(4):470-488.
74. Winer B.J. Statistical principles in experimental design 1962, McGraw-Hill, New York.
75. Witt E.D. Neuroanatomical consequences of thiamine deficiency: a comparative analysis. Alcohol Alcohol 1985, 20(2):201-221.
76. Yamauchi C., Fujita S., Obara T., Ueda T. Effects of room temperature on reproduction, body and organ weights, food and water intake, and hematology in rats. Lab Anim Sci 1981, 31(3):251-258.
77. Zarrindast M.R., Shamsi T., Azarmina P., Rostami P., Shafaghi B. GABAergic system and imipramine-induced impairment of memory retention in rats. Eur Neuropsychopharm 2004, 14(1):59-64.
78. Zhang X., Sliwowska J.H., Weinberg J. Prenatal alcohol exposure and fetal programming: effects on neuroendocrine and immune function. Exp Biol Med 2005, 230(60):376-438.