Prenatal choline supplementation attenuates neuropathological response to status epilepticus in the adult rat hippocampus

Neurobiology of Disease

Volumn 30, Issue 2, 2008, Pages 255-269

  Wong Goodrich, Sarah J E ^a   Mellott, Tiffany J ^b   Glenn, Melissa J ^a   Blusztajn, Jan K ^b   Williams, Christina L ^a  

^a DUKE UNIVERSITY   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bromodeoxyuridine; Choline; Glial fibrillary acidic protein; Glutamic acid decarboxylase; Growth factor; Hippocampus; Kainic acid; Neuroprotection; Seizures

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CHOLINE; DIAZEPAM; GENE PRODUCT; GFAP PROTEIN; GLUTAMATE DECARBOXYLASE 65; GROWTH FACTOR; KAINIC ACID; MESSENGER RNA; NERVE GROWTH FACTOR RECEPTOR; SOMATOMEDIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL PROLIFERATION; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; DIET SUPPLEMENTATION; EPILEPTIC STATE; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; MALE; NERVE DEGENERATION; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PRENATAL CARE; PRIORITY JOURNAL; PROGENY; RAT; RODENT;

ANIMALS; CHOLINE; FEMALE; HIPPOCAMPUS; MALE; PREGNANCY; PRENATAL CARE; PRENATAL NUTRITION PHYSIOLOGY; RATS; RATS, SPRAGUE-DAWLEY; STATUS EPILEPTICUS;

EID: 42649113725     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2008.01.008     Document Type: Article

References (116)

1. Anderson M.F., Aberg M.A., Nilsson M., and Eriksson P.S. Insulin-like growth factor-I and neurogenesis in the adult mammalian brain. Brain Res., Dev. Brain Res. 134 (2002) 115-122
2. Ben-Ari Y., and Represa A. Brief seizure episodes induce long-term potentiation and mossy fiber sprouting in the hippocampus. Trends Neurosci. 13 (1990) 312-318
3. Bengzon J., Kokaia Z., Elmer E., Nanobashvili A., Kokaia M., and Lindvall O. Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 10432-10437
4. Blusztajn J.K. Choline, a vital amine. Science 281 (1998) 794-795
5. Blusztajn J.K., Cermak J.M., Holler T., and Jackson D.A. Imprinting of hippocampal metabolism of choline by its availability during gestation: implications for cholinergic neurotransmission. J. Physiol. Paris 92 (1998) 199-203
6. Borges K., McDermott D., Irier H., Smith Y., and Dingledine R. Degeneration and proliferation of astrocytes in the mouse dentate gyrus after pilocarpine-induced status epilepticus. Exp. Neurol. 201 (2006) 416-427
7. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., Winkler J., Aigner L., and Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 467 (2003) 1-10
8. Cameron H.A., Hazel T.G., and McKay R.D. Regulation of neurogenesis by growth factors and neurotransmitters. J. Neurobiol. 36 (1998) 287-306
9. Cavazos J.E., Das I., and Sutula T.P. Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J. Neurosci. 14 (1994) 3106-3121
10. Chomczynski P., and Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162 (1987) 156-159
11. Cornish S.M., and Wheal H.V. Long-term loss of paired pulse inhibition in the kainic acid-lesioned hippocampus of the rat. Neuroscience 28 (1989) 563-571
12. Cotman C.W., and Berchtold N.C. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 25 (2002) 295-301
13. Couillard-Despres S., Winner B., Schaubeck S., Aigner R., Vroemen M., Weidner N., Bogdahn U., Winkler J., Kuhn H.G., and Aigner L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 21 (2005) 1-14
14. da Costa K.A., Kozreva O.G., Song J., Galanko J.A., Fischer L.M., and Zeisel S.H. Common genetic polymorphisms affect the human requirement for the nutrient choline. FASEB J. 20 (2006) 1336-1344
15. Davenport C.J., Brown W.J., and Babb T.L. GABAergic neurons are spared after intrahippocampal kainate in the rat. Epilepsy Res. 5 (1990) 28-42
16. Erlander M.G., and Tobin A.J. The structural and functional heterogeneity of glutamic acid decarboxylase: a review. Neurochem. Res. 16 (1991) 215-226
17. Esclapez M., and Houser C.R. Up-regulation of GAD65 and GAD67 in remaining hippocampal GABA neurons in a model of temporal lobe epilepsy. J. Comp. Neurol. 412 (1999) 488-505
18. Esclapez M., Tillakaratne N.J., Kaufman D.L., Tobin A.J., and Houser C.R. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J. Neurosci. 14 (1994) 1834-1855
19. Fujikawa D.G., Shinmei S.S., and Cai B. Kainic acid-induced seizures produce necrotic, not apoptotic, neurons with internucleosomal DNA cleavage: implications for programmed cell death mechanisms. Neuroscience. 98 (2000) 41-53
20. Gall C.M., and Isackson P.J. Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. Science 245 (1989) 758-761
21. Gall C., Murray K., and Isackson P.J. Kainic acid-induced seizures stimulate increased expression of nerve growth factor mRNA in rat hippocampus. Brain Res., Mol. Brain Res. 9 (1991) 113-123
22. Garner S.C., Mar M.H., and Zeisel S.H. Choline distribution and metabolism in pregnant rats and fetuses are influenced by the choline content of the maternal diet. J. Nutr. 125 (1995) 2851-2858
23. Glenn M.J., Gibson E.M., Kirby E.D., Mellott T.J., Blusztajn J.K., and Williams C.L. Prenatal choline availability modulates hippocampal neurogenesis and neurogenic responses to enriching experiences in adult female rats. Eur. J. Neurosci. 25 (2007) 2473-2482
24. Gobbo O.L., and O'Mara S.M. Exercise, but not environmental enrichment, improves learning after kainic acid-induced hippocampal neurodegeneration in association with an increase in brain-derived neurotrophic factor. Behav. Brain Res. 159 (2005) 21-26
25. Golden G.T., Smith G.G., Ferraro T.N., Reyes P.F., Kulp J.K., and Fariello R.G. Strain differences in convulsive response to the excitotoxin kainic acid. Neuroreport 2 (1991) 141-144
26. Golden G.T., Smith G.G., Ferraro T.N., and Reyes P.F. Rat strain and age differences in kainic acid induced seizures. Epilepsy Res. 20 (1995) 151-159
27. Gomez-Pinilla F., So V., and Kesslak J.P. Spatial learning and physical activity contribute to the induction of fibroblast growth factor: neural substrates for increased cognition associated with exercise. Neuroscience 85 (1998) 53-61
28. Gorter J.A., Goncalves Pereira P.M., van Vliet E.A., Aronica E., Lopes da Silva F.H., and Lucassen P.J. Neuronal cell death in a rat model for mesial temporal lobe epilepsy is induced by the initial status epilepticus and not by later repeated spontaneous seizures. Epilepsia 44 (2003) 647-658
29. Haas K.Z., S. E., Opanashuk L.A., Stanton P.K., and Moshe S.L. Resistance of immature hippocampus to morphologic and physiologic alterations following status epilepticus or kindling. Hippocampus 11 (2001) 615-625
30. Hattiangady B., Rao M.S., and Shetty A.K. Chronic temporal lobe epilepsy is associated with severely declined dentate neurogenesis in the adult hippocampus. Neurobiol. Dis. 17 (2004) 473-490
31. Hellier J.L., and Dudek F.E. Spontaneous motor seizures of rats with kainate-induced epilepsy: effect of time of day and activity state. Epilepsy Res. 35 (1999) 47-57
32. Hellier J.L., Patrylo P.R., Buckmaster P.S., and Dudek F.E. Recurrent spontaneous motor seizures after repeated low-dose systemic treatment with kainate: assessment of a rat model of temporal lobe epilepsy. Epilepsy Res. 31 (1998) 73-84
33. Holmes G.L., Yang Y., Liu Z., Cermak J.M., Sarkisian M.R., Stafstrom C.E., Neill J.C., and Blusztajn J.K. Seizure-induced memory impairment is reduced by choline supplementation before or after status epilepticus. Epilepsy Res. 48 (2002) 3-13
34. Hort J., Brozek G., Mares P., Langmeier M., and Komarek V. Cognitive functions after pilocarpine-induced status epilepticus: changes during silent period precede appearance of spontaneous recurrent seizures. Epilepsia 40 (1999) 1177-1183
35. Houser C.R., and Esclapez M. Vulnerability and plasticity of the GABA system in the pilocarpine model of spontaneous recurrent seizures. Epilepsy Res. 26 (1996) 207-218
36. Jessberger S., Romer B., Babu H., and Kempermann G. Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp. Neurol. 196 (2005) 342-351
37. Jones J.P., Meck W.H., Williams C.L., Wilson W.A., and Swartzwelder H.S. Choline availability to the developing rat fetus alters adult hippocampal long-term potentiation. Brain Res., Dev. Brain Res. 118 (1999) 159-167
38. Jorgensen M.B., Finsen B.R., Jensen M.B., Castellano B., Diemer N.H., and Zimmer J. Microglial and astroglial reactions to ischemic and kainic acid-induced lesions of the adult rat hippocampus. Exp. Neurol. 120 (1993) 70-88
39. Kang T.C., Kim D.S., Kwak S.E., Kim J.E., Won M.H., Kim D.W., Choi S.Y., and Kwon O.S. Epileptogenic roles of astroglial death and regeneration in the dentate gyrus of experimental temporal lobe epilepsy. Glia 54 (2006) 258-271
40. Kash S.F., Johnson R.S., Tecott L.H., Noebels J.L., Mayfield R.D., Hanahan D., and Baekkeskov S. Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 14060-14065
41. Katoh-Semba R., Takeuchi I.K., Inaguma Y., Ito H., and Kato K. Brain-derived neurotrophic factor, nerve growth and neurotrophin-3 selected regions of the rat brain following kainic acid-induced seizure activity. Neurosci. Res. 35 (1999) 19-29
42. Kempermann G., Kuhn H.G., and Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature. 386 (1997) 493-495
43. Khrestchatisky M., Ferhat L., Charton G., Bernard A., Pollard H., Represa A., and Ben-Ari Y. Molecular correlates between reactive and developmental plasticity in the rat hippocampus. J. Neurobiol. 26 (1995) 426-436
44. Knipper M., da Penha Berzaghi M., Blochl A., Breer H., Thoenen H., and Lindholm D. Positive feedback between acetylcholine and the neurotrophins nerve growth factor and brain-derived neurotrophic factor in the rat hippocampus. Eur. J. Neurosci. 6 (1994) 668-671
45. Kobayashi M., and Buckmaster P.S. Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy. J. Neurosci. 23 (2003) 2440-2452
46. Kotloski R., Lynch M., Lauersdorf S., and Sutula T. Repeated brief seizures induce progressive hippocampal neuron loss and memory deficits. Prog. Brain Res. 135 (2002) 95-110
47. Kovacheva V.P., Mellott T.J., Davison J.M., Wagner N., Lopez-Coviella I., Schnitzler A.C., and Blusztajn J.K. Gestational choline deficiency causes global and Igf2 gene DNA hypermethylation by up-regulation of Dnmt1 expression. J. Biol. Chem. 282 (2007) 31777-31788
48. Kuhn H.G., Dickinson-Anson H., and Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16 (1996) 2027-2033
49. Lee J., Duan W., and Mattson M.P. 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. J. Neurochem. 82 (2002) 1367-1375
50. Lee J., Seroogy K.B., and Mattson M.P. Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice. J. Neurochem. 80 (2002) 539-547
51. Lindefors N., Ernfors P., Falkenberg T., and Persson H. Septal cholinergic afferents regulate expression of brain-derived neurotrophic factor and beta-nerve growth factor mRNA in rat hippocampus. Exp. Brain Res. 88 (1992) 78-90
52. Liu Z., and Holmes G.L. Basic fibroblast growth factor is highly neuroprotective against seizure-induced long-term behavioural deficits. Neuroscience 76 (1997) 1129-1138
53. Liu Z., D'Amore P.A., Mikati M., Gatt A., and Holmes G.L. Neuroprotective effect of chronic infusion of basic fibroblast growth factor on seizure-associated hippocampal damage. Brain Res. 626 (1993) 335-338
54. Liu Z., Gatt A., Werner S.J., Mikati M.A., and Holmes G.L. Long-term behavioral deficits following pilocarpine seizures in immature rats. Epilepsy Res. 19 (1994) 191-204
55. Marcinkiewicz M., Nagao T., Day R., Seidah N.G., Chretien M., and Avoli M. Pilocarpine-induced seizures are accompanied by a transient elevation in the messenger RNA expression of the prohormone convertase PC1 in rat hippocampus: comparison with nerve growth factor and brain-derived neurotrophic factor expression. Neuroscience 76 (1997) 425-439
56. McCann J.C., Hudes M., and Ames B.N. An overview of evidence for a causal relationship between dietary availability of choline during development and cognitive function in offspring. Neurosci. Biobehav. Rev. 30 (2006) 696-712
57. Meck W.H., and Williams C.L. Metabolic imprinting of choline by its availability during gestation: implications for memory and attentional processing across the lifespan. Neurosci. Biobehav. Rev. 27 (2003) 385-399
58. Meck W.H., Smith R.A., and Williams C.L. Pre- and postnatal choline supplementation produces long-term facilitation of spatial memory. Dev. Psychobiol. 21 (1988) 339-353
59. Meck W.H., Smith R.A., and Williams C.L. Organizational changes in cholinergic activity and enhanced visuospatial memory as a function of choline administered prenatally or postnatally or both. Behav. Neurosci. 103 (1989) 1234-1241
60. Mellott T.J., Williams C.L., Meck W.H., and Blusztajn J.K. Prenatal choline supplementation advances hippocampal development and enhances MAPK and CREB activation. FASEB J. 18 (2004) 545-547
61. Mellott T.J., Follettie M.T., Diesl V., Hill A.A., Lopez-Coviella I., and Blusztajn J.K. Prenatal choline availability modulates hippocampal and cerebral cortical gene expression. FASEB J. 21 (2007) 1311-1323
62. Mikati M.A., Tarif S., Lteif L., and Jawad M.A. Time sequence and types of memory deficits after experimental status epilepticus. Epilepsy Res. 43 (2001) 97-101
63. Milgram N.W., Yearwood T., Khurgel M., Ivy G.O., and Racine R. Changes in inhibitory processes in the hippocampus following recurrent seizures induced by systemic administration of kainic acid. Brain Res. 551 (1991) 236-246
64. Montoya D.A., White A.M., Williams C.L., Blusztajn J.K., Meck W.H., and Swartzwelder H.S. Prenatal choline exposure alters hippocampal responsiveness to cholinergic stimulation in adulthood. Brain Res., Dev. Brain Res. 123 (2000) 25-32
65. Morin F., Beaulieu C., and Lacaille J.C. Selective loss of GABA neurons in area CA1 of the rat hippocampus after intraventricular kainate. Epilepsy Res. 32 (1998) 363-369
66. Mouton P. Principles and Practices of Unbiased Stereology (2002), The Johns Hopkins University Press, Baltimore
67. Mudo G., Jiang X.H., Timmusk T., Bindoni M., and Belluardo N. Change in neurotrophins and their receptor mRNAs in the rat forebrain after status epilepticus induced by pilocarpine. Epilepsia 37 (1996) 198-207
68. Namchuk M., Lindsay L., Turck C.W., Kanaani J., and Baekkeskov S. Phosphorylation of serine residues 3, 6, 10, and 13 distinguishes membrane anchored from soluble glutamic acid decarboxylase 65 and is restricted to glutamic acid decarboxylase 65alpha. J. Biol. Chem. 272 (1997) 1548-1557
69. Niculescu M.D., Yamamuro Y., and Zeisel S.H. Choline availability modulates human neuroblastoma cell proliferation and alters the methylation of the promoter region of the cyclin-dependent kinase inhibitor 3 gene. J. Neurochem. 89 (2004) 1252-1259
70. Niculescu M.D., Craciunescu C.N., and Zeisel S.H. Dietary choline deficiency alters global and gene-specific DNA methylation in the developing hippocampus of mouse fetal brains. FASEB J 20 (2006) 43-49
71. Niquet J., Ben-Ari Y., and Represa A. Glial reaction after seizure induced hippocampal lesion: immunohistochemical characterization of proliferating glial cells. J. Neurocytol. 23 (1994) 641-656
72. Niquet J., Jorquera I., Ben-Ari Y., and Represa A. Proliferative astrocytes may express fibronectin-like protein in the hippocampus of epileptic rats. Neurosci. Lett. 180 (1994) 13-16
73. Obenaus A., Esclapez M., and Houser C.R. Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures. J. Neurosci. 13 (1993) 4470-4485
74. Okragly A.J., and Haak-Frendscho M. An acid-treatment method for the enhanced detection of GDNF in biological samples. Exp. Neurol. 145 (1997) 592-596
75. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., and Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17 (1997) 3727-3738
76. Parent J.M., Tada E., Fike J.R., and Lowenstein D.H. Inhibition of dentate granule cell neurogenesis with brain irradiation does not prevent seizure-induced mossy fiber synaptic reorganization in the rat. J. Neurosci. 19 (1999) 4508-4519
77. Pitkanen A., Kharatishvili I., Narkilahti S., Lukasiuk K., and Nissinen J. Administration of diazepam during status epilepticus reduces development and severity of epilepsy in rat. Epilepsy Res. 63 (2005) 27-42
78. Pyapali G.K., Turner D.A., Williams C.L., Meck W.H., and Swartzwelder H.S. Prenatal dietary choline supplementation decreases the threshold for induction of long-term potentiation in young adult rats. J. Neurophysiol. 79 (1998) 1790-1796
79. Racine R.J. Modification of seizure activity by electrical stimulation. II Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32 (1972) 281-294
80. Rao M.S., Hattiangady B., Abdel-Rahman A., Stanley D.P., and Shetty A.K. Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur. J. Neurosci. 21 (2005) 464-476
81. Rao M.S., Hattiangady B., and Shetty A.K. The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 5 (2006) 545-558
82. Rao M.S., and Shetty A.K. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur. J. Neurosci. 19 (2004) 234-246
83. Rashid K., Van der Zee C.E., Ross G.M., Chapman C.A., Stanisz J., Riopelle R.J., Racine R.J., and Fahnestock M. A nerve growth factor peptide retards seizure development and inhibits neuronal sprouting in a rat model of epilepsy. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 9495-9499
84. Reibel S., Larmet Y., Le B.T., Carnahan J., Marescaux C., and Depaulis A. Brain-derived neurotrophic factor delays hippocampal kindling in the rat. Neuroscience 100 (2000) 777-788
85. Represa A., Niquet J., Charriaut-Marlangue C., and Ben-Ari Y. Reactive astrocytes in the kainic acid-damage hippocampus have the phenotypic features of type-2 astrocytes. J. Neurocytol. 22 (1993) 299-310
86. Represa A., Niquet J., Pollard H., and Ben-Ari Y. Cell death, gliosis, and synaptic remodeling in the hippocampus of epileptic rats. J. Neurobiol. 26 (1995) 413-425
87. Rocamora N., Massieu L., Boddeke H.W., Palacios J.M., and Mengod G. Differential regulation of the expression of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 mRNAs in adult rat brain after intrahippocampal injection of quinolinic acid. Brain Res., Mol. Brain Res. 26 (1994) 89-98
88. Sandstrom N.J., Loy R., and Williams C.L. Prenatal choline supplementation increases NGF levels in the hippocampus and frontal cortex of young and adult rats. Brain Res. 947 (2002) 9-16
89. Sarkisian M.R., Tandon P., Liu Z., Yang Y., Hori A., Holmes G.L., and Stafstrom C.E. Multiple kainic acid seizures in the immature and adult brain: ictal manifestations and long-term effects on learning and memory. Epilepsia 38 (1997) 1157-1166
90. Scharfman H.E. Functional implications of seizure-induced neurogenesis. Adv. Exp. Med. Biol. 548 (2004) 192-212
91. Scharfman H.E., and Gray W.P. Relevance of seizure-induced neurogenesis in animal models of epilepsy to the etiology of temporal lobe epilepsy. Epilepsia 48 Suppl 2 (2007) 33-41
92. Scharfman H.E., Goodman J.H., and Sollas A.L. Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. J. Neurosci. 20 (2000) 6144-6158
93. Schmidt-Kastner R., Humpel C., Wetmore C., and Olson L. Cellular hybridization for BDNF, trkB, and NGF mRNAs and BDNF-immunoreactivity in rat forebrain after pilocarpine-induced status epilepticus. Exp. Brain Res. 107 (1996) 331-347
94. Seri B., Garcia-Verdugo J.M., McEwen B.S., and Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21 (2001) 7153-7160
95. Setkowicz Z., and Mazur A. Physical training decreases susceptibility to subsequent pilocarpine-induced seizures in the rat. Epilepsy Res. 71 (2006) 142-148
96. Shetty A.K., and Turner D.A. Glutamic acid decarboxylase-67-positive hippocampal interneurons undergo a permanent reduction in number following kainic acid-induced degeneration of ca3 pyramidal neurons. Exp. Neurol. 169 (2001) 276-297
97. Shetty A.K., Zaman V., and Shetty G.A. Hippocampal neurotrophin levels in a kainate model of temporal lobe epilepsy: a lack of correlation between brain-derived neurotrophic factor content and progression of aberrant dentate mossy fiber sprouting. J. Neurochem. 87 (2003) 147-159
98. Shetty A.K., Rao M.S., Hattiangady B., Zaman V., and Shetty G.A. Hippocampal neurotrophin levels after injury: relationship to the age of the hippocampus at the time of injury. J. Neurosci. Res. 78 (2004) 520-532
99. Sloviter R.S. Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235 (1987) 73-76
100. Smith P.D., McLean K.J., Murphy M.A., Turnley A.M., and Cook M.J. Seizures, not hippocampal neuronal death, provoke neurogenesis in a mouse rapid electrical amygdala kindling model of seizures. Neuroscience 136 (2005) 405-415
101. Sperber E.F., Haas K.Z., Stanton P.K., and Moshe S.L. Resistance of the immature hippocampus to seizure-induced synaptic reorganization. Brain Res., Dev. Brain Res. 60 (1991) 88-93
102. Stafstrom C.E., Chronopoulos A., Thurber S., Thompson J.L., and Holmes G.L. Age-dependent cognitive and behavioral deficits after kainic acid seizures. Epilepsia 34 (1993) 420-432
103. Stringer J.L. Repeated seizures increase GFAP and vimentin in the hippocampus. Brain Res. 717 (1996) 147-153
104. Sutula T., He X.X., Cavazos J., and Scott G. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 239 (1988) 1147-1150
105. Tao X., Finkbeiner S., Arnold D.B., Shaywitz A.J., and Greenberg M.E. Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20 (1998) 709-726
106. Thomas J.D., Garrison M., and O'Neill T.M. Perinatal choline supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats. Neurotoxicol. Teratol. 26 (2004) 35-45
107. Thomas J.D., Biane J.S., O'Bryan K.A., O'Neill T.M., and Dominguez H.D. Choline supplementation following third-trimester-equivalent alcohol exposure attenuates behavioral alterations in rats. Behav. Neurosci. 121 (2007) 120-130
108. Tian N., Petersen C., Kash S., Baekkeskov S., Copenhagen D., and Nicoll R. The role of the synthetic enzyme GAD65 in the control of neuronal gamma-aminobutyric acid release. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 12911-12916
109. Tooyama I., Bellier J.P., Park M., Minnasch P., Uemura S., Hisano T., Iwami M., Aimi Y., Yasuhara O., and Kimura H. Morphologic study of neuronal death, glial activation, and progenitor cell division in the hippocampus of rat models of epilepsy. Epilepsia. 43. Suppl. 9 (2002) 39-43
110. Van der Zee C.E., Rashid K., Le K., Moore K.A., Stanisz J., Diamond J., Racine R.J., and Fahnestock M. Intraventricular administration of antibodies to nerve growth factor retards kindling and blocks mossy fiber sprouting in adult rats. J. Neurosci. 15 (1995) 5316-5323
111. Wagner A.F., and Hunt P.S. Impaired trace fear conditioning following neonatal ethanol: reversal by choline. Behav. Neurosci. 120 (2006) 482-487
112. West M.J. New stereological methods for counting neurons. Neurobiol. Aging 14 (1993) 275-285
113. West M.J. Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci. 22 (1999) 51-61
114. Yang Y., Liu Z., Cermak J.M., Tandon P., Sarkisian M.R., Stafstrom C.E., Neill J.C., Blusztajn J.K., and Holmes G.L. Protective effects of prenatal choline supplementation on seizure-induced memory impairment. J. Neurosci. 20 (2000) RC109
115. Zeisel S.H. Nutritional importance of choline for brain development. J. Am. Coll. Nutr 23 (2004) 621S-626S
116. Zeisel S.H. Choline: critical role during fetal development and dietary requirements in adults. Annu. Rev. Nutr. 26 (2006) 229-250