Effects of postnatal dietary choline manipulation against MK-801 neurotoxicity in pre and postadolescent rats

Brain Research

Volumn 1362, Issue , 2010, Pages 117-132

  Biasi, Elisabetta ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DURHAM VA MEDICAL CENTER   (United States)

Author keywords

Choline; Dentate gyrus; MK 801; Neuroprotection; Piriform cortex

Indexed keywords

CHOLINE; DIZOCILPINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN REGION; CONTROLLED STUDY; DENTATE GYRUS; DIET SUPPLEMENTATION; FEMALE; HIPPOCAMPUS; HISTOLOGY; MALE; NERVE DEGENERATION; NEUROPROTECTION; NEUROTOXICITY; NEWBORN; NONHUMAN; POSTNATAL CARE; PREPUBERTY; PRIORITY JOURNAL; PYRIFORM CORTEX; RAT; RETROSPLENIAL REGION;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CHOLINE; CYTOPROTECTION; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; DIZOCILPINE MALEATE; FEMALE; MALE; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; NEUROTOXINS; RATS; RATS, SPRAGUE-DAWLEY;

ANIMALIA; RATTUS;

EID: 78149359178     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.09.012     Document Type: Article

References (182)

1. E. Acquas, C. Wilson, and H.C. Fibiger Conditions and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation, and fear J. Neurosci. 16 1996 3089 3096
2. C.D. Albright, C.B. Friedrich, E.C. Brown, M.H. Mar, and S.H. Zeisel Maternal dietary choline availability alters mitosis, apoptosis and the localization of TOAD-64 protein in the developing fetal rat septum Brain Res. Dev. Brain Res. 115 1999 123 129
3. C.D. Albright, A.Y. Tsai, C.B. Friedrich, M.H. Mar, and S.H. Zeisel Choline availability alters embryonic development of the hippocampus and septum in the rat Brain Res. Dev. Brain Res. 113 1999 13 20
4. M. Alkondon, E.F. Pereira, W.S. Cortes, A. Maelicke, and E.X. Albuquerque Choline is a selective agonist of alpha7 nicotinic acetylcholine receptors in the rat brain neurons Eur. J. Neurosci. 9 1997 2734 2742
5. H.L. Allen, and L.L. Iversen Phencyclidine, dizocilpine, and cerebrocortical neurons. Technical comments Science 247 1990 221
6. M.F. Anderson, M.A. Aberg, M. Nilsson, and P.S. Eriksson Insulin-like growth factor-I and neurogenesis in the adult mammalian brain Brain Res. Dev. Brain Res. 134 2002 115 122
7. P. Andine, N. Widermark, R. Axelsson, G. Nyberg, U. Olofsson, E. Martensson, and M. Sandberg Characterization of MK-801-induced behavior as a putative rat model of psychosis J. Pharmacol. Exp. Ther. 290 1999 1393 1408
8. R.N. Auer Effect of age and sex on N-methyl-d-aspartate antagonist-induced neuronal necrosis in rats Stroke 27 1996 743 746
9. M.G. Baxter, P.C. Holland, and M. Gallagher Disruption of decrements in conditioned stimulus processing by selective removal of hippocampal cholinergic input J. Neurosci. 17 1997 5230 5236
10. J. Bengzon, Z. Kokaia, E. Elmer, A. Nanobashvili, M. Kokaia, and O. Lindvall Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures Proc. Natl. Acad. Sci. 94 1997 10432 10437
11. J. Berger-Sweeney, S. Heckers, M.M. Mesulam, R.G. Wiley, D.A. Lappi, and M. Sharma Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis J. Neurosci. 14 1994 4507 4519
12. K. Borges, D. McDermott, H. Irier, Y. Smith, and R. Dingledine Degeneration and proliferation of astrocytes in the mouse dentate gyrus after pilocarpine-induced status epilepticus Exp. Neurol. 201 2006 416 427
13. R.J. Brady, P.E. Phelps, and J.E. Vaughn Neurogenesis of basal forebrain cholinergic neurons in rat Dev. Brain Res. 47 1989 81 92
14. C. Brandner Perinatal choline treatment modifies the effects of a visuo-spatial attractive cue upon spatial memory in naive adult rats Brain Res. 928 2002 85 95
15. A.J. Bruce-Keller, G. Umberger, R. McFall, and M.P. Mattson Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic insults Ann. Neurol. 45 1999 8 15
16. C.V. Buhusi, J.A. Lamoureux, and W.H. Meck Prenatal choline supplementation increases sensitivity to contextual processing of temporal information Brain Res. 1237 2008 204 213
17. N.Y. Calingasan, and G.E. Gibson Dietary restriction attenuates the neuronal loss, induction of heme oxygenase-1 and blood-brain barrier breakdown induced by impaired oxidative metabolism Brain Res. 885 2000 62 69
18. H.A. Cameron, B.S. McEwen, and E. Gould Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus J. Neurosci. 15 1995 4687 4692
19. H.A. Cameron, T.G. Hazel, and R.D. McKay Regulation of neurogenesis by growth factors and neurotransmitters J. Neurobiol. 36 1998 287 306
20. E. Castren, M. da Penha Berzaghi, D. Londholm, and H. Thoenen Differential effects of MK-801 on brain-derived neurotrophic factor mRNA levels in different regions of the rat brain Exp. Neurol. 122 1993 244 252
21. J.M. Cermak, T. Holler, D.A. Jackson, and J.K. Blusztajn Prenatal availability of choline modifies development of the hippocampal cholinergic system FASEB J. 12 1998 349 357
22. J.M. Cermak, J.K. Blusztajn, W.H. Meck, C.L. Williams, C.M. Fitzgerald, D.L. Rosene, and R. Loy Prenatal availability of choline alters the development of acetylcholinesterase in the rat hippocampus Dev. Neurosci. 21 1999 94 104
23. D.S. Charney, and A. Deutch A functional neuroanatomy of anxiety and fear: implications for the pathophysiology and treatment of anxiety disorders Crit. Rev. Neurobiol. 10 1996 419 446
24. R.K. Cheng, and W.H. Meck Prenatal choline supplementation increases sensitivity to time by reducing non-scalar sources of variance in adult temporal processing Brain Res. 1186 2007 242 254
25. R.K. Cheng, W.H. Meck, and C.L. Williams α7 nicotinic acetylcholine receptors and temporal memory: synergistic effects of combining prenatal choline and nicotine on reinforcement-induced resetting of an interval clock Learn. Mem. 13 2006 127 134
26. R.K. Cheng, A.C. Scott, T.B. Penney, C.L. Williams, and W.H. Meck Prenatal-choline supplementation differentially modulates timing of auditory and visual stimuli in aged rats Brain Res. 1237 2008 167 175
27. R.K. Cheng, C.J. MacDonald, C.L. Williams, and W.H. Meck Prenatal choline supplementation alters the timing, emotion, and memory performance (TEMP) of adult male and female rats as indexed by differential reinforcement of low-rate schedule behavior Learn. Mem. 15 2008 153 162
28. R.K. Cheng, A.C. Scott, C.L. Williams, and W.H. Meck Modality-specificity of duration discrimination in vision and audition as a function of prenatal choline availability Brain Res. 1237 2008 167 175
29. A. Contestabile, and E. Ciani Dietary restriction protects from neurodegeneration in animal models of excitotoxicity Brain Res. 1002 2004 162 166
30. T.D. Corso, M.A. Sesma, T.I. Tenkova, T.C. Der, D.F. Wozniak, N.B. Farber, and J.W. Olney Multifocal brain damage induced by phencyclidine is augmented by pilocarpine Brain Res. 752 1997 1 14
31. J.S. De Olmos, C.A. Beltramino, and A. de Olmos de Lorenzo Use of an amino-cupric-silver technique for the detection of early and semiacute neuronal degeneration caused by neurotoxicants, hypoxia, and physical trauma Neurotoxicol. Teratol. 16 1994 545 561
32. S. De Olmos, A. Bueno, C. Bender, A. Lorenzo, and J. De Olmos Sex differences and influence of gonadal hormones on MK801-induced neuronal degeneration in the granular retrosplenial cortex of the rat Brain Struct. Funct. 213 1-2 2008 229 238
33. W. Duan, J. Lee, Z. Guo, and M.P. Mattson Dietary restriction stimulates BDNF production in the brain and thereby protects neurons against excitotoxic injury J. Mol. Neurosci. 16 2001 1 12
34. W. Duan, Z. Guo, and M.P. Mattson Brain-derived neurotrophic factor mediates an excitoprotective effect of dietary restriction in mice J Neurochem. 76 2001 619 626
35. W. Duan, Z. Guo, H. Jiang, M. Ware, X.J. Li, and M.P. Mattson Dietary restriction normalizes glucose metabolism and BDNF levels, slows disease progression, and increases survival in huntingtin mutant mice Proc. Natl. Acad. Sci. 100 2003 2911 2916
36. G. Ellison Competitive and non-competitive NMDA antagonists induce similar limbic degeneration Neuroreport 5 1994 2688 2692
37. N.B. Farber, D.F. Wozniak, M.T. Price, J. Labruyere, J. Huss, H. St Peter, and J.W. Olney Age-specific neurotoxicity in the rat associated with NMDA receptor blockade: potential relevance to schizophrenia? Biol. Psychiatry 38 1995 788 796
38. P.A. Ferchmin, D. Perez, V.A. Eterovic, and J. de Vellis Nicotinic receptors differentially regulate N-methyl-d-aspartate damage in acute hippocampal slices J. Pharmacol. Exp. Ther. 305 2003 1071 1078
39. R.P. Fink, and L. Heimer Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system Brain Res. 4 1967 369 374
40. A.S. Fix, D.F. Wozniak, L.L. Trex, M. McEwan, J.P. Miller, and J.W. Olney Quantitative analyses of factors influencing neuronal necrosis induced by MK-801 in the rat posterior cingulated/retrosplenial cortex Brain Res. 696 1995 194 204
41. F.H. Gage Mammalian neural stem cells Science 287 2000 1433 1438
42. C.M. Gall, and P.J. Isackson Limbic seizures increase neuronal production of messenger RNA for nerve growth factor Science 245 1989 758 761
43. C. Gall, K. Murray, and P.J. Isackson Kainic acid-induced seizures stimulate increased expression of nerve growth factor mRNA in rat hippocampus Brain Res. Mol. Brain Res. 9 1991 113 123
44. F. Gallyas, J.R. Wolff, H. Böttcher, and L. Zaborszky A reliable and sensitive method to localize terminal degeneration and lysosomes in the central nervous system Stain Technol. 55 1980 299 306
45. F. Gallyas, F.H. Guldner, G. Zoltay, and J.R. Wolff Golgi-like demonstration of 'dark' neurons with an argyrophil III method for experimental neuropathology Acta Neuropathol. 79 1990 620 628
46. F. Gallyas, M. Hsu, and G. Buzsaki Four modified silver methods for thick sections of formaldehyde-fixed mammalian central nervous tissue: 'dark' neurons, perikarya of all neurons, microglial cells and capillaries J. Neurosci. Methods 50 1993 159 164
47. R.B. Gibbs, D. Wu, L.B. Hersh, and D.W. Pfaff Effects of estrogen replacement on the relative levels of choline acetyltransferase, trkA, and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adult rats Exp. Neurol. 129 1994 70 80
48. M.J. Glenn, E.M. Gibson, E.D. Kirby, T.J. Mellott, J.K. Blusztajn, and C.L. Williams Prenatal choline availability modulates hippocampal neurogenesis and neurogenic responses to enriching experiences in adult female rats Eur. J. Neurosci. 25 2007 2473 2482
49. M.J. Glenn, E.D. Kirby, E.M. Gibson, S.J. Wong-Goodrich, T.J. Mellott, J.K. Blusztajn, and C.L. Williams Age-related declines in exploratory behavior and markers of hippocampal plasticity are attenuated by prenatal choline supplementation in rats Brain Res. 1237 2008 110 123
50. O.L. Gobbo, and S.M. O'Mara 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
51. F. Gomez-Pinilla, V. So, and J.P. Kesslak 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
52. E. Gould, H.A. Cameron, and B.S. McEwen Blockade of NMDA receptors increases cell death and birth in the developing dentate gyrus J. Comp. Neurol. 1340 1994 551 565
53. Z. Guo, A. Ersoz, D.A. Butterfield, and M.P. Mattson Beneficial effects of dietary restriction on cerebral cortical synaptic terminals: preservation of glucose transport and mitochondrial function after exposure to amyloid β-peptide and oxidative and metabolic insults J. Neurochem. 75 2000 314 320
54. S.X. Guo-Ross, S. Clark, D.A.C. Montoya, K.H. Jones, J. Obernier, A.K. Shetty, A.M. White, J.K. Blusztajn, W.A. Wilson, and H.S. Swartzwelder Prenatal choline supplementation protects against postnatal neurotoxicity J. Neurosci. 21 195 2002 1 6
55. S.X. Guo-Ross, K.H. Jones, A.K. Shetty, W.A. Wilson, and H.S. Swartzwelder Prenatal dietary choline availability alters postnatal neurotoxic vulnerability in the adult rat Neurosci. Lett. 341 2003 161 163
56. K. Hashimoto, S. Tomitaka, N. Narita, Y. Minabe, M. Iyo, and S. Fukui Induction of heat shock protein (HSP)-70 in posterior cingulate and retrosplenial cortex of rat brain by dizocilpine and phencyclidine: lack of protective effects of receptor ligands Addict. Biol. 1 1996 61 70
57. K. Hashimoto, S. Tomitaka, Y. Bi, N. Marita, Y. Minabe, and M. Iyo Rolipram, a selective phosphodiesterase type-IV inhibitor, prevents induction of heat shock protein HSP-70 and hsp-70 mRNA in rat retrosplenial cortex by dizocilpine Eur. J. Neurosci. 9 1997 1891 1901
58. K. Hashimoto, Y. Minabe, and M. Iyo Expression of brain derived neurotrophic factor (BDNF) mRNA in rat retrosplenial cortex following administration of PCP Addict. Biol. 3 1998 79 83
59. G.L. Holmes, Y. Yang, Z. Liu, J.M. Cermak, M.R. Sarkisian, C.E. Stafstrom, J.C. Neill, and J.K. Blusztajn Seizure-induced memory impairment is reduced by choline supplementation before or after status epilepticus Epilepsy Res. 48 2002 3 13
60. D. Hönack, and W. Löscher Sex differences in NMDA receptor mediated responses in rats Brain Res. 620 1993 167 170
61. Z.C. Horvath, J. Czopf, and G. Buzsaki Research report MK-801-induced neuronal damage in rats Brain Res. 753 1997 181 195
62. M. Hsu, and G. Buzsaki Vulnerability of mossy fiber targets in the rat hippocampus to forbrain ischemia J. Neurosci. 13 1993 3964 3979
63. P. Hughes, M. Dragunow, E. Beiharz, P. Lawlor, and P. Gluckman MK-801 induces immediate-early gene proteins and BDNF mRNA in rat cerebrocortical neurons Neuroreport 4 1993 183 186
64. D.N.C. Jones, J.C. Barnes, D.L. Kirkby, and G.A. Higgins Age-associated impairments in a test of attention: evidence for involvement of cholinergic systems J. Neurosci. 15 1995 7282 7292
65. J.P. Jones, W.H. Meck, C.L. Williams, W.A. Wilson, and H.S. Swartzwelder Choline availability to the developing rat fetus alters adult hippocampal long-term potentiation Dev. Brain Res. 118 1999 159 167
66. R. Katoh-Semba, I.K. Takeuchi, Y. Inaguma, H. Ito, and K. Kato 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
67. G. Kempermann, H.G. Kuhn, and F.H. Gage Experience-induced neurogenesis in the senescent dentate gyrus J. Neurosci. 18 1998 3206 3212
68. J.H. Krystal, L.P. Karper, J.P. Seibyl, G.K. Freeman, R. Delaney, J.D. Bremner, G.R. Heninger, M.B. Bowers Jr., and D.S. Charney Subanesthetic effects of the non competitive NMDA antagonist, ketamine, in humans Arch. Gen. Psychiatry 51 1994 199 214
69. H.G. Kuhn, H. Dickinson-Anson, and F.H. Gage Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation J. Neurosci. 16 1996 2027 2033
70. S. Lee, J. Williamson, E.W. Lothman, F.G. Szele, M.F. Chesselet, S. Von Hagen, R.M. Sapolsky, M.P. Mattson, and S. Christakos Early induction of mRNA for calbindin-D28k and BDNF but not NT-3 in rat hippocampus after kainic acid treatment Mol. Brain Res. 47 1997 183 194
71. J. Lee, W. Duan, J.M. Long, D.K. Ingram, and M.P. Mattson Dietary restriction increases survival of newly-generated neural cells and induces BDNF expression in the dentate gyrus of rats J. Mol. Neurosci. 15 2000 99 108
72. J. Lee, K.B. Seroogy, and M.P. Mattson Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice J. Neurochem. 80 2002 539 547
73. J. Lee, W. Duan, and M.P. Mattson Evidence that BDNF 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
74. X. Li, P. Somogyi, A. Ylinen, and G. Buzsaki The hippocampal CA3 network: an in vivo intracellular labelling study J. Comp. Neurol. 339 1994 181 208
75. Q. Li, S. Clark, W.A. Wilson, and D.V. Lewis MK-801, an NMDA receptor antagonist, modulates the inhibitory postsynaptic currents in pyramidal neurons in the cingulate cortex of rats Soc. Neurosci. Abstr. 26 2000 431
76. Q. Li, S. Clark, D.V. Lewis, and W.A. Wilson NMDA receptor antagonists disinhibit rat posterior cingulate and retrosplenial cortices: a potential mechanism of neurotoxicity J. Neurosci. 22 2002 3070 3080
77. Y. Li, E.M. Meyer, D.W. Walker, W.J. Millard, Y.J. He, and M.A. King Alpha7 nicotinic receptor activation inhibits ethanol-induced mitochondrial dysfunction, cytochrome c release and neurotoxicity in primary rat hippocampal neuronal cultures J. Neurochem. 81 2002 853 858
78. Q. Li, S. Guo-Ross, D.V. Lewis, D. Turner, A.M. White, W.A. Wilson, and H.S. Swartzwelder Dietary prenatal choline supplementation alters postnatal hippocampal structure and function J. Neurophysiol. 91 2004 1545 1555
79. N. Lindefors, P. Ernfors, T. Falkenberg, and H. Persson 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
80. D.H. Lowenstein, and L. Arsenault The effects of growth factors on the survival and differentiation of cultured dentate gyrus neurons J. Neurosci. 16 1996 1759 1769
81. R. Loy, D. Heyer, C.L. Williams, and W.H. Meck Choline-induced spatial memory facilitation correlates with altered distribution and morphology of septal neurons Adv. Exp. Med. Biol. 295 1991 373 382
82. R.J. Maddock The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain Trends Neurosci. 22 1999 310 316
83. Z.F. Mainen, and T.J. Sejnowski Influence of dendritic structure on firing pattern in model neocortical neurons Nature 382 1996 363 366
84. H. Matsuki, Y. Shirayama, K. Hashimoto, A. Tanaka, and Y. Minabe Effects of age and gender on the expression of brain-derived neurotrophic factor mRNA in rat retrosplenial cortex following administration of dizocilpine Neuropsychopharmacology 25 2001 258 266
85. S. Matsuyama, A. Matsumoto, T. Enomoto, and T. Nishizaki Activation of nicotinic acetylcholine receptors induces long-term potentation in vivo in the intact mouse dentate gyrus Eur. J. Neurosci. 12 2000 3741 3747
86. J.C. McCann, M. Hudes, and B.N. Ames An overview of evidence for a causal relationship between dietary availability of choline during development and cognitive function in offspring Neurosci. Behav. Rev. 30 2006 696 712
87. P.J. McMillan, C.A. Singer, and D.M. Dorsa Effects of ovariectomy and estrogen replacement on trkA and choline acetyltransferase mRNA expression in the rat basal forebrain J. Neurosci. 16 1996 1860 1865
88. W.H. Meck, and C.L. Williams Characterization of the facilitative effects of perinatal choline supplementation on timing and temporal memory Neuroreport 8 1997 2831 2835
89. W.H. Meck, and C.L. Williams Simultaneous temporal processing is sensitive to prenatal choline availability in mature and aged rats Neuroreport 8 1997 3045 3051
90. W.H. Meck, and C.L. Williams Perinatal choline supplementation increases the threshold for chunking in spatial memory Neuroreport 8 1997 3053 3059
91. W.H. Meck, and C.L. Williams Choline supplementation during prenatal development reduces proactive interference in spatial memory Dev. Brain Res. 118 1999 51 59
92. W.H. Meck, and C.L. Williams 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
93. W.H. Meck, R.A. Smith, and C.L. Williams Pre- and postnatal choline supplementation produces long-term facilitation of spatial memory Dev. Psychobiol. 21 1988 339 353
94. W.H. Meck, R.A. Smith, and C.L. Williams Organizational changes in cholinergic activity and enhanced visuospatial memory as a function of choline administered prenatally or postnatally or both Behav. Neurosci. 109 1989 1234 1241
95. W.H. Meck, C.L. Williams, J.M. Cermak, and J.K. Blusztajn Developmental periods of choline sensitivity provide an ontogenetic mechanism for regulating memory capacity and age-related dementia Front. Integr. Neurosci. 1 2008 7
96. T.J. Mellott, M.T. Follettie, V. Diesl, A.A. Hill, I. Lopez-Coviella, and J.K. Blusztajn Prenatal choline availability modulates hippocampal and cerebral cortical gene expression FASEB J. 21 2007 1311 1323
97. T.J. Mellott, N.W. Kowall, I. Lopez-Coviella, and J.K. Blusztajn Prenatal choline deficiency increases choline transporter expression in the septum and hippocampus during postnatal development and in adulthood in rats Brain Res. 1151 2007 1 11
98. A. Mendelowitscha, M.-F. Ritzb, J. Rosb, H. Langemannb, and O. Gratzl 17β-Estradiol reduces cortical lesion size in the glutamate excitotoxicity model by enhancing extracellular lactate: a new neuroprotective pathway Brain Res. 901 2001 230 236
99. E.M. Meyer, E.T. Tay, J.A. Zoltewicz, C. Meyers, M.A. King, R.L. Papke, and C.M. De Fiebre Neuroprotective and memory-related actions of novel alpha-7 nicotinic agents with different mixed agonist/antagonist properties J. Pharmacol. Exp. Ther. 284 1998 1026 1032
100. E.G. Mohler, W.H. Meck, and C.L. Williams Sustained attention in adult mice is modulated by prenatal choline availability Int. J. Comp. Psychol. 14 2001 136 150
101. D. Montoya, and H.S. Swartzwelder Prenatal choline supplementation alters hippocampal N-methyl-d-aspartate receptor-mediated neurotransmission in adult rats Neurosci. Lett. 296 2000 85 88
102. Moore, J.A., 2008. Effects of subcutaneous postnatal choline supplementation on hippocampus-mediated learning and memory in rat pups. In drc.ohiolink.edu/handle/2374.OX/19628.
103. J.L. Muir, S.B. Dunnett, T.W. Robbins, and B.J. Everitt Attentional functions of the forebrain cholinergic systems: effects of intraventricular hemicholinium, physostigmine, basal forebrain lesions and intracortical grafts on a multiple-choice serial reaction time task Exp. Brain Res. 89 1992 611 622
104. J.L. Muir, B.J. Everitt, and T.W. Robbins AMPA-induced excitotoxic lesions of the basal forebrain: a significant role for the cortical cholinergic system in attentional function J. Neurosci. 14 1994 2313 2326
105. P.J. Mulholland, R.L. Self, B.R. Harris, J.M. Littleton, and M.A. Prendergast Choline exposure reduces potentiation of N-methyl-d-aspartate toxicity by corticosterone in the developing hippocampus Develop. Brain Res. 153 2004 203 211
106. T. Nabeshima, K. Yamaguchi, K. Yamada, M. Hiramatsu, Y. Kuwabara, H. Furukawa, and T. Kameyama Sexdependent differences in the pharmacological actions and pharmacokinetics of phencyclidine Eur. J. Pharmacol. 97 1984 217 227
107. N. Nag, and J.E. Berger-Sweeney Postnatal dietary choline supplementation alters behavior in a mouse model of Rett syndrome Neurobiol. Dis. 26 2007 473 480
108. N. Nag, T.J. Mellott, and J.E. Berger-Sweeney Effects of postnatal dietary choline supplementation on motor regional brain volume and growth factor expression in a mouse model of Rett syndrome Brain Res. 1237 2008 101 109
109. N. Nakamura, H. Fujita, and M. Kawata Effects of gonadectomy on immunoreactivity for choline acetyltransferase in the cortex, hippocampus, and basal forebrain of adult male rats Neuroscience 109 2002 473 485
110. I. Napoli, J.K. Blusztajn, and T.J. Mellott Prenatal choline supplementation in rats increases the expression of IGF2 and its receptor IGF2R and enhances IGF2-induced acetylcholine release in hippocampus and frontal cortex Brain Res. 1237 2008 124 135
111. National Research Council, 2002. Guide for the Care and Use of Laboratory Animals, 6th ed. National Academy Press, Washington, D.C., pp.1-125.
112. W.J.H. Nauta, and P.A. Gygax Silver impregnation of degenerating axons in the central nervous system: a modified technic Biotech. Histochem. 29 1954 91 93
113. J. Niquet, Y. Ben-Ari, and A. Represa Glial reaction after seizure induced hippocampal lesion: immunohistochemical characterization of proliferating glial cells J. Neurocytol. 23 1994 641 656
114. K.K. Noguchi, B. Nemmers, and N.B. Farber Age has a similar influence on the susceptibility to NMDA antagonist-induced neurodegeneration in most brain regions Brain Res. Dev. Brain Res. 158 2005 82 91
115. K. Ogita, N. Nishiyama, C. Sugiyama, K. Higuchi, M. Yoneyama, and Y. Yoneda Regeneration of granule neurons after lesioning of hippocampal dentate gyrus: evaluation using adult mice treated with trimethyltin chloride as a model J. Neurosci. Res. 82 2005 609 621
116. J.W. Olney, and N.B. Farber Glutamate receptor dysfunction and schizophrenia Arch. Gen. Psychiatry 52 1995 998 1007
117. J.W. Olney, J. Labruyere, and M.T. Price Pathological changes induced in cerebrocortical neurons by phencyclidine and related drugs Science 244 1989 1360 1362
118. J.W. Olney, J. Labruyere, G. Wang, D.F. Wozniak, M.T. Price, and M.A. Sesma NMDA antagonist neurotoxicity: mechanism and prevention Science 254 1991 1515 1518
119. R.L. Papke, and J.K. Porter Papke Comparative pharmacology of rat and human alpha7 nAChR conducted with net charge analysis Br. J. Pharmacol. 137 2002 49 61
120. J.M. Parent, T.W. Yu, R.T. Leibowitz, D.H. Geschwind, R.S. Sloviter, and D.H. Lowenstein 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
121. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 5th ed. 2005 Elsevier Academic Press New York 1 367
122. R.N. Pechnick, R. George, and R.E. Poland Characterization of the effects of the acute and repeated administration of MK-801 on the release of adrenocorticotropin, corticosterone and prolactin in the rat Eur. J. Pharmacol. 164 1989 257 263
123. T.A. Prolla, and M.P. Mattson Molecular mechanisms of brain aging and neurodegenerative disorders: lessons from dietary restriction Trends Neurosci. 24 2001 521 531
124. G.K. Pyapali, D.A. Turner, C.L. Williams, W.H. Meck, and H.S. Swartzwelder Prenatal dietary choline supplementation decreases the threshold for induction of long-term potentiation in young adult rats J. Neurophysiol. 79 1998 1790 1796
125. P.J. Raubenheimer, M.J. Nyirenda, R. Brian, and A. Walker Choline-deficient diet exacerbates fatty liver but attenuates insulin resistance and glucose intolerance in mice fed a high-fat diet Diabetes 55 2006 2015 2020
126. S. Reibel, Y. Larmet, B.T. Le, J. Carnahan, C. Marescaux, and A. Depaulis Brain-derived neurotrophic factor delays hippocampal kindling in the rat Neuroscience 100 2000 777 788
127. L. Ricceri, and J. Berger-Sweeney Postnatal choline supplementation in preweanling mice: sexually dimorphic behavioral and neurochemical effects Behav. Neurosci. 112 1998 1387 1392
128. N. Rocamora, L. Massieu, H.W. Boddeke, J.M. Palacios, and G. Mengod 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
129. N.J. Sandstrom, R. Loy, and C.L. Williams Prenatal choline supplementation increases NGF levels in the hippocampus and frontal cortex of young and adult rats Brain Res. 947 2002 9 16
130. F. Schenk, and C. Brandner Indirect effect of peri- and postnatal choline treatment on place-learning abilities in rat Psychobiology 35 1995 302 313
131. L.C. Schmued, and K.J. Hopkins Fluorojade. Novel fluorochromes for detecting toxicant-induced neuronal degeneration Toxicol. Pathol. 28 2000 91 99
132. L.C. Schmued, C. Albertson, and W. Slikker Jr. Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration Brain Res. 751 1997 37 46
133. P.H. Schwartz, and C.G. Wasterlain Cardiac arrest and resuscitation alters the pharmacokinetics of MK-801 in the rat Res. Commun. Chem. Pathol. Pharmacol. 73 1991 181 195
134. K. Semba, and H.C. Fibiger Organization of central cholinergic systems Prog. Brain Res. 79 1989 37 63
135. L. Seress, and J. Pokorny Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study J. Anat. 133 1981 181 195
136. B. Seri, J.M. Garcia-Verdugo, B.S. McEwen, and A. Alvarez-Buylla Astrocytes give rise to new neurons in the adult mammalian hippocampus J. Neurosci. 21 2001 7153 7160
137. F.R. Sharp, and S.M. Sagar Alterations in gene expression as an index of neuronal injury: heat shock and the immediate early gene response Neurotoxicology 15 1994 51 60
138. F.R. Sharp, P. Jasper, J. Hall, J. Noble, and S.M. Sagar MK-801 and ketamine induce heat shock protein HSP70 in injured neurons in posterior cingulate and retrosplenial cortex Ann. Neurol. 30 1991 801 809
139. F.R. Sharp, M. Butman, K. Aardalen, J. Nickolenko, R. Nakki, S.M. Massa, R.A. Swanson, and S.M. Sagar Neuronal injury produced by NMDA receptor antagonists can be detected using heat shock proteins and can be blocked with antipsychotics Psychopharmacol. Bull. 30 1994 555 560
140. F.R. Sharp, M. Tomitaka, M. Bernaudin, and S. Tomitaka Psychosis: pathological activation of limbic thalamocortical circuits by psychomimetics and schizophrenia? Trends Neurosci. 24 2001 330 334
141. G.M. Shaw, S.L. Carmichael, W. Yang, S. Selvin, and D.M. Schaffer Periconceptional dietary intake of choline and betaine and neural tube defects in offspring Am. J. Epidemiol. 160 2004 102 109
142. A.K. Shetty, M.S. Rao, B. Hattiangady, V. Zaman, and G.A. Shetty Hippocampal neurotrophin levels after injury: relationship to the age of the hippocampus at the time of injury J. Neurosci. Res. 78 2004 520 532
143. C.A. Singer, X.A. Figueroa-Masot, R.H. Batchelor, and D.M. Dorsa The mitogen-activated protein kinase pathway mediates estrogen neuro-protection after glutamate toxicity in primary cortical neurons J. Neurosci. 19 1999 2455 2463
144. M. Singh, E.M. Meyer, and J.W. Simpkins The effect of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats Endocrinology 136 1995 2320 2324
145. S.R. Sohal, S. Agarwal, M. Candas, M.J. Foster, and H. Lal Effect of age and caloric restriction on DNA oxidative damage in different tissues of C57BL/6 mice Mech. Ageing Dev. 76 1994 215 224
146. F. Sohrabji, L.A. Greene, R.C. Mirando, and C.D. Toran-Allerand Reciprocal regulation of estrogen and NGF receptors by their ligands in PC12 cells J. Neurobiol. 25 1994 974 988
147. F. Sohrabji, R.C. Mirando, and C.D. Toran-Allerand Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons J. Neurosci. 14 1994 459 471
148. S.S. Stensaas, C.Q. Edwards, and L.J. Stensaas An experimental study of hyperchromic nerve cells in the cerebral cortex Exp. Neurol. 36 1972 472 487
149. S. Sveinbjornsdottir, J.W.A.S. Sander, D. Upton, P.J. Thompson, P.N. Patsalos, D. Hirt, M. Emre, D. Lowe, and J.S. Duncan The excitatory amino acid antagonist D-CPP-ene (SDZ EAA-494) in patients with epilepsy Epilepsy Res. 16 1993 165 174
150. J. Takahashi, T.D. Palmer, and F.H. Gage Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures J. Neurobiol. 38 1999 65 81
151. R.C. Tees The influences of rearing environment and neonatal choline dietary supplementation on spatial learning and memory in adult rats Behav. Brain Res. 105 1999 173 188
152. R.C. Tees The influences of sex, rearing environment, and neonatal choline dietary supplementation on spatial and nonspatial learning and memory in adult rats Dev. Psychobiol. 35 1999 328 342
153. R.C. Tees, and E. Mohammadi The effects of neonatal choline dietary supplementation on adult spatial and configural learning and memory in rats Dev. Psychobiol. 35 1999 226 240
154. J.D. Thomas, M.H. La Fiette, V.R. Quinn, and E.P. Riley Neonatal choline supplementation ameliorates the effects of prenatal alcohol exposure on a discrimination learning task in rats Neurotoxicol. Teratol. 22 2000 703 711
155. J.D. Thomas, M. Garrison, and T.M. O'Neill Perinatal choline supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats Neurotoxicol. Teratol. 26 2004 35 45
156. J.D. Thomas, J.S. Biane, K.A. O'Bryan, T.M. O'Neill, and H.D. Dominguez Choline supplementation following third-trimester-equivalent alcohol exposure attenuates behavioral alterations in rats Behav. Neurosci. 121 2007 120 130
157. J.D. Thomas, J.E. Abou, and H.D. Dominguez Prenatal choline supplementation mitigates the adverse effects of prenatal alcohol exposure on development in rats Neurotoxicol. Teratol. 31 2009 303 311
158. N. Tian, C. Petersen, S. Kash, S. Baekkeskov, D. Copenhagen, and R. Nicoll The role of the synthetic enzyme GAD65 in the control of neuronal gamma-aminobutyric acid release Proc. Natl. Acad. Sci. 96 1999 12911 12916
159. S. Tomitaka, K. Hashimoto, N. Marita, A. Sakamoto, Y. Minabe, and A. Tamura Memantine induces heat shock protein HSP70 in the posterior cingulated cortex, retrosplenial cortex and dentate gyrus of rat brain Brain Res. 740 1996 1 5
160. S. Tomitaka, M. Tomitaka, B.K. Tolliver, and F.R. Sharp Bilateral blockade of NMDA receptors in anterior thalamus by dizocilpine (MK-801) injures pyramidal neurons in rat retrosplenial cortex Eur. J. Neurosci. 12 2000 1420 1430
161. K. Utsugisawa, Y. Nagane, D. Obara, and H. Tohgi Overexpression of alpha7 nicotinic acetylcholine receptor prevents G1-arrest and DNA fragmentation in PC12 cells after hypoxia J. Neurochem. 81 2002 497 505
162. A.N. Van den Pol, and F. Gallyas Trauma-induced Golgi-like staining of neurons: a new approach to neuronal organization and response to injury J. Comp. Neurol. 296 1990 654 673
163. S.D. Vann, and J.P. Aggleton Extensive cytotoxic lesions of the rat retrosplenial cortex reveal consistent deficits on tasks that tax allocentric special memory Behav. Neurosci. 116 2002 85 94
164. P. Vetter, A. Roth, and M. Hausser Propagation of action potentials in dendrites depend on dendritic morphology J. Neurophysiol. 85 2001 926 937
165. A. Vezzani, R. Serafini, M.A. Stasi, S. Caccia, I. Conti, R.V. Tridico, and R. Samanin Kinetics of MK-801 and its effect on quinolinic acid-induced seizures and neurotoxicity in rats J. Pharmacol. Exp. Ther. 249 1989 278 283
166. B.A. Vogt, D.M. Finch, and C.R. Olson Functional heterogeneity in cingulated cortex: the anterior executive and posterior evaluative regions Cereb. Cortex 2 1992 435 443
167. A.F. Wagner, and P.S. Hunt Impaired trace fear conditioning following neonatal ethanol: reversal by choline Behav. Neurosci. 120 2006 482 487
168. H.A. Wilkinson, K.M. Davidson, and R.I. Davidson Bilateral anterior cingulotomy for chronic noncancer pain Neurosurgery 45 1999 1129 1145
169. C.L. Williams, W.H. Meck, D.D. Heyer, and R. Loy Hypertrophy of basal forebrain neurons and enhanced visuospatial memory in perinatally choline-supplemented rats Brain Res. 794 1998 225 238
170. S.J.E. Wong-Goodrich, T.J. Mellott, M.J. Glenn, J.K. Blusztajn, and C.L. Williams Prenatal choline supplementation attenuates neuropathological response to status epilepticus in the adult rat hippocampus Neurobiol. Dis. 30 2008 255 269
171. C.S. Woolley Estradiol facilitates kainic acid-induced, but not flurothyl-induced, behavioral seizure activity in adult female rats Epilepsia 41 2000 510 515
172. C.S. Woolley, N.G. Weiland, B.S. McEwen, and P.A. Schwartzkroin Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density J. Neurosci. 17 1997 1848 1859
173. D.F. Wozniak, K. Dikranian, M. Ishimaru, A. Nardi, T.D. Corso, T.I. Tenkova, J.W. Olney, and A.S. Fix Disseminated corticolimbic neuronal degeneration induced in rat brain by MK-801: potential relevance to Alzheimer's disease Neurobiol. Dis. 5 1998 305 322
174. Y. Yang, Z. Liu, J.M. Cermak, P. Tandon, M.R. Sarkisian, C.E. Stafstrom, J.C. Neill, J.K. Blusztajn, and G.L. Holmes Protective effects of prenatal choline supplementation on seizure-induced memory impairment J. Neurosci. 20 2000 1 6
175. 1-7 cells through an estrogen receptor-dependent mechanism NeuroToxicol. 24 2003 65 73
176. J.M. Yeung, and E. Friedman Effect of aging and diet restriction on monoamines and amino acids in cerebral cortex of Fischer-344 rats Growth Dev. Aging 55 1991 275 283
177. D. Young, P.A. Lawlor, P. Leone, M. Dragunow, and M.J. During Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective Nat. Med. 5 1999 448 453
178. A. Zanardi, G. Leo, G. Bigini, and M. Zoli Nicotine and neurodegeneration in ageing Toxicol. Lett. 127 2002 207 215
179. S.H. Zeisel Choline: critical role during fetal development and dietary requirements in adults Annu Rev Nutr. 26 2006 229 250
180. Zeisel, S.H., 2007. Estrogen protects pregnant women from choline deficiency. UNC School of Public Health. Edition of the Journal of the Federation of American Societies for Experimental Biology (FASEB).
181. S.H. Zeisel, and J.K. Blusztajn Choline and human nutrition Annu Rev Nutr. 14 1994 269 296
182. H. Zhu, Q. Guo, and M.P. Mattson Dietary restriction protects hippocampal neurons against the death-promoting action of a presenilin-1 mutation Brain Res. 842 1999 224 229