Effect of neonatal isolation on outcome following neonatal seizures in rats - The role of corticosterone

Epilepsy Research

Volumn 68, Issue 2, 2006, Pages 123-136

  Lai, Ming Chi ^a,b   Holmes, Gregory L ^c   Lee, Ko Hung ^d   Yang, San Nan ^a,e   Wang, Chien An ^a,f   Wu, Chia Lu ^e   Tiao, Mao Meng ^e   Hsieh, Chih Sung ^e   Lee, Chiang Hsuan ^b   Huang, Li Tung ^e  

^a CHANG GUNG UNIVERSITY   (Taiwan)

^b CHI MEI FOUNDATION HOSPITAL   (Taiwan)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

^d NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^e CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^f E DA HOSPITAL   (Taiwan)

Author keywords

Corticosterone; Metyrapone; Neonatal isolation; Neonatal seizures; Spatial learning and memory

Indexed keywords

CORTICOSTERONE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; LITHIUM CHLORIDE; METYRAPONE; PHOSPHOSERINE; PILOCARPINE; SERINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOSTERONE RELEASE; DOSE RESPONSE; DRUG EFFECT; DRUG POTENTIATION; EPILEPTIC STATE; HIPPOCAMPUS; LEARNING; MALE; MATERNAL DEPRIVATION; NERVE CELL LESION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SEIZURE; SEIZURE THRESHOLD; SPATIAL MEMORY;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; CONVULSANTS; CORTICOSTERONE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENZYME INHIBITORS; HIPPOCAMPUS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; KINDLING, NEUROLOGIC; LITHIUM; MALE; MATERNAL DEPRIVATION; MAZE LEARNING; METYRAPONE; PHOSPHORYLATION; PILOCARPINE; PITUITARY-ADRENAL SYSTEM; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SOCIAL ISOLATION; SPATIAL BEHAVIOR; STATUS EPILEPTICUS;

EID: 31544464382     PISSN: 09201211     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2005.10.005     Document Type: Article

References (81)

1. S. Avishai-Eliner, K.L. Brunson, C.A. Sandman, and T.Z. Baram Stressed-out, or in (utero)? Trends Neurosci. 25 2002 518 524
2. J.W. Brown, and L.M. Fishman Biosynthesis and metabolism of steroid hormones by human adrenal carcinomas Braz. J. Med. Biol. Res. 33 2000 1235 1244
3. K.L. Brunson, N. Khan, M. Eghbal-Ahmadi, and T.Z. Baram Corticotropin (ACTH) acts directly on amygdala neurons to down-regulate corticotropin- releasing hormone gene expression Ann. Neurol. 49 2001 304 312
4. J.C. Butte, R. Kakihana, and E.P. Noble Circadian rhythm of corticosterone levels in rat brain J. Endocrinol. 68 1976 235 239
5. M.R. Cilio, Y. Sogawa, B.H. Cha, Z. Liu, L.T. Huang, and G.L. Holmes Long-term effects of status epilepticus in the immature brain are age- and model-specific Epilepsia 44 2003 518 528
6. A receptors in rats Pharmacol. Biochem. Behav. 78 2004 495 504
7. D.B. Clifford, J.W. Olney, A. Maniotis, R.C. Collins, and C.F. Zorumski The functional anatomy and pathology of lithium-pilocarpine and high-dose pilocarpine seizures Neuroscience 23 1987 953 968
8. R. Druga, P. Mares, J. Otahal, and H. Kubova Degenerative neuronal changes in the rat thalamus induced by status epilepticus at different developmental stages Epilepsy Res. 63 2005 43 65
9. C. Dube, S. Boyet, C. Marescaux, and A. Nehlig Progressive metabolic changes underlying the chronic reorganization of brain circuits during the silent phase of the lithium-pilocarpine model of epilepsy in the immature and adult rat Exp. Neurol. 162 2000 146 157
10. C. Dube, S. Boyet, C. Marescaux, and A. Nehlig Relationship between neuronal loss and interictal glucose metabolism during the chronic phase of the lithium-pilocarpine model of epilepsy in the immature and adult rat Exp. Neurol. 167 2001 227 241
11. B.O. Dubrovsky Steroids, neuroactive steroids and neurosteroids in psychopathology Prog. Neuropsychopharmacol. Biol. Psychiatr. 29 2005 169 192
12. D.A. Eagle, S.J. Boyd, A. Kotak, and F. Allan Calorie restriction of a high-carbohydrate diet elevates the threshold of PTZ-induced seizures to values equal to those seen with a ketogenic diet Epilepsy Res. 54 2003 41 52
13. D.D. Francis, J. Diorio, P.M. Plotsky, and M.J. Meaney Environmental enrichment reverses the effects of maternal separation on stress reactivity J. Neurosci. 22 2002 7840 7843
14. C.G. Hatalski, C. Guirguis, and T.Z. Baram Corticotropin releasing factor mRNA expression in the hypothalamic paraventricular nucleus and the central nucleus of the amygdala is modulated by repeated acute stress in the immature rat J. Neuroendocrinol. 10 1998 663 669
15. S.R. Haut, M. Vouyiouklis, and S. Shinnar Stress and epilepsy: a patient perception survey Epilepsy Behav. 4 2003 511 514
16. E. Hirsch, T.Z. Baram, and O.C. Snead III Ontogenic study of lithium-pilocarpine-induced status epilepticus in rats Brain Res. 583 1992 120 126
17. G.L. Holmes, R. Khazipov, and Y. Ben-Ari Seizure-induced damage in the developing human: relevance of experimental models Prog. Brain Res. 135 2002 321 334
18. G.L. Holmes, M. Sarkisian, Y. Ben-Ari, and N. Chevassus-Au-Louis Mossy fiber sprouting after recurrent seizures during early development in rats J. Comp. Neurol. 404 1999 537 553
19. L.T. Huang, G.L. Holmes, M.C. Lai, P.L. Huang, C.L. Wang, T.J. Wang, C.H. Yang, C.W. Liou, and S.N. Yang Maternal deprivation stress exacerbates cognitive deficits in immature rats with recurrent seizures Epilepsia 43 2002 1141 1148
20. Ser133 phosphorylation Dev. Brain Res. 145 2003 213 218
21. H. Jeltsch, F. Bertrand, C. Lazarus, and J.C. Cassel Cognitive performances and locomotor activity following dentate granule cell damage in rats: role of lesion extent and type of memory tested Neurobiol. Learn Mem. 76 2001 81 105
22. M. Joels Corticosteroid actions in the hippocampus J. Neuroendocrinol. 13 2001 657 669
23. H. Karst, E.R. de Kloet, and M. Joels Episodic corticosterone treatment accelerates kindling epileptogenesis and triggers long-term changes in hippocampal CA1 cells, in the fully kindled state Eur. J. Neurosci. 11 1999 889 898
24. D. Kaufer, W.O. Ogle, Z.S. Pincus, K.L. Clark, A.C. Nicholas, K.M. Dinkel, T.C. Dumas, D. Ferguson, A.L. Lee, M.A. Winters, and R.M. Sapolsky Restructuring the neuronal stress response with anti-glucocorticoid gene delivery Nat. Neurosci. 7 2004 947 953
25. T.W. Kruckeberg, P.K. Gaetano, E.M. Burns, H. Stibler, E. Cerven, and S. Borg Ethanol in preweanling rats with dams: body temperature unaffected Neurobehav. Toxicol. Teratol. 6 1984 307 311
26. H.J. Krugers, S. Maslam, J. Korf, M. Joels, and F. Holsboer The corticosterone synthesis inhibitor metyrapone prevents hypoxia/ischemia-induced loss of synaptic function in the rat hippocampus Stroke 31 2000 1162 1172
27. H. Kubova, P. Mares, L. Suchomelova, G. Brozek, R. Druga, and A. Pitkanen Status epilepticus in immature rats leads to behavioral and cognitive impairment and epileptogenesis Eur. J. Neurosci. 19 2004 3255 3265
28. M.C. Lai, C.W. Liou, S.N. Yang, C.L. Wang, P.L. Hung, C.L. Wu, Y.R. Tung, and L.T. Huang Recurrent bicuculline-induced seizures in rat pups cause long-term motor deficits and increase vulnerability to a subsequent insult Epilepsy Behav. 3 2002 60 66
29. S. Levine Maternal behavior as a mediator of pup adrenocortical function Ann. NY Acad. Sci. 746 1994 260 275
30. I. Lissau, and T.I.A. Sorensen Parental neglect during childhood and increased risk of obesity in young adulthood Lancet 343 1994 324 327
31. D. Liu, J. Diorio, B. Tannenbaum, C. Caldji, D. Francis, A. Freedman, S. Sharma, D. Pearson, P.M. Plotsky, and M.J. Meaney Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress Science 277 1997 1659 1662
32. H. Liu, K. Dashtipour, R. Kinyamu, C.E. Ribak, and L.K. Friedman Suppression of hippocampal neurogenesis is associated with developmental stage, number of perinatal seizure episodes, and glucocorticoid level Exp. Neurol. 184 2003 196 213
33. B.E. Lonze, and D.D. Ginty Function and regulation of CREB family transcription factors in the nervous system Neuron 35 2002 605 623
34. S.J. Lupien, and B.S. McEwen The acute effects of corticosteroids on cognition: integration of animal and human model studies Brain Res. Rev. 24 1997 1 27
35. M. Lynch, U. Sayin, J. Bownds, S. Janumpalli, and T. Sutula Long-term consequences of early postnatal seizures on hippocampal learning and plasticity Eur. J. Neurosci. 12 2000 2252 2264
36. K. Majak, and A. Pitkanen Do seizures cause irreversible cognitive damage? Evidence from animal studies Epilepsy Behav. 5 2004 S35 S44
37. G.W. Mathern, J.K. Pretorius, and T.L. Babb Influence of the type of initial precipitating injury and at what age it occurs on course and outcome in patients with temporal lobe seizures J. Neurosurg. 82 1995 220 227
38. G.W. Mathern, G. Price, C. Rosales, J.K. Pretorius, A. Lozada, and D. Mendoza Anoxia during kainate status epilepticus shortens behavioral convulsions but generates hippocampal neuron loss and supragranular mossy fiber sprouting Epilepsy Res. 30 1998 133 152
39. S.G. Matthews Early programming of the hypothalamo-pituitary-adrenal axis Trend Endocrinol. Metab. 13 2002 373 380
40. C.M. McCormick, P. Kehoe, and S. Kovacs Corticosterone release in response to repeated, short episodes of neonatal isolation: evidence of sensitization Int. J. Dev. Neurosci. 16 1998 175 185
41. B.S. McEwen Effects of adverse experiences for brain structure and function Biol. Psychiatr. 48 2000 721 731
42. M.J. Meaney Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations Annu. Rev. Neurosci. 24 2001 1161 1192
43. M.A. Mikati, G.L. Holmes, A. Chronopoulos, P. Hyde, S. Thurber, A. Gatt, Z. Liu, S. Werner, and C.E. Stafstrom Phenobarbital modifies seizure-related brain injury in the developing brain Ann. Neurol. 36 1994 425 433
44. S.P. Miller, J. Weiss, A. Barnwell, D.M. Ferriero, B. Latal-Hajnal, A. Ferrer-Rogers, N. Newton, J.C. Partridge, D.V. Glidden, D.B. Vigneron, and A.J. Barkovich Seizure-associated brain injury in term newborns with perinatal asphyxia Neurology 58 2002 542 548
45. S. Moriceau, T.L. Roth, T. Okotoghaide, and R.M. Sullivan Corticosterone controls the developmental emergence of fear and amygdala to predator odors in infant rat pups Int. J. Dev. Neurosci. 22 2004 415 422
46. P.J. Mulholland, R.L. Self, B.R. Harris, J.M. Littleton, and M.A. Prendergast (-)-Nicotine ameliorates corticosterone's potentiation of N-methyl-d-aspartate receptor-mediated cornu ammonis 1 toxicity Neuroscience 125 2004 671 682
47. S.M. Nair, T.R. Werkman, J. Craig, R. Finnell, M. Joels, and J.H. Eberwine Corticosteroid regulation of ion channel conductances and mRNA levels in individual hippocampal CA1 neurons J. Neurosci. 18 1998 2685 2696
48. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 1986 Academic Press San Diego
49. P.M. Plotsky, and M.J. Meaney Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats Mol. Brain Res. 18 1993 195 200
50. M.R. Priel, N.F. dos Santos, and E.A. Cavalheiro Developmental aspects of the pilocarpine model of epilepsy Epilepsy Res. 26 1996 115 121
51. R.J. Racine Modification of seizure activity by electrical stimulation. I. After-discharge threshold Electroencephalogr. Clin. Neurophysiol. 32 1972 269 279
52. H. Raff Neonatal dexamethasone therapy: short- and long-term consequences Trend Endocrinol. Metab. 15 2004 351 352
53. M. Roceri, F. Cirulli, C. Pessina, P. Peretto, G. Racagni, and M.A. Riva Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions Biol. Psychiatr. 55 2004 708 714
54. H.J. Romijn, H.A. Hoffman, and A. Gramsbergen At what ages is the developing cortex of the rat comparable to that of the full-term newborn baby? Early Hum. Dev. 26 1991 61 67
55. B. Roozendaal, E.L. Hahn, S.V. Nathan, D.J. de Quervain, and J.L. McGaugh Glucocorticoid effects on memory retrieval require concurrent noradrenergic activity in the hippocampus and basolateral amygdala J. Neurosci. 24 2004 8161 8169
56. B. Roozendaal, and J.L. McGaugh The memory-modulatory effects of glucocorticoids depend on an intact stria terminalis Brain Res. 709 1996 243 250
57. R. Rupprecht, and F. Holsboer Neuroactive steroids: mechanisms of action and neuropsychopharmacological perspectives Trends Neurosci. 22 1999 410 416
58. R. Sankar, D.H. Shin, H. Liu, A. Mazarati, A.P. de Vasconcelos, and C.G. Wasterlain Patterns of status epilepticus-induced neuronal injury during development and long-term consequences J. Neurosci. 18 1998 8382 8393
59. R.M. Sapolsky A mechanism for glucocorticoid toxicity in the hippocampus: increased neuronal vulnerability to metabolic insults J. Neurosci. 5 1985 1228 1232
60. R.M. Sapolsky Glucocorticoid toxicity in the hippocampus: temporal aspects of synergy with kainic acid Neuroendocrinology 43 1986 440 444
61. R.M. Sapolsky, and M.J. Meaney Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period Brain Res. 39 1986 64 76
62. M.R. Sarkisian, P. Tandon, Z. Liu, Y. Yang, A. Hori, G.L. Holmes, and C.E. Stafstrom 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
63. U. Sayin, T.P. Sutula, and C.E. Stafstrom Seizures in the developing brain cause adverse long-term effects on spatial learning and anxiety Epilepsia 45 2004 1539 1548
64. M.S. Scher Neonatal seizures and brain damage Pediatr. Neurol. 29 2003 381 390
65. M.S. Scher, M.Y. Hamid, D.A. Steppe, M.E. Beggarly, and M.J. Painter Ictal and interictal electrographic seizure durations in preterm and term neonates Epilepsia 34 1993 284 288
66. R. Schmid, P. Tandon, C.E. Stafstrom, and G.L. Holmes Effects of neonatal seizures on subsequent seizure-induced brain injury Neurology 53 1999 1754 1761
67. A.J. Silva, J.H. Kogan, P.W. Frankland, and S. Kida CREB and memory Annu. Rev. Neurosci. 21 1998 127 148
68. V.L. Smith-Swintosky, L.C. Pettigrew, R.M. Sapolsky, C. Phares, S.D. Craddock, S.M. Brooke, and M.P. Mattson Metyrapone, an inhibitor of glucocorticoid production, reduces brain injury induced by focal and global ischemia and seizures J. Cereb. Blood Flow Metab. 16 1996 585 598
69. C.E. Stafstrom, A. Chronopoulos, S. Thurber, J.L. Thompson, and G.L. Holmes Age-dependent cognitive and behavioral deficits after kainic acid seizures Epilepsia 34 1993 420 432
70. C.E. Stafstrom Assessing the behavioral and cognitive effects of seizures on the developing brain Prog. Brain Res. 135 2002 377 390
71. B.A. Stein-Behrens, W.J. Lin, and R.M. Sapolsky Physiological elevations of glucocorticoids potentiate glutamate accumulation in the hippocampus J. Neurochem. 63 1994 596 602
72. M. Talmi, E. Carlier, W. Bengelloun, and B. Soumireu-Mourat Synergistic action of corticosterone on kainic acid-induced electrophysiological alterations in the hippocampus Brain Res. 704 1995 97 102
73. T.E. Temple, and G.W. Liddle Inhibitors of adrenal steroid biosynthesis Annu. Rev. Pharmacol. 10 1970 199 218
74. C. Venero, and J. Borrell Rapid glucocorticoid effects on excitatory amino acid levels in the hippocampus: a microdialysis study in freely moving rats Eur. J. Neurosci. 11 1999 2465 2473
75. C.E. Virgin Jr., T.P. Ha, D.R. Packan, G.C. Tombaugh, S.H. Yang, H.C. Horner, and R.M. Sapolsky Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: implications for glucocorticoid neurotoxicity J. Neurochem. 57 1991 1422 1428
76. P.D. Wadhwa, C.A. Sandman, and T.J. Garite The neurobiology of stress in human pregnancy: implications for prematurity and development of the fetal central nervous system Prog. Brain Res. 133 2001 131 142
77. I.C. Weaver, N. Cervoni, F.A. Champagne, A.C. D'Alessio, S. Sharma, J.R. Seckl, S. Dymov, M. Szyf, and M.J. Meaney Epigenetic programming by maternal behavior Nat. Neurosci. 7 2004 847 854
78. C.L. Wu, L.T. Huang, C.W. Liou, T.J. Wang, Y.R. Tung, H.Y. Hsu, and M.C. Lai Lithium-pilocarpine-induced status epilepticus in immature rats result in long-term deficits in spatial learning and hippocampal cell loss Neurosci. Lett. 312 2001 113 117
79. T.F. Yeh, Y.J. Lin, H.C. Lin, C.C. Huang, W.S. Hsieh, C.H. Lin, and C.H. Tsai Outcomes at school age after postnatal dexamethasone therapy for lung disease of prematurity N. Engl. J. Med. 350 2004 1304 1313
80. T. Yoshihara, Y. Otsuki, A. Yamazaki, S. Honma, Y. Yamasaki, and K. Honma Maternal deprivation in neonatal rats alters the expression of circadian system under light-dark cycles and restricted daily feeding in adulthood Physiol. Behav. 85 2005 646 654
81. G. Zhang, Y.S. Raol, F.C. Hsu, and A.R. Brooks-Kayal Long-term alterations in glutamate receptor and transporter expression following early life seizures are associated with increased seizure susceptibility J. Neurochem. 88 2004 91 101