Seizure-induced damage in the developing human: Relevance of experimental models

Progress in Brain Research

Volumn 135, Issue , 2002, Pages 321-334

  Holmes, Gregory L ^a   Khazipov, Rustem ^b   Ben Ari, Yehezkiel ^b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b Turing Center for Living Systems CENTURI Aix Marseille University   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; N METHYL DEXTRO ASPARTIC ACID;

ANIMAL MODEL; COGNITIVE DEFECT; CONFERENCE PAPER; CONTROLLED STUDY; EPILEPSY; EPILEPTIC STATE; EXPERIMENTAL MODEL; HUMAN; INFANTILE SPASM; LEARNING; LENNOX GASTAUT SYNDROME; LONG TERM POTENTIATION; MAZE TEST; MEMORY; MYOCLONUS EPILEPSY; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; ONSET AGE; PRIORITY JOURNAL; RAT; SEIZURE;

EID: 0036456772     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(02)35030-1     Document Type: Conference Paper

References (127)

1. Aicardi, J. and Chevrie, J.J. (1970) Convulsive status epilepticus in infants and children. Epilepsia, 11: 187-197.
2. Albala, B.J., Moshé, S.L. and Okada, R. (1984) Kainic-acid-induced seizures: A developmental study. Dev. Brain Res., 13: 139-148.
3. Altman, J. and Das, G.D. (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol., 124: 319-336.
4. Angevine Jr., J.B. (Jr., 1965) Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp. Neurol., Suppl. 2: 1-70.
5. Bailet, L.L. and Turk, W.R. (2000) The impact of childhood epilepsy on neurocognitive and behavioral performance: A prospective longitudinal study. Epilepsia, 41: 426-431.
6. 3H-thymidine autoradiography. J. Comp. Neurol., 190: 87-114.
7. Ben-Ari, Y. (1985) Limbic seizure and brain damage produced by kainic acid: Mechanisms and relevance to human temporal lobe epilepsy. Neuroscience, 14: 375-403.
8. Ben-Ari, Y. (1987) Brain damage cause by seizure activity. Electroencephalogr. Clin. Neurophysiol., 39(Suppl.): 209-211.
9. Ben-Ari, Y. and Gho, M. (1988) Long-lasting modification of the synaptic properties of rat CA3 hippocampal neurones induced by kainic acid. J. Physiol., 404: 365-384.
10. Ben-Ari, Y, Lagowska, Y. and Le Gall La Salle, G. et al. (1978) Diazepam pretreatment reduces distant hippocampal damage induced by intra-amygdaloid injections of kainic acid. Eur. J. Pharmacol., 52: 419-420.
11. Ben-Ari, Y., Tremblay, E. and Ottersen, O.P. (1980a) Injections of kainic acid into the amygdaloid complex of the rat: An electrographic, clinical and histological study in relation to the pathology of epilepsy. Neuroscience, 5: 515-528.
12. Ben-Ari, Y., Tremblay, E. and Ottersen, O.P. et al. (1980b) The role of epileptic activity in hippocampal and 'remote' cerebral lesions induced by kainic acid. Brain Res., 191: 79-97.
13. Bengzon, J., Kokaia, Z. and Elmér, E. et al. (1997) Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc. Natl. Acad. Sci. USA, 94: 10432-10437.
14. Berger, M.L., Tremblay, E. and Nitecka, L. et al. (1984) Maturation of kainic acid seizure-brain damage syndrome in the rat. III. Postnatal development of kainic acid binding sites in the limbic system. Neuroscience, 13: 1095-1104.
15. Bergman, I., Painter, M.I. and Hirsch, R.P. et al. (1983) Outcome of neonates with convulsions treated in an intensive care unit. Ann. Neurol., 14: 642-647.
16. Bickler, P.E., Gallego, S.M. and Hansen, B.M. (1993) Developmental changes in intracellular calcium regulation in rat cerebral cortex during hypoxia. J. Cereb. Blood Flow Metab., 13: 811-819.
17. Bourgeois, B.F.D., Prensky, A.L. and Palkes, H.S, et al. (1983) Intelligence in epilepsy: A prospective study in children. Ann. Neurol., 14: 438-444.
18. Bulteau, C., Jambaque, I. and Viguier, D. et al. (2000) Epileptic syndromes, cognitive assessment and school placement: A study of 251 children. Dev. Med. Child Neural., 42: 319-327.
19. Cameron, H.A. and Gould, E. (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience, 61: 203-209.
20. Cameron, H.A. and Gould, E. (1996) Distinct populations of cells in the adult dentate gyrus undergo mitosis or apoptosis in response to adrenalectomy. J. Comp. Neurol., 369: 56-63.
21. Cameron, H.A., McEwen, B.S. and Gould, E. (1995) Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J. Neurosci., 15: 4687-4692.
22. Cameron, H.A., Hazel, T.G. and McKay, R.D.G. (1998) Regulation of neurogenesis by growth factors and neurotransmitters. J. Neurobiol., 36: 287-306.
23. Cavazos, J.E., Golarai, G. and Sutula, T.P. (1991) Mossy fiber synaptic reorganization induced by kindling: Time course of development, progression, and permanence. J. Neurosci., 11: 2795-2803.
24. Cherubini, E., Ben-Ari, Y. and Krnjevic, K. (1989) Anoxia produces smaller changes in synaptic transmission, membrane potential and input resistance in immature rat hippocampus. J. Neurophysiol., 62: 882-895.
25. Cilio, M.R., Sogawa, Y., Huang, L.-T., Silveira, D.C., McCabe, B.K. and Holmes, G.L. (1999) Status epilepticus in the developing brain: Age-dependent neuronal injury, mossy fiber sprouting, seizure susceptibility, and cognitive impairment. Epilepsia, 40(Suppl. 7): 34.
26. Cossart, R., Dinocourt, C. and Hirsch, J.C. et al. (2001) Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat. Neurosci., 4: 52-62.
27. Cronin, J. and Dudek, F.E. (1988) Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res., 474: 181-184.
28. Cronin, J., Obenaus, A. and Houser, C.R. et al. (1992) Electrophysiology of dentate granule cells after kainate-induced synaptic reorganization of mossy fibers. Brain Res., 573: 305- 310.
29. Crusio, W.E., Schwegler, H. and Lipp, H.-P. (1987) Radial-maze performance and structural variation of the hippocampus in mice: A correlation with mossy fiber distribution. Brain Res., 425:182-185.
30. De Keyser, J., Sulter, G. and Luiten, P.G. (1999) Clinical trials with neuroprotective drugs in acute ischaemic stroke: Are we doing the right thing?. Trends Neurosci., 22: 535-540.
31. De Rogalski Landrot, I., Minokoshi, M. and Silveira, D.C. et al. (2001) Recurrent neonatal seizures: Relationship of pathology to the electroencephalogram and cognition. Dev. Brain Res., 129: 27-38.
32. DeBassio, W.A., Kemper, T.L. and Tonkiss, J. et al. (1996) Effect of prenatal protein deprivation on postnatal granule cell generation in the hippocampal dentate gyrus. Brain Res. Bull., 41: 379-383.
33. DeLorenzo, R,J., Hauser, W.A. and Towne, A.R. et al. (1996) A prospective, population-based epidemiologic study of status epilepticus in Richmond, Virginia. Neurology, 46: 1029-1035.
34. Eriksson, K.J. and Koivikko, M.J. (1997) Status epilepticus in children: Aetiology, treatment, and outcome. Dev. Med. Child Neurol., 39: 652-658.
35. Esclapez, M., Hirsch, J. and Ben-Ari, Y. et al. (1999) Newly formed excitatory pathways provide a substrate for hyperexcitablity in experimental temporal lobe epilepsy, J. Comp. Neurol., 408: 449-460.
36. Farwell, J.R., Dodrill, C.B. and Batzel, L.W. (1985) Neuropsychological abilities of children with epilepsy. Epilepsia, 26: 395-400.
37. Funakoshi, A., Morikawa, T. and Muramatsu, R. et al. (1988) A prospective WISC-R study in children with epilepsy. Jap. J. Psychiatry Neurol., 42(3): 562-564.
38. Gould, E. and Tanapat, P. (2000) Stress and hippocampal neurogenesis. Biol. Psychiatry, 46: 1472-1479.
39. Gould, E., Tanapat, P. and McEwen, B.S. et al. (1998) Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl. Acad. Sci. USA, 95: 3168-3171.
40. Gould, E., Beylin, A. and Tanapat, P. et al. (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci., 2: 260-265.
41. Gray, W.P. and Sundstrom, L.E. (1998) Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat. Brain Res., 790: 52-59.
42. Hauser, W.A. and Hersdorffer, D.C. (1990) Epilepsy: Frequency, Causes and Consequences. Demos, New York.
43. Hirsch, E., Baram, T.Z. and Snead III, O.C. (1992) Ontogenic study of lithium-pilocarpine-induced status epilepticus in rats. Brain Res., 583: 120-126.
44. Holmes, G.L. (1997) Epilepsy in the developing brain: Lessons from the laboratory and clinic. Epilepsia, 38: 12-30.
45. Holmes, G.L. and Ben-Ari, Y. (1998) Seizures in the developing brain: Perhaps not so benign after all. Neuron, 21: 1231-1234.
46. Holmes, G.L., Gaiarsa, J.-L. and Chevassus-Au-Louis, N. et al, (1998a) Consequences of neonatal seizures in the rat: Morphological and behavioral effects. Ann. Neurol., 44: 845-857.
47. Holmes, M.D., Dodrill, C.B. and Wilkus, R.J. et al. (1998b) Is partial epilepsy progressive? Ten-year follow-up of EEG and neuropsychological changes in adults with partial seizures. Epilepsia, 39: 1189-1193.
48. Holmes, G.L., Thompson, J.L. and Marchi, T. et al. (1988c) Behavioral effects of kainic acid administration on the immature brain. Epilepsia, 29: 721-730.
49. Holmes, G.L., Sarkisian, M. and Ben-Ari, Y. et al. (1999) Mossy fiber sprouting following recurrent seizures during early development in rats. J. Comp. Neurol., 404: 537-553.
50. Huang, L.-T., Cilio, M.R. and Silveira, D.C. et al. (1999) Long- term effects of neonatal seizures: A behavioral, electrophysiological, and histological study. Dev. Brain Res., 118: 99-107.
51. Huttenlocher, P.R. and Hapke, R.J. (1990) A follow-up study of intractable seizures in childhood. Ann. Neurol., 28: 699-705.
52. Jokeit, H. and Ebner, A. (1999) Long term effects of refractory temporal lobe epilepsy on cognitive abilities: A cross sectional study. J. Neurol. Neurosurg. Psychiatry, 67: 44-50.
53. Kelsey, J.E., Sanderson, K.L. and Frye, C.A. (2000) Perforant path stimulation in rats produces seizures, loss of hippocampal neurons, and a deficit in spatial mapping which are reduced by prior MK-801. Behav. Brain Res., 107: 59-69.
54. Khazipov, R., Esclapez, M., Caillard, O., Bernard, C., Hirsch, E., Leinekugel, X., Berger, B. and Ben-Ari, Y. (1999) Early maturation of hippocampal network in the fetal cynomolgus monkey. Soc. Neurosci. Abstr., 25: 2266.
55. Ko, T.-S. and Holmes, G.L. (1999) EEG and clinical predictors of medically intractable childhood epilepsy. Clin. Neurophysiol., 110: 1245-1251.
56. Koh, S., Storey, T.W. and Santos, T.C. et al. (1999) Early-life seizures in rats increase susceptibility to seizure-induced brain injury in adulthood. Neurology, 53: 915-921.
57. Kubová, H., Druga, R. and Lukasiuk, K. et al. (2001) Status epilepticus causes necrotic damage in the mediodorsal nucleus of the thalamus in immature rats. J. Neurosci., 21: 3593-3599.
58. Kwong, K.L., Lee, S.L. and Yung, A. et al. (1995) Status epilepticus in 37 Chinese children: Aetiology and outcome. J. Paediatr: Child Health, 31: 395-398.
59. Lamsa, K., Palva, J.M. and Ruusuvuori, E. et al. (2000) Synaptic GABA(A) activation inhibits AMPA kainate receptor mediated bursting in the newborn (POP2) rat hippocampus. J. Neurophysiol., 83: 359-366.
60. Lipp, H.-P., Schwegler, H. and Driscoll, P. (1984) Postnatal modification of hippocampal circuitry alters avoidance learning in adult rats. Science, 225: 80-82.
61. Lipp, H.-P., Schwegler, H. and Heimrich, B. et al. (1988) Infrapyramidal mossy fibers and two-way avoidance learning: Developmental modification of hippocampal circuitry and adult behavior of rats and mice. J. Neurosci., 8: 1905-1921.
62. Lipton, S.A. and Rosenberg, P.A. (1994) Excitatory amino acids as a final common pathway for neurologic disorders. New Engl. J. Med., 330: 613-622.
63. Liu, J., Solway, K. and Messing, R.O. et al. (1998) Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J. Neurosci., 18: 7768-7778.
64. Liu, Z., Gatt, A. and Mikati, M. et al. (1995) Long-term behavioral deficits following pilocarpine seizures in immature rats. Epilepsy Res., 19: 191-204.
65. Liu, Z., Stafstrom, C.E. and Sarkisian, M. et al. (1996) Agedependent effects of glutamate toxicity in the hippocampus. Dev. Brain Res., 97: 178-184.
66. Liu, Z., Yang, Y. and Silveira, D.C. et al. (1999) Consequences of recurrent seizures during early brain development. Neuroscience, 92: 1443-1454.
67. Marks, J.D., Friedman, J.E. and Haddad, G.G. (1996) Vulnerability of CA1 neurons to glutamate is developmentally regulated. Dev. Brain Res., 97: 194-206.
68. Mathern, G.W., Leite, J.P. and Pretorius, J.K. et al. (1994) Children with severe epilepsy: Evidence of hippocampal neuron losses and aberrant mossy fiber sprouting during postnatal granule cell migration and differentiation. Dev. Brain Res., 78: 70-80.
69. Maytal, J. and Shinnar, S. (1995) Status epilepticus in children. In: S. Shinnar, N. Amir and D. Branski (Eds.), Childhood Seizures. Karger, Basel, pp. 111- 122.
70. Maytal, J., Shinnar, S. and Moshé, S.L. et al. (1989) Low morbidity and mortality of status epilepticus in children. Pediatrics, 83(3): 323-331.
71. McCabe, B.K., Silveira, D.C. and Cilio, M.R. et al. (2001) Neonatal seizures result in a decrease in neurogenesis in the dentate. J. Neurosci., 21: 2094-2103.
72. McNamara, R.K. and Routtenberg, A. (1995) NMDA receptor blockade prevents kainate induction of protein FI/GAP-43 mRNA in hippocampal granule cells and subsequent mossy fiber sprouting in the rat. Mol. Brain Res., 33: 22-28.
73. Mehler, M.F. and Kessler, J.A. (1999) Progenitor cell biology. Implications for neural regeneration. Arch. Neurol., 56: 780- 784.
74. Meldrum, B.S. and Brierley, J.B. (1973) Prolonged epileptic seizures in primates: Ischaemic cell change and its relation to ictal physiological events. Arch. Neurol., 28: 10-17.
75. Meldrum, B.S., Vigouroux, R.A. and Brierley, J.B. (1973) Systemic factors and epileptic brain damage. Prolonged seizures in paralyzed artificially ventilated baboons. Arch. Neurol., 29: 82-87.
76. Montaron, M.F., Petry, K.G. and Rodriguez, J.J. et al. (1999) Adrenalectomy increases neurogenesis but not PSA-NCAM expression in aged dentate gyrus. Eur. J. Neurosci., 11: 1479-1485.
77. Morris, R.G.M., Garrud, P. and Rawlins, J.N.P. et al. (1982) Place navigation impaired in rats with hippocampal lesions. Nature, 297: 681-683.
78. Morris, R.G.M., Anderson, E. and Lynch, G.S. et al. (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature, 319: 774-776.
79. Moshé, S.L. and Albala, B.J. (1982) Kindling in developing rats: Persistence of seizures into adulthood. Dev. Brain Res., 4: 67-71.
80. Nadler, J.V. (1981) Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci., 29: 2031-2042.
81. Nadler, J.V., Perry, B.W. and Cotman, C.W. (1978) Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature, 271: 676-677.
82. Neill, J., Liu, Z. and Sarkisian, M. et al. (1996) Recurrent seizures in immature rats: Effect on auditory and visual discrimination. Dev. Brain Res., 95: 283-292.
83. Neyens, L.G., Aldenkamp, A.P. and Meinardi, H.M. (1999) Prospective follow-up of intellectual development in children with a recent onset of epilepsy. Epilepsy Res., 34: 85-90.
84. Nitecka, L., Tremblay, E. and Charton, G. et al. (1984) Maturation of kainic acid seizure-brain damage syndrome in the rat. II. Histopathological sequelae. Neuroscience, 13: 1073-1094.
85. Olney, J.W., Fuller, T. and De Gubareff, T. (1979) Acute dendrotoxic changes in the hippocampus of kainate treated rats. Brain Res., 176: 91-100.
86. Painter, M.J., Bergman, I. and Crumrine, R (1986) Neonatal seizures. Pediatr. Clin. North Am., 33: 91-109.
87. Parent, J.M., Yu, T.W. and Leibowitz, R.T. et al. (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network plasticity in the adult hippocampus. J. Neurosci., 17: 3727-3738.
88. Parent, J.M., Janumpalli, S. and McNamara, J.O. et al. (1998) Increased dentate granule cell neurogenesis following amygdala kindling in the adult rat. Neurosci. Lett., 247: 9-12.
89. Pellock, J.M. (1993) Status epilepticus. In: W.E. Dodson and J.M. Pellock (Erisa), Pediatric Epilepsy: Diagnosis and Therapy. Demos, New York, pp. 197-206.
90. Represa, A., and Ben-Ari, Y. (1997) Molecular and cellular cascades in seizure-induced neosynapse formation. Adv. Neurol., 72: 25-34.
91. Represa, A., Tremblay, E. and Ben-Ari, Y. (1987) Kainate binding sites in the hippocampal mossy fibers: Localization and plasticity. Neuroscience, 20: 739-748.
92. Rice, A.C., Floyd, C.L. and Lyeth, B.G. et al. (1998) Status epilepticus causes long-term NMDA receptor-dependent behavioral changes and cognitive deficits. Epilepsia, 39: 1148-1157.
93. Rodin, E.A., Schmaltz, S. and Twitty, G. (1986) Intellectual functions of patients with childhood-onset epilepsy. Dev. Med Child Neurol., 28: 25-33.
94. Sankar, R., Shin, D.H. and Liu, H. et al. (1998) Patterns of status epilepticus-induced neuronal injury during development and long-term consequences. J. Neurosci., 18: 8382-8393.
95. Scher, M.S., Aso, K. and Beggarly, M.E. et al. (1993) Electrographic seizures in preterm and full term neonates: Clinical correlates, associated brain lesions and risk for neurological sequelae. Pediatrics, 91: 128-134.
96. Schmid, R., Tandon, P. and Stafstrom, C.E. et al. (1999) Effects of neonatal seizures on subsequent seizure-induced brain injury. Neurology, 53: 1754-1761.
97. Scott, B.W., Wang, S. and Burnham, W.M. et al. (1998) Kindling-induced neurogenesis in the dentate gyrus of the rat. Neurosci. Lett., 248: 73-76.
98. Shinnar, S., Pellock, J.M. and Moshé, S. et al. (1997) In whom does status epilepticus occur: Age-related differences in children. Epilepsia, 38: 907-914.
99. Shinnar, S., Pellock, J.M. and Berg, A.T. et al. (2001) Short-term outcomes of children with febrile status epilepticus. Epilepsia, 42: 47-53.
100. Sillanpaa, M., Jalava, M. and Kaleva, O. et al. (1998) Long-term prognosis of seizures with onset in childhood. New Engl. J. Med., 338: 1916-1918.
101. Sloviter, R.S. (1983) 'Epileptic' brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain Res. Bull., 10: 675-697.
102. Sloviter, R.S. and Damiano, B.P. (1981) Sustained electrical stimulation of the perforant path duplicates kainate-induced electrophysiological effects and hippocampal damage in rats. Neurosci. Lett., 24: 279-284.
103. Sperber, E.F., Haas, K.Z. and Stanton, P.K. et al. (1991) Resistance of the immature hippocampus to seizure-induced synaptic reorganization. Dev. Brain Res., 60: 88-93.
104. Stafstrom, C.E., Thompson, J.L. and Holmes, G.L. (1992) Kainic acid seizures in the developing brain: Status epilepticus and spontaneous recurrent seizures. Dev. Brain Res., 65: 227-236.
105. Stafstrom, C.E., Chronopoulos, A. and Thurber, S. et al. (1993) Age-dependent cognitive and behavioral deficits following kainic acid-induced seizures. Epilepsia, 34: 420-432.
106. Sutula, T, Koch, J. and Golarai, G. et al. (1996) NMDA receptor dependence of kindling and mossy fiber sprouting: Evidence that the NMDA receptor regulates patterning of hippocampal circuits in the adult brain. J. Neurosci., 16: 7398-7406.
107. Tanapat, P., Galea, L.A. and Gould, E. (1998) Stress inhibits the proliferation of granule cell precursors in the developing dentate gyrus. Int. J. Dev. Neurosci., 16: 235-239.
108. Tanapat, P., Hastings, N.B. and Gould, E. (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci., 19: 5792-5801.
109. Tassinari, C.A., Rubboli, G. and Volpi, L. et al. (2000) Encephalopathy with electrical status epilepticus during slow sleep or ESES syndrome including the acquired aphasia. Clin. Neurophysiol., 111(Suppl. 2): S94-S102.
110. Tauck, D. and Nadler, J.V. (1985) Evidence of functional mossy fiber sprouting in the hippocampal formation of kainic acid-treated rats. J. Neurosci., 5: 1016-1022.
111. Tremblay, E., Nitecka, L. and Berger, M.L. et al. (1984) Maturation of kainic acid seizure-brain damage syndrome in the rat. I. Clinical, electrographic and metabolic observations. Neuroscience, 13(4): 1051-1072.
112. Van Esch, A., Ramlal, I.R. and van Steensel-Moll, H.A. et al. (1996) Outcome after febrile status epilepticus. Dev. Med. Child Neurol., 38: 19-24.
113. Van Praag, H., Christie, B.R. and Sejnowski, T.J. et al. (1999a) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. USA, 96: 13427-13431.
114. Van Praag, H., Kempermann, G. and Gage, EH. (1999b) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci., 2: 266-270.
115. Vasconcellos, E., Wyllie, E. and Sullivan, S. et al. (2001) Mental retardation in pediatric candidates for epilepsy surgery: The role of early seizure onset. Epilepsia, 42: 268-274.
116. Villeneuve, N., Ben-Ari, Y. and Holmes, G.L. et al. (2000) Neonatal seizures induced persistent changes in intrinsic properties of CA1 rat hippocampal cells. Ann. Neurol., 47: 729-738.
117. Wagner, J.P., Black, I.B. and DiCicco-Bloom, E. (1999) Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth hormone. J. Neurosci., 19: 6006-6016.
118. Wakamoto, H., Nagao, H. and Hayashi, M. et al. (2000) Long-term medical, educational, and social prognoses of childhood-onset epilepsy: A population-based study in a rural district of Japan. Brain Dev., 22: 246-255.
119. Wasterlain, C.G. (1976) Effects of neonatal status epilepticus on rat brain development. Neurology, 26: 975-986.
120. Wasterlain, C.G. (1978) Neonatal seizures and brain growth. Neuropaediatrie, 9: 213-228.
121. Wasterlain, C.G. (1997) Recurrent seizures in the developing brain are harmful. Epilepsia, 38: 728-734.
122. Wasterlain, C.G. and Plum, F. (1973) Vulnerability of developing rat brain to electroconvulsive seizures. Arch. Neurol., 29: 38- 45.
123. Williams, J., Griebel, M.L. and Dykman, R.A. (1998) Neuropsychological patterns in pediatric epilepsy. Seizure, 7: 223-228.
124. Wolf, H.K., Buslei, R. and Schmidt-Kastner, R. et al. (1996) NeuN: A useful neuronal marker for diagnostic histopathology. J. Histochem. Cytochem., 44: 1167-1171.
125. Yang, Y., Tandon, P. and Liu, Z. et al. (1998) Synaptic reorganization following kainic acid-induced seizures during development. Dev. Brain Res., 107: 169-177.
126. Young, D., Lawlor, P.A. and Leone, P. et al. (1999) Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nat. Med., 4: 448-453.
127. Zupanc, M.L. (2001) Infantile spasms. Curr. Treat. Opt. Neurol., 3: 289-300.