Epilepsy in the developing brain: Lessons from the laboratory and clinic

Epilepsia

Volumn 38, Issue 1, 1997, Pages 12-30

  Holmes, Gregory L ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b Hôpital de Port Royal ^*  (France)

Author keywords

Developing brain; Electroencephalography; Epilepsy; Epileptogenesis; Pathophysiology

Indexed keywords

BRAIN MATURATION; CHILDHOOD DISEASE; EPILEPSY; EPILEPTIC FOCUS; EPILEPTOGENESIS; HUMAN; ONSET AGE; PRIORITY JOURNAL; REVIEW;

ADULT; AGE FACTORS; ANIMALS; ANTICONVULSANTS; BRAIN; CEREBRAL CORTEX; CHILD; ELECTROENCEPHALOGRAPHY; EPILEPSY; HIPPOCAMPUS; HUMANS; INFANT, NEWBORN; RATS;

EID: 0031037650     PISSN: 00139580     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1528-1157.1997.tb01074.x     Document Type: Review

References (250)

1. Hauser WA, Hersdorffer DC. Epilepsy: frequency, causes and consequences. New York: Demos, 1990.
2. Schwartzkroin PA, Moshé SL, Noebels JL, Swann JW. Brain development and epilepsy. New York: Oxford University Press, 1995.
3. Chronister RB, WhiteLEJr. Fiberarchitectureofthehippocampal formation: anatomy, projections, and structural significance. In: Isaacson RL, Pribram KH, eds. The hippocampus, vol. 1. New York: Plenum Press, 1975:9-45.
4. Witter MP. Connectivity of the rat hippocampus. In: Chan-Palay V, Köhler C, eds. Neurology and neurobiology. Volume 52, The hippocampus-new vistas. New York: Alan R. Liss, 1989:53-69.
5. Gulyàs AI, Hajos N, Freund TF. Intemeurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci 1996;! 6:3397-411.
6. Ottersen OP, Storm-Mathisen J. Excitatory and inhibitory amino acids in the hippocampus. In: Chan-Palay V, Köhler C, eds. Neurology and neurobiology. Volume 52. The hippocampus-new vistas. New York: Alan R. Liss, 1989:97-117.
7. Nadler JV, White WF, Vaca KW, Perry BW, Cotman CW. Biochemical correlates of transmission mediated by glutamate and aspartate. J Neurochem 1978:31:147-55.
8. Sloviter RS, Nilaver G. Immunocytochemical localization of GABA-, cholecytokinin-, vasoactive intestinal polypeptide-, and somatostatin-like immunoreactivity in the area dentata and hippocampus of the rat. J Comp Neural 1987;256:42-60.
9. Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neural 1965; 124:319-36.
10. Bayer SA. Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. / Comp Neural 1980; 190:87-114.
11. Amaral DG, Dent JA. Development of the mossy fibers of the dentate gyms: I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neural 1981;195:5186.
12. Ribak CE, Navetta MS. An immature mossy fiber innervation of hilar neurons may explain their resistance to kainate-induced cell death in 15-day-old rats. Dev Brain Res 1994;79:47-62.
13. Muller D, Oliver M, Lynch G. Developmental changes in synaptic properties in hippocampus of neonatal rats. Dev Brain Res 1989;49:105-14.
14. Stringer JL, Lothman EW. Ontogeny of hippocampal afterdischarges in the urethane-anesthetized rat. Dev Drain Res 1992;70: 223-9.
15. Walsh CA. Neuronal identity, neuronal migration, and epileptic disorders of the cerebral cortex. In: Schwartzkroin PA, Moshé SL, Noebels JL, Swarm J\V, eds. Brain development and epilepsy. New York: Oxford University Press, 1995:122-43.
16. Allendoerfer KL, Schatz CJ. The subplate, a transient neocortical structure: its role in development of connections between thalamus and cortex. Annu Rev Neurosci 1994;17:185-218.
17. McDonald J\V, Johnston MV. Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res Rev 1990; 15:41-70.
18. McDonald JW, Silverstein FS, Cardona D, Hudson C, Chen R, Johnston MV. Systemic administration of MK-801 protects against W-methyl-D-aspartate- and quisqualate-mediated neurotoxicity in perinatal rats. Neuroscience 1990;36:589-99.
19. Schoepfer R, Monyer H, Sommer B, et al. Molecular biology of glutamate receptors. Prog Neurobio! 1994;42:353-7.
20. Monaghan DT, Bridges RJ, Cotman CW. The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu Rev Pharmacol Toxicol I989;29:365-402.
21. Tanabe Y, Masu M, Ishii T, Shigemoto R, Nakanishi S. A family of metabotropic glutamate receptors. Neuron 1992;8:169-79.
22. Sugiyama H, Ito I, Watanabe M. Glutamate receptor subtypes may be classified into two major categories: a study on Xenopus oocytes injected with rat brain mRNA. Neuron 1989;3:129-32.
23. Hollmann M, Hartley M, Heinemann S. Ça2permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 1991;252:851-3.
24. Verdoom TA, Burnashev N, Monyer H, Seeburg PH, Sakmann B. Structural determinants of ion flow through recombinant glutamate receptor channels. Science 1991;252:1715-8.
25. Lipton SA. Prospects for clinically tolerated NMDA antagonists: open-channel blockers and alternative redox states of nitric oxide. Trends Neurosci 1993;16:527-32.
26. Lipton SA, Singet DJ, Stamler JS. Nitric oxide in the central nervous system. Prog Brain Res 1994; 103:359-64.
27. Sugiyama H, Ito I, Hirono C. A new type of glutamate receptor linked to inositol phospholipid metabolism. Nature 1987;325: 531-3.
28. Schoepp DD, Bockaert J, Sladeczek F. Pharmacological and functional characteristics of metabotropic excitatory amino acid receptors. Trends Pharmacol Sei 1990; 11:508-15.
29. Nakanishi S. Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity. Neuron 1994;13:1033-7.
30. Crépel V, Aniksztejn L, Ben-Ari Y, Hammond C. Glutamate metabotropic receptors increase a Ca2-activated nonspecific cationic current in CA1 hippocampal neurons. / Neurophysiol 1994; 72:1561-9.
31. Batchelor AM, Madge DJ, Garthwaite J. Synaptic activation of metabotropic glutamate receptors in the parallel fibre-Purkinje cell pathway in rat cerebellar slices. Neuroscience 1994;63: 911-5.
32. Glaum SR, Miller RJ. Metabotropic glutamate receptors mediate excitatory transmission in the nucleus of the solitary tract. / Neurosci 1992;12:2251-8.
33. Bode-Greuel KM, Singer W. The development of A'-methyl-Daspartate receptors in cat visual cortex. Dev Brain Res 1989;46: 197-204.
34. Kleinschmidt A, Bear MF, Singer W. Blockade of "NMDA" receptors disrupts experience-department plasticity of kitten striate cortex. Science 1987:238:355-8.
35. Cherubini E, Gaiarsa JL, Ben-Ari Y. GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 1991;14:515-9.
36. Durand GM, Kovalchuk Y, Konnerth A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 1996:381:71-5.
37. Pokorny J, Yamamato T. Postnatal ontogenesis of the hippocampal CA1 area in rats. II. Development of ultrastructure in stratum lacunosum and moleculare. Brain Res Bull 1981;7:121-30.
38. Richter K, Wolf G. High-affinity glutamate uptake of rat hippocampus during postnatal development: a quantitative autoradiographie study. Neuroscience 1990;34:49-55.
39. Miller LP, Johnson AE, Gelhard RE, Insel TR. The ontogeny of excitatory amino acid receptors in the rat forebrain-II. Kainic acid receptors. Neuroscience 1990;35:45-51.
40. Insel TR, Miller LP, Gelhard RE. The ontogeny of excitatory amino acid receptors in rat forebrain. I. /V-Methyl-D-aspartate and quisqualate receptors. Neuroscience 1990;35:31-43.
41. Tremblay E, Roisin MP, Represa A, Charriaut-Marlangue C, Ben-Ari Y. Transient increased density of NMDA binding sites in the developing rat hippocampus. Brain Res 1988;461:393-6.
42. Ben-Ari Y, Cherubini E, Kmjevic K. Changes in voltage dependence of NMDA currents during development. Neurosci Lett 1988:94:88-92.
43. Morrisett RA, Mott DD, Lewis DV, Wilson WA. Swartzwelder HS. Reduced sensitivity of the Ar-methyl-D-aspartate component of synaptic transmission to magnesium in hippocampal slices from immature rats. Dev Brain Res 1990:56:257-62.
44. Carmignoto G, Vicini S. Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 1992:258:1007-11.
45. Bowe MA, Nadler JV. Developmental increase in the sensitivity to magnesium of NMDA receptors on CA1 hippocampal pyramidal cells. Dev Brain Res 1990;56:55-61.
46. Bashir ZI, Boitolotto ZA, Davies CH, et al. Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature 1993:363:347-50.
47. Bortolotto ZA, Bashir ZI, Davies CM, Collingridge GL. A molecular switch activated by metabotropic glutamate receptors regulates induction of long-term potentiation. Nature 1994:368: 740-3.
48. Bliss TV, Collingridge GL. A synaptic model of memory: longterm potentiation in the hippocampus. Nature 1993:362:31-9.
49. Pollard H, Khrestchatisky M, Moreau J, Ben-Ari Y. Transient expression of the NR2C subunit of the NMDA receptor in developing rat brain. NeuroReport 1993;4:411-4.
50. Monyer H, Burnashev N, Laurie DJ, Sakman B, Seeburg PH. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 1994; 12: 520-40.
51. Hestrin S. Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature 1992:357: 686-9.
52. Burgard EC, Hablitz JJ. Developmental change in NMDA and non-NMDA receptor-mediated synaptic potentials in rat neocortex. J Neurophysiol 1993;69:230-9.
53. Nevvberry NR, Nicoll RA. Comparison of the action of baclofen with -y-aminobutyric acid on rat hippocampal pyramidal cells in vitro. J Physio! 1985:350:161-85.
54. Sivilotti L, Nistri A. GABA receptor mechanism in the central nervous system. Prog Neurobiol 1991:36:35-92.
55. Alger BE, Nicoll RA. Pharmacological evidence for two kinds of GABA receptor on rat hippocampal pyramidal cells studied m vitro. J Pliysiol 1982:328:125-41.
56. Alger BE, Nicoll RA. Feed-forward dendritic inhibition in rat hippocampal pyramidal cells studied in vitro. J Pliysiol 1982;328: 105-23.
57. Anrade R, Malenka RC, Nicoll RA. A G protein couples serotonin and GABAB receptors to the same channels in hippocampus. Science 1986;234:1261-5.
58. Dutar P. Nicoll RA. Pre- and postsynaptic GABAB receptors in the hippocampus have different pharmacological properties. Neuron 1988; 1:585-91.
59. Bowery NG, Hill DR, Hudson AL, et al. (-)BacIofen decreases neurotransmitter release in the mammalian CNS by an action at a i novel GABA receptor. Nature 1980;283:92-4. ';
60. Howe JF, Sutor B, Zieglgänsberger W. Baclofen reduces postsynaptic potentials of rat conical neurons by an action other than its hyperpolarizing action. J Physiol 1987;384:539-69. ?
61. Lubbers K, Wolff JR, Frotscher M. Neurogcnesis of GABAergic ! neurons in the rat dentate gyrus: a combined autoradiographic and immunocytochemical study. Neurosci Lett 1985;62:317-22.
62. Amaral DG, Kurz J. The time of origin of cells demonstrating glutamic acid decarboxylase-like immunoreactivity in the hippocampal formation of the rat. Neurosci Lett 1985;59:33-9.
63. Seress L, Frotscher M, Riback EC. Local circuit neurons in both , the dentate gyrus and Ammon's hom establish synaptic connections with the principal neurons in five day old rats: a morphological basis for inhibition in early development. Exp Brain Res 1989;78:l-9. !
64. Ben-Ari Y, Rovira C, Gaiarsa JL, Coradetti R, Robain O, Cherubini E. GABAergic mechanisms in the CA3 hippocampal region during early postnatal life. Prog Drain Res 1990;83:313-21.
65. Ben-Ari Y, Tseeb V, Ragozzino D, Khazipov R, Gaiarsa JL. y-Aminobutyric acid (GABA): a fast excitatory transmitter which may regulate the development of hippocampal neurons in early postnatal life. Prog Brain Res 1994;102:261-73.
66. . 67. ' Rozenberg F, Robain O, Jardin L, Ben-Ari Y. Distribution of GABAergic neurons in late and early postnatal rat hippocampus. Dev Brain Res 1989;50:177-87.
67. Coyle JT, Enna SJ. Neurochemical aspects of the ontogenesis of , GABAergic neurons in the rat brain. Brain Res 1976;! 11:119-33.
68. Swann JW, Brady RJ, Martin DL. Postnatal development of GABA-mediated synaptic inhibition in rat hippocampus. Neuroscience 1989:28:551-61. .
69. Redburn DA, Broome D, Ferkany J, Enna SJ. Development of rat brain uptake and calcium-dependent release of GABA. Brain Res 1978:152:511-9.
70. Moshé SL, Shinnar S, Swann JW. Partial (focal) seizures in developing brain. In: Schwartzkroin PA, Moshé SL, Noebels SL, Swann JW, eds. Brain development and epilepsy. New York: Oxford University Press, 1995:34-65.
71. Gaiarsa JI, McLean H, Congar P, et al. Postnatal maturation of ' GABA-A and GABA-B mediated inhibition in the CA3 hippocampal region of the rat. J Nenrophysiol 1995;26:339-49.
72. Gaiarsa JI, Tseeb V, Ben-Ari Y. Postnatal development of pre and postsynaptic GABAB-mediated inhibitions in the rat CA3 hippocampal region of the rat. J Nenrophysiol 1994;73:246-55.
73. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 1989;416:303-25.
74. Killisch I, Dotti CG, Laune DJ, Lüddens H, Seeburg PH. Expression patterns of GAB AA receptor subtypes in developing hippocampal neurons. Neuron I991;7:927-36.
75. Laurie DJ, Wisden W, Seeburg PH. The distribution of the thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 1992;12:4151-72.
76. Poulter MO, Barker JL, O'CarroIl A-M, Lolait SJ, Mahan LC. Differential and transient expression of GABAA receptor a-subunit MRNAs in the developing rat CNS. J Neurosci Abst 1992; 12:2888-900.
77. Prince DA, Gutnick MJ. Neuronal activities in epileptogenic foci of immature cortex. Brain Res 1972;45:455-68.
78. Purpura DP. Relationship of seizure susceptibility to morphological and physiologic properties of normal and abnormal immature cortex. In: Kellaway P, Petersén I, eds. Neurologic and electroencephalographic correlative studies in infancy. New York: Grune & Stratton, 1964:117-54.
79. Purpura DP. Stability and seizure susceptibility of immature brain. In: Ward AA, Pope A, eds. Basic mechanisms of the epilepsies. Boston: Little Brown, 1969:481-505.
80. Purpura DP, Prelevic S, Santini M. Postsynaptic potentials and spike variations in feline hippocampus during postnatal ontogenesis. Exp Neural 1968;22:408-22.
81. Kriegstein AR, Suppes T, Prince DA. Cellular and synaptic physiology and epileptogenesis of the developing rat neocortical neurons in vitro. Dev Brain Res 1987;34:161-71. ' 83. Moshé SL. The effects of age on the kindling phenomenon. Dev Psychobiol 1981; 14:75-81.
82. Moshé SL, Sharpless NS, Kaplan J. Kindling in developing rats: variability of afterdischarge thresholds with age. Brain Res 1981; 211:190-5.
83. Michelson HB, Lothman E\V. An ontogenetic study of kindling using rapidly recurring hippocampal seizures. Dev Brain Res 1991:61:79-85.
84. Mattson MP, Kumar KN, Wang H, Cheng B, Michaelis EK. Basic FGF regulates the expression of a functional 71 kDa NMDA receptor protein that mediates calcium influx and neurotoxicity in hippocampal neurons. J Neurosci 1993;13:4575-88.
85. Velîsek L, Mares P. Increased epileptogenesis in the immature hippocampus. Exp Brain Res 1991;20:183-5.
86. Purpura DP. Analysis of axodendrilic synaptic organizations in immature cerebral cortex. Ann NY Acad Sei 1961;94:604-54.
87. Purpura DP, Shofer RJ, Scarff T. Properties of synaptic activities and spike potentials of neurons in immature neocortex. J Neuropliysiol 1965;28:925-42.
88. Sawa M, Maruyama N, Kaji S. Intracellular potential recording during electrically induced seizures. Electroencephalogr Clin Neitrophysiol 1963:15:209-20.
89. Jensen FE, Applegate CD, Holzman D, Belin TR, Burchfiel JL. Epileptogenic effect of hypoxia in the immature rodent brain. Ann Neural 1991;29:629-37.
90. Cavalheiro EA, Suva DF, Turski WA, Calderazzo-Filho LS, Bortolotto ZA, Turski L. The susceptibility of rats to pilocarpineinduced seizures is age-dependent. Dev Brain Res 1987;37:4358.
91. Liu Z, Gatt A, Mikati M, Holmes GLi Long-term behavioral deficits following pilocarpine seizures in immature rats. EpilepsyRes 1995:19:191-204.
92. Stafstrom CE, Thompson JL, Holmes GL. Kainic acid seizures in the developing brain: status epilepticus and spontaneous recurrent seizures. Dev Brain Res 1992;65:237-46.
93. Stafstrom CE, Holmes GL, Chronopoulos A, Thurber S, Thompson JL. Age-dependent cognitive and behavior deficits following kainic acid-induced seizures. Epilepsia 1993;34:420-32.
94. McCowan TJ, Breese GR. The developmental profile of seizure genesis in the inferior collicular cortex of the rat: relevance to human neonatal seizures. Epilepsia 1992;33:2-10.
95. Gilbert ME, Cain DP. A developmental study of kindling in the rat. Dev Brain Res 1982;2:321-8.
96. Baram TZ, Hirsch E, Schultz L. Short-interval amygdala kindling in neonatal rats. Dev Brain Res 1993:73:79-83.
97. Schmidt-Kastner R, Heim C, Sontag K-H. Damage of substantia nigra pars reticulata during pilocarpine-induced status epilepticus in the rat: immunohistochemistry study of neurons, astrocytes and serum-protein extravasation. Exp Brain Res 1991;86:125-10.
98. Holmes GL, Thompson JL. Rapid kindling in the prepubescent rat. Brain Res 1987;433:281l.
99. Moshé SL, Albala BJ, Ackermann RF, Engel J Jr. Increased seizure susceptibility of the immature brain. Dev Brain Res 1983; 7:81-5.
100. Goddard GV, Mclntyre DC, Leech CK. A permanent change in brain function resulting from daily electrical stimulation. Exp Neural 1969;25:295-30.
101. Racine RJ, Burnham WM, Gärtner JG, Levitan D. Rates of motor seizure development in rats subjected to electrical brain stimulation: strain and interstimulation interval effects. Electroencephalogr Clin Neitrophysiol 1973:35:553-6.
102. Peterson SL, Albertson TE, Stark LG. Intertriai intervals and kindled seizures. Exp Neural 1981:71:144-53.
103. Duchowny MS, Burchfiel JL. Facilitation and antagonism of kindled seizure development in the limbic system of the rat. Electroencephalogr Clin Neiirophysiol 1981;51:403-16.
104. Burchfiel JL, Serpa KA, Duffy FH. Further studies of antagonism of seizure development between concurrently developing kindled limbic foci in the rat. Exp Neural 1982:75:476-89.
105. Sperber EF, Haas K, Moshé SL. Mechanism of kindling in de-veloping animals. In: Wada JA, ed. Kindling 4. New York: Plenum Press, 1990:157-67.
106. Hablitz JJ. Spontaneous ictal-like discharges and sustained potential shifts in the developing rat neocortex. J Neurophysiol 1987:58:1052-65.
107. Hablitz JJ, Heinemann U. Alterations in the microenvironment during spreading depression associated with epileptiform activity in the immature neocortex. Dev Brain Res 1989;46:243-52.
108. S wann J\V. Synaptogenesis and epileptogenesis in developing neural networks. In: Schwartzkroin PA, Moshé SL, Noebels JL, Swann JW, eds. Brain development and epilepsy. New York: Oxford University Press, 1995:195-233.
109. Schwartzkroin PA. Development of rabbit hippocampus: physiology. Dev Brain Res 1982;2:469-86.
110. Dunwiddie TV. Age-related differences in the in vitro rat hippocampus: development of inhibition and the effects of hypoxia. Dev Neurosci 1981 ;4:165-75.
111. Harris KM, Teyler TJ. Evidence for late development of inhibition in area CA1 of the rat hippocampus. Brain Res 1983;268: 339-43.
112. Schwartzkroin PA, Altschuler RJ. Development of kitten hippocampal neurons. Brain Res 1977; 134:429-44.
113. Brady RJ, Swann JW. Postsynaptic actions of baclofen associated with its antagonism of bicuculline-induced epileptogenesis in hippocampus. Celt Mol Nenrobiol 1984;4:403-8.
114. Janigro D, Schwartzkroin PA. Effects of GABA and baclofen on pyramidal cells in the developing rabbit hippocampus: an 'in vitro' study. Brain Res 1988;41:171-84.
115. Schwartzkroin PA, Kunkel DD. Electrophysiology and morphology of the developing hippocampus of fetal rabbits. J Neurosci 1982:2:448-62.
116. Schwartzkroin PA, Kunkel DD, Mathers LH. Development of rabbit hippocampus: anatomy. Dev Brain Res 1982;2:463-68.
117. Schwartzkroin PA. Epileptogenesis in the immature CNS. In: Schwartzkroin PA, Wheat HV, eds. Electrophysiology of epilepsy. London: Academic Press, 1984:389-12.
118. Hamon B, Heinemann U. Developmental changes in neuronal sensitivity to excitatory amino acids in area CA, of the rat hippocampus. Dev Brain Res 1988:38:286-90.
119. Luhmann JH, Prince DA. Postnatal maturation of the GABAergic system in rat neocortex. J Neurophysiol 1991;65:247-63.
120. Cherubini E, De Feo MR, Mecarelli O, Ricci GF. Behavioral and electrographic patterns induced by systemic administration of kainic acid in developing rats. Dev Brain Res 1983;9:69-77.
121. Moshé SL, Comblath M. Developmental aspects of epileptogenesis. In: Wyllie E, ed. The treatment of epilepsy: principles and practice. Philadelphia: Lea & Febiger, 1993:99-110.
122. ladarola MJ, Gale K. Substantia nigra: site of anticonvulsant activity mediated by -y-aminobutyric acid. Science 1982;218:123740.
123. Gilbert ME, Cain DP. A single neonatal pentylenetetrazol or hyperthermia convulsion increases kindling susceptibility in the adult rat. Dev Brain Res 1985;22:169-80.
124. Turski L, Cavalheiro EA, Schwarz M, et al. Susceptibility to seizures produced by pilocarpine in rats after microinjection of isoniazid or -y-vinyl-GABA into the substantia nigra. Brain Res 1986:370:294-309.
125. McNamara JO, Galloway MT, Rigsbee LC, Shin C. Evidence implicating substantia nigra in regulation of kindled seizure threshold. / Neurosci 1984;4:2410-7.
126. Okada R, Moshé SL, Wong BY, Sperber EF, Zhao D. Age-related substantia nigra-mediated seizure facilitation. Exp Neural 1986; 93:180-7.
127. Farwell JR, Dodrill CB, Batzel LW. Neuropsychological abilities of children with epilepsy. Epitepsia 1985;26:395-100.
128. Holmes GL. Diagnosis and management of seizures in children. Philadelphia: W.B. Saunders, 1987.
129. Collins AL, Lennox WG. The intelligence of 300 private epileptic patients. Proc Assoc Res Nerv Ment Dis 1947:26:586-603.
130. Holmes GL. Do seizures cause brain damage? Epilepsia 1991; 32(suppl5):S 14-28.
131. Holmes GL. The long-term effects of seizures on the developing brain: clinical and laboratory issues. Brain Dev 1991:13:393-409.
132. Rodin EA, Schmaltz S, Twitty G. Intellectual functions of patients with childhood-onset epilepsy. Dev Med Child Neural 1986;28:25-33.
133. Funakoshi A, Morikawa T, Muramatsu R, Yagi K, Seino M. A prospective W1SC-R study in children with epilepsy. Jpn J Psychiatry Neural 1988;42:562-4.
134. Bourgeois BFD, Prensky AL, Palkes HS, Talent BK, Busch SG. Intelligence in epilepsy: a prospective study in children. Ann Neural 1983:14:438-44.
135. Falconer MA, Serafetinides EA, Corsellis JAN. Etiology and pathogenesis of temporal lobe epilepsy. Arch Neural 1964; 10: 233-18.
136. Ounsted C, Lindsay J, Norman R. Biological factors in temporal lobe epilepsy. Lond: The Spastics Society Medical Education and Information Unit, in association with William Heinemann Medical Books, 1966. (Clinics in developmental medicine; no. 22.)
137. Annegers JF, Hauser WA, Elveback LR, Kurland LT. The risk of epilepsy following febrile convulsions. Neurology 1979;29:297303.
138. Rocca WA, Sharbrough FW, Hauser WA, Annegers JF, Schoenberg BS. Risk factors for complex partial seizures: A populationbased case-control study. Ann Neural 1987;21:22-31.
139. Aicardi J, Chevrie J-J. Consequences of status epilepticus in infants and children. In: Delgado-Escueta AV, Wasterlain CG, Treiman DM, Porter RJ, eds. Status epilepticus: mechanisms of brain damage and treatment. New York: Raven Press, 1983:11525. (Advances in neurology; vol. 34.)
140. Cavanagh JB, Meyer A. Aetiological aspects of Ammon's horn sclerosis associated with temporal lobe epilepsy. BrMedJ 1956; 2:1403-7.
141. Corsellis JAN, Bruton CJ. Neuropathology of status epilepticus in humans. In: Delgado-Escueta AV, Wasterlain CG, Treiman DM, Porter RJ, eds. Status epilepticus. New York: Raven Press, 1983: 129-39.
142. Wasterlain CG, Fujikawa DG, Penix L, Sankar R. Pathophysiological mechanisms of brain damage from status epilepticus. Epilepsia 1993;34(suppl l):S37-53.
143. Zimmerman HM. The histopathology of convulsive disorders in children. J Pediatr 1941:13:859-90.
144. Olney JW, Collins RC, Sloviter RS. Excitotoxic mechanisms of epileptic brain damage. Adv Neural 1986;44:857-77.
145. Represa A, Le Gai La Salle G, Ben-Ari Y. Hippocampal plasticity in the kindling model of epilepsy in rats. Neurosci Lett 1989;99: 345-50.
146. Choi DW. Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischémie damage. Trends Neurosci 1988:11:465-9.
147. Nadler JV. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sei 1981;29:2031-42.
148. Fariello GG, Golden GT, Smith GG, Reyes PF. Potentiation of kainic acid epileptogenicity and sparing from neuronal damage by an NMDA receptor antagonist. Epilepsy Res 1989;3:206-13.
149. Lees GJ, Leong W. The non-NMDA glutamate antagonist NBQX blocks the local hippocampus toxicity of kainic acid, but not the diffuse extrahippocampal damage. Neurosci Lett 1992;143:3942.
150. Sloviter RS, Dempster DW. "Epileptic" brain damage is replicated qualitatively in the rat hippocampus by central injection of glutamate or aspartate but not by GABA or acetylcholine. Brain Res Bull 1985:15:39-60.
151. Monaghan DT, Cotman DW. Distribution on N-Methyl-o-aspartate sensitive L-[3H]glutamate binding sites in rat brain. J Neurosci 1985:5:2909-19.
152. Monaghan DT, Yao D, Cotman CW. L-[3H] glutamate binds to kainate-, NMDA- and AMPA-sensitive binding sites: an autoradiographic analysis. Brain Res 1985;340:378-83.
153. Cotman CW, Monaghan DT. Anatomical organization of excitatory amino acid receptors and their properties. In: Schwarcz R, Ben-Ari Y, eds. Excitatory amino acids and epilepsy. New York: Plenum Press, 1986:237-52.
154. Tremblay E, Represa A, Ben-Ari Y. Autoradiographic localization of kainic acid binding sites in the human hippocampus. Brain Res 1985:343:378-82.
155. Collingridge GL, Bliss TVP. MNDA brains-their role in long, term potentiation. Trends Neurosci 1987; 10:288-93.
156. Hori N, ffrench-Mullen JMH, Carpenter DO. Kainic acid response and toxicity show pronounced Ca2+ dependence. Brain Res 1985:358:380-4.
157. Kudo Y, Ogura A. Glutamate-induced increase in intracellular Ça" concentration in isolated hippocampal neurons. Br J Pliarmacol 1986;89:191-8.
158. Choi DW. Ionic dependence of glutamate neurotoxicity. J Neurosci 1987:7:369-79.
159. Choi DW. Glutamate toxicity and diseases of the nervous system. Neuron 1988;l:623t.
160. Orrenius S, McConkey D, Belloma G, Nicoterm P. Role of Ca[2] in toxic killing. Trends Pliarmacol Sei 1989:10:281-5.
161. Siesjo BK. Historical review: calcium, ischemia, and death of brain cells. Ann NY Acad Sei 1988:522:638-61.
162. Sloviter RS, Dean E, Sollas AI, Goodman JH. Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat. J Comp Neural 1996:366:516-33.
163. Pollard H, Charriaut-Marlangue S, Cantagrel S, et al. Kainateinduced apoptotic cell death in hippocampal neurons. Neuroscience 1994:63:7-18.
164. Cavalheiro EA, Czuzwar SJ, Kleinrok Z, Turski L, Turski WA. Intracerebral cholinomimetics produce seizure-related brain dam, age in rats. Br J Pliarmacol 1983;79:284P.
165. Holmes GL, Thompson JL, Marchi T, Feldman DS. Behavioral effects of kainic acid administration on the immature brain. Epilepsia 1988:29:721-30.
166. Holmes GL, Thompson JL. Effects of kainic acid on seizure susceptibility in the developing brain. Brain Res 1988;467:51-9.
167. Albala BJ, Moshé SL, Okada R. Kainic-acid-induced seizures: a developmental study. De\- Brain Res 1984:13:139-48.
168. Moshé SL. Epileptogenesis and the immature brain. Epilepsia 1987;28(suppl 1):S3-15.
169. Pisa M, Sanberg MR, Corcoran ME, Fibiger HC. Spontaneously recurrent seizures after intracerebral injections of kainic acid in rat: a possible model of human temporal lobe epilepsy. Brain Res 1980:200:481-7.
170. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 1985;14:375-03.
171. Tauck D, Nadler JV. Evidence of functional mossy fiber sprouting in the hippocampal formation of kainic acid-treated rats. J Neurosci 1985;5:1016-22.
172. Cronin J, Dudek FE. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res 1988;474:181-t.
173. Sutula TP. Experimental models of temporal lobe epilepsy: new insights from the study of kindling and synaptic reorganization. Epilepsia 1990;31(suppl 3):S45-54.
174. Sutula TP. The pathology of the epilepsies: insights into the causes and consequences of epileptic syndromes. In: Dodson WE, Pellock JM, eds. Pédiatrie epilepsy: diagnosis and treatment. New York: Demos, 1993:37-44.
175. Soliviter RS. Decreased hippocampal inhibition and a selective loss of intemeurons in experimental epilepsy. Science 1987:235: 73-6.
176. Sloviter RS. Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the "dormant basket cell" hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1991;l:41-66.
177. Sloviter RS. The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy. Ann Neural 1994;35:640-54.
178. Sloviter RS. Decreased hippocampal inhibition and a selective loss of intemeurons in experimental epilepsy. Science 1995;235: 73-6.
179. Danscher G. Histochemical demonstration of heavy metals. A revised version of the sulphide silver method suitable for both light and electronmicroscopy. Hislochemistry I981;71:l-16.
180. Golarai G, Paroda I, Sutula T. Mossy fibers synaptic reorganiza-tion induced by repetitive pentylenetetrazol seizures. Soc Neurosci Absir 1988;14:882.
181. Stanfield BB. Excessive intra- and supragranular mossy fibers in the dentate gyrus of tottering (tg/tg) mice. Brain Res 1989;480: 294-9.
182. Sutula T, Harrison C, Steward O. Chronic epileptogenesis induced by kindling of the entorhinal cortex: the role of the dentate gyrus. Brain Res 1986;385:291-9.
183. Sutula T, Xiao-Xian H, Cavazos J, Scott G. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 1988:239:1147-50.
184. Babb TL, Kupfer WR, Pretorius JK, Crandall PH, Levesque PF. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience 1991;42:351-63.
185. Sutula T, Cascino G, Cavazos J, Parada I, Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neural 1989;26:321-30.
186. Mathern GW, Leite JP, Pretorius JK, Quinn B, Peacock WJ, Babb TL. Children with severe epilepsy: evidence of hippocampal neuron losses and aberrant mossy fiber sprouting during postnatal granule cell migration and differentiation. Dev Brain Res 1994; 78:70-80.
187. Babb TL, Brown WJ. Neuronal, dendritic and vascular profiles of human temporal lobe activity correlated with cellular physiology "in vivo". Adv Neural 1986;44:949-66.
188. Babb TL, Pretorius JK, Kupfer WR, Crandall PH. Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus. J Neurasci 1989;9:2562-74.
189. Sherwin AL, Quesney LF, Gauthier S, et al. Enzyme changes in actively spiking areas of human epileptic cerebral cortex. Neurology 1984:34:927-33.
190. Tursky T, Lassanova M, Sramka M, Nadvornik P. Formation of glutamate and GABA in epileptogenic tissue from human hippocampus in vitro. Acta Neurochir 1976;23:111-8.
191. Bekenstein JW, Lothman EW. Dormancy of inhibitory interneurons in a model of temporal lobe epilepsy. Science 1993:259:97100.
192. Obenaus A, Esclapez M, Houser CR. Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures. J Neurosci 1993:13:447085.
193. Thurber S, Chronopoulos A, Stafstrom CE, Holmes GL. Behavioral effects of continuous hippocampal stimulation in the developing rat. Dev Brain Res 1992:68:35-40.
194. Sperber EF, Haas KZ, Stanton PK, Moshé SL. Resistance of the immature hippocampus to seizure-induced synaptic reorganization. Dev Brain Res 1991;60:88-93.
195. Hirsch E, Baram TZ, Snead OC III. Ontogenic study of lithiumpilocarpine-induced status epilepticus in rats. Brain Res 1992; 583:120-6.
196. Thurber S, Mikati MA, Stafstrom CE, Jensen FE, Holmes GL. Quisqualic acid-induced seizures during development: a behavioral and EEG study. Epilepsia 1994;35:868-75.
197. Liu Z, Stafstrom C, Sarkisian M, et al. Age-dependent effects of
198. Baram TZ, Ribak CE. Peptide-induced infant status epilepticus causes neuronal death and synaptic reorganization. NeuroReport 1995;6:277-80.
199. Ribak CE, Baram TZ. Selective death of hippocampal CA3 py-1 ramidal cells with mossy fiber afférents after CRH-induced status epilepticus in infant rats. Dev Brain Res 1996;91:245-51.
200. Campochiaro P, Coyle JT. Ontogenic development of kainate neurotoxicity: correlates with glutamatergic innervation. Proc ' Nail Acad Sei USA 1978:75:2025-9.
201. Barca MA, Toledano A: Histochemical electron microscopic study of the enzyme glutamate dehydrogenase (GD) in post-natal developing cerebellum. Cell Mol Biol 1982;28:187-95.
202. RotheF, Schmidt W, Wolf G. Postnatal changes in the activity of glutamate dehydrogenase and aspartate aminotransferase in the rat nervous system with special reference to the glutamate trans, mitter metabolism. Dev Brain Res 1983;ll:67-74.
203. Kvamme E, Svenneby G, Torgner IAA, Drejer J, Schousboe A. Postnatal development of glutamate metabolizing enzymes in hippocampus from mice. Int J Dev Neurosci 1985:3:359-64.
204. Minc-Golomb D, Levy Y, Kleinberger N, Schramm M. D-[3H]Aspartate release from hippocampus slices studied in a multiwell system: controlling factors and postnatal development of release. Brain Res 1987;402:255-63.
205. Schmidt W, Wolf G: High-affinity uptake of L-[3H]glutamate and D-[3H]aspartate during postnatal development of the hippocampal formation: a quantitative autoradiographic study. Exp Brain Res 1988;70:50-4.
206. Gaiarsa JL, Zagrean L, Ben-Ari Y. Neonatal irradiation prevents the formation of hippocampal mossy fibers and the epileptic action of kainate on rat CA3 pyramidal neurons. J Neurophysiot 1994:71:204-15.
207. Nicoletti F, ladarola MJ, Wrobleswski JT, Costa E. Excitatory amino acid recognition sites coupled with inositol phospholipid metabolism: developmental changes and interaction with otladrenoceptors. Proc Nail Acad Sei USA 1986:83:1931-5.
208. Ferriero DM, Arcavi LJ, Simon RP. Ontogeny of excitotoxic injury to nicotinamide adenine dinucleotide phosphate diaphorase reactive neurons in the neonatal rat striatum. Neuroscience 1990; 36:417-24.
209. Brady RJ, Gorier JA, Monroe MT, Swann JW. Developmental alterations in the sensitivity of hippocampal NMDA receptors to AP5. Dev Brain Res 1994;83:190-6.
210. McDonald JW, Silverstein FS, Johnston MV. Neurotoxicity of Af-methyl-D-aspartate is markedly enhanced in developing rat central nervous system. Brain Res 1988:459:200-3.
211. McDonald JW, Johnston MV. Pharmacology of W-methyl-Daspartate-induced brain injury in an in vivo perinatal rat model. Synapse 1990;6:179-88.
212. McDonald JW, Trescher WH, Johnston MV. Susceptibility of brain to AMPA induced excitotoxicity transiently peaks during early postnatal development. Brain Res 1992;583:54-70.
213. McDonald JW, Trescher WH, Johnston MV. The selective ionotropic-type quisqualate receptor agonist AMPA is a potent neurotoxin in immature rat brain. Brain Res 1990;526:165-8.
214. Silverstein FS, Chen R, Johnston MV. The glutamate analogue quisqualic acid is neurotoxic of immature rat brain. Neurosci Lett 1986:71:13-8.
215. Silverstein FS, Chen RC, Johnston MV. The glutamate agonist quisqualic acid is neurotoxic in striatum and hippocampus of immature rat brain. Neurosci Lett 1986:71:13-8.
216. Trescher WH, McDonald JW, Johnston MV. Quinolinate-induced injury is enhanced in developing rat brain. Dev Brain Res 1994; 83:224-32.
217. Young RSK, Petroff OAC, Aquila WJ, Yates J. Effects of glutamate, quisqualate, and A'-methyl-D-aspartate in neonatal brain. ExpNeurol 1991;lll:362-8.
218. Wolf G, Keilhoff G. Kainate and glutamate neurotoxicity in dependence on the postnatal development with special reference to hippocampal neurons. Dev Brain Res 1984;14:15-21.
219. Kish PE, Kim SY, Ueda T. Ontogeny of glutamate accumulating activity in rat brain synaptic vesicles. Neurosci Lett 1989;97:18590.
220. Bickler PE, Gallego SM, Hansen BM. Developmental changes in intracellular calcium regulation in rat cerebral cortex during hypoxia. / Cereb Blood Flow Metab 1993;13:811-9.
221. Carmant L, Liu Z, Werner SJ, Mikati MA, Holmes GL. Effect of kainic acid-induced status epilepticus on inositol-trisphosphate and seizure-induced brain damage in mature and immature animals. Dev Brain Res 1995:89:67-72.
222. Irvine RF. Inositol tetrakisphosphate as a second messenger: confusions, contradictions and a potential resolution. BioEssays 1991:13:419-27.
223. Mitani A, Yanase H, Sakai K, Wake Y, Kataoka K. Origin of intracellular calcium elevation induced by in vitro ischemia-like condition in hippocampal slices. Brain Res 1993:601:103-10.
224. Sperber EF, Weireter KK, Kubova H, Romero M-T. Age-related changes in parvalbumin immunoreactivity following kainic acid seizure. Soc Neurosci Abstr 1995:21:1473.
225. Burke JP, Hablitz JJ. Modulation of epileptiform activity by metabotropic glutamate receptors in immature rat neocortex. J Neurophysiol 1995:73:205-17.
226. Vecil GG, Li PP, Warsch JJ. Evidence for metabotropic excitatory amino acid receptor heterogeneity: developmental and brain regional studies. J Neitrochem 1992:59:252-8.
227. McDonald JW, Fix AS, Tizzano JP, Schoepp DD. Seizures and brain injury in neonatal rats induced by 1S,3R-ACPD, a metabotropic glutamate receptor agonist. J Neurosci 1993; 13:4445-55.
228. Aniksztejn L, Sciancalepore M, Ben-Ari Y. Persistent current oscillations produced by activation of metabotropic glutamate receptors in immature CA3 hippocampal neurons. J Neurophysiol 1995;73:1422-9.
229. Franck JE, Schwartzkroin PA. Immature rabbit hippocampus is damaged by systemic but not intraventricular kainic acid. Dev Brain Res 1984;13:219-27.
230. Neill J, Liu Z, Sarkisian M, et al. Recurrent seizures in immature rats: effect on auditory and visual discrimination. Dev Brain Res 1996;95:283-92.
231. Camfield CS, Chaplin S, Doyle A-B, Shapiro SH, Cummings C, Camfield PR. Side effects of phénobarbital in toddlers; behavioral and cognitive aspects. J Pediatr 1979;95:361-5.
232. Vining EPG, Mellits D, Dorsen M, et al. Psychological and behavioral effects of antiepileptic drugs in children: a double blind comparison between phénobarbital and valproic acid. Pediatrics 1987;80:165-74.
233. Herranz JL, Armijo JA, Artega R. Clinical side effects of phénobarbital, primidone, phenytoin, carbamazepine, and valproate during monotherapy in children. Epilepsia 1988;29:794-804.
234. Farwell JR, Lee YJ, Hirtz DG, Sulzbacher SI, Ellenberg JH, Nelson KB. Phénobarbital for febrile seizures. Effects on intelligence and on seizure recurrence. N Engl J Med 1990;322:364-9.
235. Fishman RHB, Yanai J. Long-lasting effects of early barbiturates on central nervous system and behavior. Neurosci Biobehav Rev 1983:7:19-28.
236. Diaz J, Schain RJ, Bailey BG. Phenobarbital-induced brain growth retardation in artificially reared rat pups. Biol Neonate 1977:32:77-82.
237. Yanai J, Roselli-Austin L, Tabakoff B. Neuronal deficits in mice following prenatal exposure to phénobarbital. Exp Neural 1979; 64:237-44.
238. Serrano EE, Kunis DM, Ransom BR. Effects of chronic pheno- barbital exposure on cultured mouse spinal cord neurons. Ann ' Neural 1988:24:429-38.
239. Bergey GK, Swaiman KF, Schrier BK, Fitzgerald S, Nelson PG. j Adverse effects of phénobarbital on morphological and biochemi- | cal development of fetal mouse spinal cord neurons in culture Ann Neural 1981;9:584-9.
240. Leite JR, Rodriguez De Lores Amaiz G. Effect of chronic administration and withdrawal of sodium barbitone on protein synthesis of rat brain. Pliarmacol Biochem Behav 1978:8:323-6.
241. Telwari S, Greenberg SA, Do K, Grey PA. The response of rat brain protein synthesis to ethanol and sodium barbital. Alcohol Drug Res 1987;7:243-58.
242. Pick CG, Yanai J. Long-term reduction in spontaneous alternations after early exposure to phénobarbital. Int J Dev Neurosci 1984:2:223-8.
243. Diaz J, Schain RJ. Phénobarbital: effects of long-term administration on behavior and brain of artificially reared rats. Science 1978; 199:90-1.
244. Renfrey G, Schlinger H, Jakubow J, Poling A. Effects of phenytoin and phénobarbital on schedule-controlled responding and seizure activity in the amygdala-kindled rat. J Pliarmacol Exp Tlier 1989;248:967-73.
245. Wilks LJ, File SE, Dingemanse J. Hyperactivity and increased aggression in the rat several hours after a single dose of phénobarbital. Pharmacopsychologia 1988;1:23-31.
246. .File SE, Wilks LJ. Changes in seizure threshold and aggression ' ~ during chronic treatment with three anticonvulsants and on drug withdrawal. Psychophartnacology 1990:100:237-2.
247. McBride MC, Rosman NP, Davidson SJ, Oppenheimer EY. Long-term behavioral effects of phénobarbital in suckling rats. Exp Neural 1985;89:59-70.
248. Weinberger SB, Killam EK. Alterations in learning performance in the seizure-prone baboon: effects of elicited seizures and chronic treatment with diazepam and phénobarbital. Epilepsia 1978:19:301-16.
249. Mikati MA, Holmes GL, Chronopoulos A, et al. Phénobarbital therapy modifies seizure related brain injury in the developing brain. Ann Neural 1994;36:425-33.
250. McNamara JO. Cellular and molecular basis of activity. J Neurosci 1994:14:3413-25.