Is neuronal death required for seizure-induced epileptogenesis in the immature brain?

Progress in Brain Research

Volumn 135, Issue , 2002, Pages 365-375

  Baram, Tallie Z ^a   Eghbal Ahmadi, Mariam ^a   Bender, Roland A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL MODEL; CELL SPECIFICITY; CONFERENCE PAPER; CONTROLLED STUDY; EPILEPSY; EPILEPTOGENESIS; FEBRILE CONVULSION; GENE EXPRESSION; HIPPOCAMPUS; LIMBIC SYSTEM; NERVE CELL EXCITABILITY; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; RAT; SEIZURE; TEMPORAL LOBE EPILEPSY;

EID: 0036454727     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(02)35033-7     Document Type: Conference Paper

References (81)

1. Albala, B.J., Moshe, S.L. and Okada, R. (1984) Kainic-acid-induced seizures: A developmental study. Brain Res., 315: 139-148.
2. Armstrong, D.D. (1993) The neuropathology of temporal lobe epilepsy. J. Neuropathol. Exp. Neurol., 52: 433-443.
3. Babb, T.L. and Brown, B.J. (1987) Pathological findings in epilepsy. In: J. Engel (Ed.), Surgical Treatment of the Epilepsies. Raven, New York, NY, pp. 511-552.
4. Baram, T.Z. and Hatalski, C.G. (1998) Neuropeptide-mediated excitability: A key triggering mechanism for seizure generation in the developing brain. Trends Neurosci., 21: 471-476.
5. Baram, T.Z., Gerth, A. and Schultz, L. (1997) Febrile seizures: An appropriate-aged model suitable for long-term studies. Brain Res. Dev. Brain Res., 98: 265-270.
6. Baram, T.Z., Mina, E. and Bender, R.A. (2000) Neurogenesis of dentate gyrus granule cells is not altered by prolonged febrile seizures in the immature rat. Epilepsia, 41(Suppl. 7): 13.
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. Bender, R.A. and Baram, T.Z. (1999) Effects of febrile seizures in the immature rat model on interneuronal parvalbumin (PV) expression in the dentate gyrus. Epilepsia, 40(Suppl. 7): 120.
9. Bender, R.A. and Baram, T.Z. (2002) Do prolonged febrile seizures injure hippocampal neurons? Insights from animal models. In: T.Z. Baram and S. Shinnar (Eds.), Febrile Seizures. Academic Press, San Diego, CA, pp. 127-137.
10. Bender, R.A., Dube, C. and Baram, T.Z. (2000) Mossy fiber sprouting into the dentate gyrus inner molecular layer follows prolonged febrile seizures in the immature rat model. Epilepsia, 41 (Suppl. 7): 76.
11. Bender, R.A., Brewster, A., Santoro, B., Ludwig, A., Hofmann, F., Biel, M. and Baram, T.Z. (2001) Differential and age-dependent expression of hyperpolarization-activated, cyclic nucleotide-gated cation channel isoforms 1-4 suggest evolving roles in the developing rat hippocampus. Neuroscience, 106: 689-698.
12. Brunson, K.L., Eghbal-Ahmadi, M., Bender, R., Chen, Y. and Baram, T.Z. (2001) Long-term, progressive hippocampal cell loss and dysfunction induced by early-life administration of corticotropin-releasing hormone reproduce the effects of early-life stress. Proc. Natl. Acad. Sci. USA, 98: 8856-8861.
13. Bruton, C.J. (1988) The Neuropathology of Temporal Lobe Epilepsy. Oxford University Press, New York, Maudsley Monographs, No. 31.
14. Buckmaster, P.S. and Dudek, F.E. (1997) Neuron loss, granule cell axon reorganization and functional changes in the dentate gyrus of epileptic kainate-treated rats. J. Comp. Neurol., 385: 385-404.
15. Cavazos, J.E., Das, I. and Sutula, T.P. (1994) Neuronal loss induced in limbic pathways by kindling: Evidence for induction of hippocampal sclerosis by repeated brief seizures. J. Neurosci., 14: 3106-3121.
16. Cendes, F., Andermann, F., Gloor, P., Lopes-Cendes, I., Andermann, E., Melanson, D., Jones-Gotman, M., Robitaille, Y., Evans, A. and Peters, T. (1993) Atrophy of mesial structures in patients with temporal lobe epilepsy: Cause or consequence of repeated seizures?. Ann. Neurol., 34: 795-801.
17. Chang, D. and Baram, T.Z. (1994) Status epilepticus results in reversible neuronal injury in infant rat hippocampus: Novel use of a marker. Brain Res. Dev. Brain Res., 77: 133-136.
18. Chen, K., Baram, T.Z. and Soltesz, I. (1999) Febrile seizures in the developing brain result in persistent modification of neuronal excitability in limbic circuits [see comments]. Nat. Med., 5: 888-894.
19. Chen, K., Aradi, I., Thon, N., Eghbal-Ahmadi, M., Baram, T.Z. and Soltesz, I. (2001) Persistently modified H-channels after complex febrile seizures convert the seizure-induced enhancement of inhibition to hyperexcitability. Nat. Med., 7: 1-7.
20. Chen, Y., Bender, R.A., Frotscher, M. and Baram, T.Z. (2001) Novel and transient populations of corticotropin-releasing hormone-expressing neurons in developing hippocampus suggest unique functional roles: A quantitative spatiotemporal analysis. J. Neurosci., 21: 7171-7181.
21. Clifford, D.B., Olney, J.W., Maniotis, A., Collins, R.C. and Zorumski, C.F. (1987) The functional anatomy and pathology of lithium-pilocarpine and high-dose pilocarpine seizures. Neuroscience, 23: 953-968.
22. Dobbing, J. and Sands, J. (1973) Quantitative growth and development of human brain. Arch. Dis. Child, 48: 757-767.
23. Dobbing, J. and Sands, J. (1979) Comparative aspects of the brain growth spurt. Early Hum. Dev., 3: 79-83.
24. Dube, C., Chen, K., Eghbal-Ahmadi, M., Brunson, K., Soltesz, I. and Baram, TZ. (2000) Prolonged febrile seizures in immature rat model enhance hippocampal excitability long-term. Ann. Neurol., 47: 336-344.
25. Dudek, F.E., Obenaus, A., Schweitzer, J.S. and Wuarin, J.-P. (1994) Functional significance of hippocampal plasticity in epileptic brain: Electrophysiological changes of the dentate granule cells associated with mossy fiber sprouting. Hippocampus, 4: 259-265.
26. Eghbal-Ahmadi, M. (2000) Potential Role of Corticotropin Releasing Hormone (CRH) in Age-Specific Developmental Seizures. Thesis. University of California.
27. French, J.A., Williamson, P.D., Thadani, V.M., Darcey, T.M., Mattson, R.H., Spencer, S.S. and Spencer, D.D. (1993) Characteristics of medial temporal lobe epilepsy. I. Results of history and physical examination. Ann. Neurol., 34: 774-780.
28. Gallyas, F., Guldner, F.H., Zoltay, G. and Wolff, J.R. (1990) Golgi-like demonstration of 'dark' neurons with an argyrophil III method for experimental neuropathology. Acta Neuropathol., 79: 620-628.
29. Gallyas, F., Zoltay, G. and Horvath, Z. (1992) Light microscopic response of neuronal somata, dendrites and axons to postmortem concussive head injury. Acta Neuropathol., 83: 499-503.
30. Gottlieb, A., Keydar, I. and Epstein, H.T. (1977) Rodent brain growth stages: An analytical review. Biol. Neonate, 32: 166- 176.
31. Hatalski, C.G., Brunson, K.L., Tantayanubutr, B., Chen, Y. and Baram, T.Z. (2000) Neuronal activity and stress differentially regulate hippocampal and hypothalamic corticotropin-releasing hormone expression in the immature rat. Neuroscience, 101: 571-580.
32. Hjeresen, D.L. and Diaz, J. (1988) Ontogeny of susceptibility to experimental febrile seizures in rats. Dev. Psychobiol., 21: 261-275.
33. Holmes, G.L. and Ben-Ari, Y. (1998) Seizures in the developing brain: Perhaps not so benign after all. Neuron, 21: 1231-1234.
34. Holmes, G.L. and Thompson, J.L. (1988) Effects of kainic acid on seizure susceptibility in the developing brain. Brain Res., 467: 51-59.
35. Holmes, G.L., Gairsa, J.L., Chevassus Au Louis, N. and Ben Ari, Y. (1998) Consequences of neonatal seizures in the rat: Morphological and behavioral effects. Ann. Neurol., 44: 845-857.
36. Jensen, F.E. and Baram, T.Z. (2000) Developmental seizures induced by common early-life insults: Short- and long-term effects on seizure susceptibility. Ment. Retard. Dev. Disabil. Res. Rev., 6: 253-257.
37. Jensen, F.E., Applegate, C.D., Holtzman, D., Belin, T.R. and Burchfiel, J.L. (1991) Epileptogenic effect of hypoxia in the immature rodent brain. Ann. Neurol., 29: 629-637.
38. Kalviainen, R., Salmenpera, T., Partanen, K., Vainio, P., Riekkinen, P. and Pitkanen, A. (1998) Recurrent seizures may cause hippocampal damage in temporal lobe epilepsy. Neurology, 50:1377-1382.
39. Knudsen, F.U. (1996) Febrile seizures - Treatment and outcome. Brain Dev., 18: 438-449.
40. Kubova, H., Druga, R., Lukasiuk, K., Suchomelova, L., Haugvicova, R., Jirmanova, I. and Pitkanen, A. (2001) Status epilepticus causes necrotic damage in the mediodorsal nucleus of the thalamus in immature rats. J. Neurosci., 21: 3593-3599.
41. Kuzniecky, R.I., Bilir, E., Gilliam, F., Faught, E., Palmer, C., Morawetz, R. and Jackson, G. (1997) Multimodality MRI in mesial temporal sclerosis: Relative sensitivity and specificity. Neurology, 49: 774-778.
42. Lewis, D.V. (1999) Febrile convulsions and mesial temporal sclerosis. Curr. Opin. Neurol., 12: 197-201.
43. Liu, Z., Nagao, T., Desjardins, G.C., Gloor, P. and Avoli, M. (1994) Quantitative evaluation of neuronal loss in the dorsal hippocampus in rats with long-term pilocarpine seizures. Epilepsy Res., 17: 237-247.
44. Lothman, E.W. and Collins, R.C. (1981) Kainic acid induced limbic seizures: Metabolic, behavioral, electroencephalographic and neuropathological correlates. Brain Res., 218: 299-318.
45. Margerison, J.H. and Corsellis, J.A.N. (1966) Epilepsy and the temporal lobes: A clinical electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain, 399: 1246-1283.
46. McCabe, B.K., Silveira, D.C., Cilio, M.R., Cha, B.H., Liu, X., Sogawa, Y. and Holmes, G.L. (2001) Reduced neurogenesis following neonatal seizures. J. Neurosci., 21: 2094-2103.
47. Mello, L.E., Cavalheiro, E.A., Tan, A.M., Kupfer, W.R., Pretorius, J.K., Babb, T.L. and Finch, D.M. (1993) Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: Cell loss and mossy fiber sprouting. Epilepsia, 34: 985-995.
48. Motte, J., Fernandes, M.J., Baram, T.Z. and Nehlig, A. (1998) Spatial and temporal evolution of neuronal activation, stress and injury in lithium-pilocarpine seizures in adult rats. Brain Res., 793: 61-72.
49. Nadler, J.V. (1981) Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci., 29: 2031-2041.
50. Nadler, J.V., Perry, B.W. and Cotman, C.W. (1978) Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature, 271: 676-677.
51. Nehlig, A. and Pereira de Vasconcelos, A. (1996) The model of pentylenetetrazol-induced status epilepticus in the immature rat: Short- and long-term effects. Epilepsy Res., 26: 93-103.
52. Nitecka, L., Tremblay, E., Charton, G., Bouillot, J.P., Berger, M.L. and Ben-Ari, Y. (1984) Maturation of kainic acid seizure-brain damage syndrome in the rat, II. Histopathological sequelae. Neuroscience, 13: 1073-1094.
53. Obenaus, A., Esclapez, M. and Houser, C.R. (1993) Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures. J. Neurophysiol., 13: 4470-4485.
54. Owens, J.J., Robbins, C.A., Wenzel, H.J. and Schwartzkroin, P.A. (1997) Acute and chronic effects of hypoxia on the developing hippocampus. Ann. Neurol., 41: 187-199.
55. Parent, J.M. and Lowenstein, D.H. (2002) Seizure-induced neurogenesis: Are more new neurons good for an adult brain? In: T. Sutula and A. Pitkänen (Eds.), Do Seizures Damage the Brain. Progress in Brain Research, Vol. 135. Elsevier, Amsterdam, pp. 121-132.
56. Parent, J.M., Yu, T.W., Leibowitz, R.T., Geschwind, D.H., Sloviter, R.S. and Lowenstein, D.H. (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci., 17: 3727-3738.
57. Pineau, N., Charriaut-Marlangue, C., Motte, J. and Nehlig, A. (1999) Pentylenetetrazol seizures induce cell suffering but not death in the immature rat brain. Brain Res. Dev. Brain Res., 112:139-144.
58. Pollard, H., Charriaut-Marlangue, C., Cantagrel, S., Represa, A., Robain, O., Moreau, J. and Ben-Ari, Y. (1994) Kainate-induced apoptotic cell death in hippocampal neurons. Neuroscience, 63: 7-18.
59. Sankar, R., Shin, D.H., Liu, H., Mazarati, A., Pereira de Vasconcelos, A. and Wasterlain, C. (1998) Patterns of status epilepticus-induced neuronal injury during development and long-term consequences. J. Neurosci., 18: 8382-8393.
60. Santoro, B., Liu, D.T., Yao, H., Bartsch, D., Kandel, E.R., Siegelbaum, S.A. and Tibbs, G.R. (1998) Identification of a gene encoding a hyperpolarization-activated pacemaker channel of brain. Cell, 93: 717-729.
61. Santoro, B., Chen, S., Lüthi, A., Pavlidis, P., Shumyatsky, G.P., Tibbs, G.R. and Siegelbaum, S.A. (2000) Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J. Neurosci., 20: 5264-5275.
62. Scharfman, H.E. (1999) The role of nonprincipal cells in dentate gyrus excitability and its relevance to animal models of epilepsy and temporal lobe epilepsy. In: A.V. Delgado-Esqueta, W.A. Wilson, R.A. Olson and R.J. Porter (Eds.), Basic Mechanisms of the Epilepsies: Molecular and Cellular Approaches. Lippincott-Raven, New York, NY, 3rd ed., pp. 805-820.
63. Scharfman, H.E., Goodman, J.H. and Sollas, A.L. (2000) Granule-like neurons at the Hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: Functional implications of seizure-induced neurogenesis. J. Neurosci., 20: 6144-6158.
64. Schauwecker, P.E., Ramirez, J.J. and Steward, O. (2000) Genetic dissection of the signals that induce synaptic reorganization. Exp. Neurol., 161: 139-152.
65. Siegelbaum, S.A. (2000) Presynaptic facilitation by hyperpolarization-activated pacemaker channels. Nat. Neurosci., 3: 101-102.
66. Shinnar, S. (1998) Prolonged febrile seizures and mesial temporal sclerosis. Ann. Neurol., 43: 411-412.
67. Sloviter, R.S. (1991) 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, 1: 41-66.
68. Sloviter, R.S. (1994) The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy. Ann. Neurol., 35: 640-654.
69. Sloviter, R.S. and Pedley, T.A. (1998) Subtle hippocampal malformation: Importance in febrile seizures and development of epilepsy. Neurology, 50: 846-849.
70. Sperber, E.F., Stanton, P.K., Haas, K., Ackerman, R.F. and Moshe, S.L. (1992) Developmental differences in the neurobiology of epileptic brain damage. In: J. Engel Jr., C. Wasterlain, E. A. Cavalheiro, U. Heinemann and G. Avanzini (Eds.), Molecular Neurobiology of Epilepsy. Elsevier, Amsterdam, pp. 67-81.
71. Sperber, E.F., Germano, I.M., Friedman, L.K., Velísková, J. and Romero, M.T. (1999) The resiliency of the immature brain to seizure-induced damage. In: A. Nehlig, J. Motte, S.L. Moshé and P. Plouin (Eds.), Childhood Epilepsies and Brain Development. John Libbey, London, pp. 255-262.
72. Sperk, G., Lassmann, H., Baran, H., Kish, S.J., Seitelberger, F. and Homykiewicz, O. (1983) Kainic acid induced seizures: Neurochemical and histopathological changes. Neuroscience, 10: 1301-1315.
73. Sperk, G., Lassman, H., Baran, H., Seitelberger, F. and Homykiewicz, O. (1985) Kainic acid-induced seizures: Dose relationship of behavioural, neurochemical and histopathological changes. Brain Res., 338: 289-295.
74. Sutula, T.P. (1991) Reactive changes in epilepsy: Cell death and axon sprouting induced by kindling. Epilepsy Res., 10: 62-70.
75. Thon, N., Chen, K., Aradi, I. and Soltesz, I. (2002) Physiology of limbic hyperexcitability after experimental complex febrile seizures: Interactions of seizure-induced alterations at multiple levels of neuronal organization. In: T.Z. Baram and S. Shinnar (Eds.), Febrile Seizures. Academic Press, San Diego, CA, pp. 202-213.
76. Toth, Z., Yan, X.X., Haftoglou, S., Ribak, C.E. and Baram, T.Z. (1998) Seizure-induced neuronal injury: Vulnerability to febrile seizures in an immature rat model. J. Neurosci., 18: 4285-4294.
77. Van den Pol, A.N. and Gallyas, F. (1990) Trauma-induced Golgi-like staining of neurons: A new approach to neuronal organization and response to injury. J. Comp. Neurol., 296: 654-673.
78. VanLandingham, K.E., Heinz, E.R., Cavazos, J.E. and Lewis, D.V. (1998) Magnetic resonance imaging evidence of hippocampal injury after prolonged focal febrile convulsions. Ann. Neurol., 43: 413-426.
79. Veliskova, J., Velisek, L. and Mares, P. (1988) Epileptic phenomena produced by kainic acid in laboratory rats during ontogenesis. Physiologia Bohemoslovaca, 37: 395-405.
80. Walker, M.C. and Kullmann, D.M. (1999) Febrile convulsions: A 'benign' condition?. Nat. Med., 5: 871-872.
81. Yan, X.X., Toth, Z., Schultz, L., Ribak, C.E. and Baram, T.Z. (1998) Corticotropin-releasing hormone (CRH)-containing neurons in the immature rat hippocampal formation: Light and electron microscopic features and colocalization with glutamate decarboxylase and parvalbumin. Hippocampus, 8: 231-243.