Secondary epileptogenesis, kindling, and intractable epilepsy: A reappraisal from the perspective of neural plasticity

International Review of Neurobiology

Volumn 45, Issue , 2001, Pages 355-386

  Sutula, Thomas P ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; EPILEPSY; GENETICS; HUMAN; KINDLING; NERVE CELL PLASTICITY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; TEMPORAL LOBE EPILEPSY;

ANIMALS; EPILEPSY; EPILEPSY, TEMPORAL LOBE; HUMANS; KINDLING, NEUROLOGIC; NEURONAL PLASTICITY;

EID: 0035200893     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/s0074-7742(01)45019-7     Document Type: Article

References (141)

1. Adams, B., Sazgar, M., Osehobo, P., Vanderzee, C., Diamond, J. Fahnestock, M., and Racine, R. J. (1997). Nerve growth factor accelerates seizure development, enhances mossy fiber sprouting, and attenuates seizure-induced decreases in neuronal density in the kindling model of epilepsy. J. Neurosci. 17, 5288-5296.
2. Alvarez, P., Zola-Morgan, S., and Squire, L. R. (1995). Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys. J. NeuroseJ. 15, 3796-3807.
3. Babb, T., and Brown, W. (1987). Pathological findings in epilepsy. In Surgical Treatment of the Epilepsies (J. Engel, Jr., éd.), pp. 51 1-540. Raven Press, New York.
4. Barr, W. B., Ashtari, M., and Schaul, N. (1997). Bilateral reductions in hippocampal volume in adults with epilepsy and a history of febrile seizures. J. Neurol. Neurosurg. Psychmtr. 63, 461-467.
5. Bengzon, J., Kokaia, Z., Elmer, E., Nanobashvili, A., Kokaia, M., and Lindvall, (). (1997). Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc. Null. Acad. Sei. U.S.A. 94, 10432-10437.
6. Berg, A. T., and Shinnar, S. (1997). Do seizures beget seizures? An assessment of the clinical evidence in humans. J. Clin. Neurophysiol. 14, 102-110.
7. Berkovic, S. F., and Scheffer, I. E. (1998). Febrile seizures: genetics and relationship to other epilepsy syndromes. Curr. Opin. Neuwl. 11, 129-134.
8. Bertram, E. H. D., and Lothman, E. W. (1993). Morphometric effects of intermittent kindled seizures and limbic status epilepticus in the dentate gyrus of the rat. Brain Res. 603,25-31.
9. 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. Neural. 385, 385-404.
10. Buhl, E. H., Otis, T. S., and Mody, I. (1996). Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science 271, 369-373.
11. Bunsey, M., and Eichenbaum, H. (1996). Conservation of hippocampal memory function in rats and humans. Nature 379, 255-257.
12. Camrnisuli, S., Murphy, M. P., Ikeda-Douglas, C. ]., Balkissoon, V., Holsinger, R. M., Head, E., Michael, M., Racine, R. J., and Milgram, N. W. (1997). Effects of extended electrical kindling on exploratory behavior and spatial learning. Behav. Brain Res. 89, 179-190.
13. Cascino, G. D., Jack, C. R., Jr., Parisi, J. E., Sharbrough, F. W., Hirschorn, K. A., Meyer, F. B., Marsh, W. R., and O'Brien, P. C]. (1991). Magnetic resonance imaging-based volume studies in temporal lobe epilepsy: pathological correlations. Ann Neural. 30, 31-36.
14. Cavazos, J., and Sutula, F. (1990). Progressive neuronal loss induced by perforant path kindling: a possible cellular mechanism of synaptic reoi-ganization and hippocampal sclerosis. Brain. Res. 527:1-6.
15. Cavazos, J., Golarai, G., and Sutula, T. (1991). Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence. J. Neurosci. 11, 2795-2803.
16. Cavazos, J. E., Das, I., and Sutula, T. (1994). Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J. Neurosci. 14, 3106-3121.
17. Cavazos, J., Zhang, P., and Sutula, T. (1997). Ultrastructural features of synapses and recurrent circuits of sprouted mossy fibers in kainate-treated and kindled rats. Soc. Neurosci. Abstr. 23, 814.
18. Corkin, S., Amaral, D. G., Gonzalez, R. G., Johnson, K. A., and Hyman, B. T. (1997). H. M.'s medial temporal lobe lesion: findings from magnetic resonance imaging. J. Neurosci. 17, 3964-3979.
19. Dalby, N. O., West, M., and Finsen, B. (1998). Hilar somatostatin-mrna containing neurons are preserved after perforant path kindling in the rat. Neurosci. Lett. 255, 45-48.
20. Davies, K. G., Hermann, B. P., Dohan, F. C., Jr., Foley, K. T., Bush, A. J., and Wyler, A. R. (1996). Relationship of hippocampal sclerosis to duration and age of onset of epilepsy, and childhood febrile seizures in temporal lobectomy patients. Epilepsy Res. 24, 119-126.
21. DeCarli, G., Hatta, J., Fazilat, S., Fazilat, S., Gaillard, W. D., and Theodore, W. H. (1998). Extratemporal atrophy in patients with complex partial seizures of left temporal origin. Ann Neural. 43, 41-45.
22. Eliashiv, S. D., Dewar, S., Wainwright, I., Engel, J., and Fried, I. (1997). Long-term follow-up after temporal lobe resection for lesions associated with chronic seizures. Neurology 48, 1383-1388.
23. Elmer, E., Kokaia, M., Kokaia, Z., Mclntyre, D. C., and Lindvall, O. (1998). Epileptogenesis induced by rapidly recurring seizures in genetically fast- but not slow-kindling rats. Brain Res. 789, 111-117.
24. Elwes, R. D., Chesterman, P., and Reynolds, E. H. (1985). Prognosis after a first untreated tonic-clonic seizure. Lancet ii, 752-753.
25. Elwes, R. D., Johnson, A. L., and Reynolds, E. H. (1988). The course of untreated epilepsy. Br. Med. J. 297, 948-950.
26. Engel, J., Jr. (1996a). Clinical evidence for the progressive nature of epilepsy. Epilepsy Res., Suppl. 12, 9-20.
27. Engel, J., Jr. (1996b). Introduction to temporal lobe epilepsy. Epilepsy Res. 26, 141-150.
28. Engel, J., Jr. (1996c). Surgery for seizures. N. Engl.J. Med. 334, 647-652.
29. Engel, J., Jr. (1998). Etiology as a risk factor for medically refractory epilepsy-a case for early surgical intervention. Neurology 51, 1243-1244.
30. Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A., and Gage, F. H. (1998). Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317.
31. Gilbert, T. H., McNamara, R. K., and Corcoran, M. E. (1996). Kindling of hippocampal field CA1 impairs spatial learning and retention in the Morris water maze. Behav. Brain Res. 82, 57-66.
32. Gloor, P. (1991). Mesial Temporal Sclerosis: Historical Background and an Overview from a Modern Perspective. Raven, New York.
33. Goddard, G. V. (1969). The development of epileptic seizures through brain stimulation at low intensity. Nature 214, 1020-1021.
34. Goddard, G. V., Mclntyre, D., and Leech, C. (1969). A permanent change in brain function resulting from daily electrical stimulation. Exp. Neural. 25, 295-330.
35. Golarai, G., Cavazos, J. E., and Sutula, T. P. (1992). Activation of the dentate gyrus by pentylenetetrazol evoked seizures induces mossy fiber synaptic reorganization. Brain Res. 593, 257-264.
36. Goldensohn, E. S. (1984). The relevance of secondary epileptogenesis to the treatment of epilepsy: kindling and the mirror focus. Epilepsia 25, S156-173.
37. Golla, F., Graham, S., and Grey Walter, W. (1937). The electroencephalogram in epilepsy. J. MenJ. S. 83, 137-155.
38. Gould, E., Tanapat, P., McEwen, B. S., Flügge, G., and Fuchs, E. (1998). Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Nntl. Aaid. Sei. U.S.A. 95, 3168-3171.
39. Gowers, W. R. (1901). Epilepsy and Other Chronic Convulsive Diseases: Their Causes, Symptoms, and Treatment. Churchhill, London.
40. Harvey, A. S., Grattan-Smith, J. D., Desmond, P. M., Chow, C. W., and Berkovic, S. F. (1995). Febrile seizures and hippocampal sclerosis: frequent and related findings in intractable temporal lobe epilepsy of childhood. Pediatr. Neural. 12, 201-206.
41. Hauser, W. A. (1992). The natural history of drug resistant epilepsy: epidemiologic considerations. Epilepsy Res., Suppl. 5, 25-28.
42. Hauser, W. A. (1994). The prevalence and incidence of convulsive disorders in children. Epilepsia 35, SI-6.
43. Hauser, W. A. (1995). Epidemiology of epilepsy in children. Neurosurg. Clin. North Am. 6, 419-429.
44. Hauser, W. A., Rich, S. S., Lee, J. R., Annegers, ). F., and Andersen, V. E. (1998). Risk of recurrent seizures after two unprovoked seizures. N. Engl. J. MJ. 338, 429-434.
45. Hellier, J. L., Patrylo, P. R., Buckmaster, P. S., and Dudek, F. E. (1998). Recurrent spontaneous motor seizures after repeated low-dose systemic treatment with kainateassessment of a rat model of temporal lobe epilepsy. Epilepsy Res. 31, 73-84.
46. Hermann, B. P., Seidenberg, M., Dohan, F. C., Jr., Wyler, A. R., Haitiner, A., Bobhol, J., and Perrine, A. (1995). Reports by patients and their families of memory change after left anterior temporal lobectomy: relationship to degree of hippocampal sclerosis. Neitrosurgery 36, 39-44.
47. Hermann, B. P., Seidenberg, M., Schoenfeld, J., and Da vies, K. (1997). Neuropsychological characteristics of the syndrome of mesial temporal lobe epilepsy. Arch. Nenrol. 54, 369-376.
48. Hiyoshi, T., Seino, M., Kakegawa, N., Higashi, T., Yagi, K., and Wada, J. A. (1993). Evidence of secondary epileptogenesis in amygdaloid overkindled cats: electroclinical documentation of spontaneous seizures. Epilepsia 34, 408-415.
49. Houser, C. R. (1990). Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Rmin Res. 535, 195-204.
50. Houser, C. R., Miyashiro, J. E., Swartz, B. E., Walsh, G. (.)., Rich, J. R., and DelgadoEscueta, A. V. (1990). Altered patterns of dynorphin immunoreactivity suggest mossy Ober reorganization in human hippocampal epilepsy. J. Neurosei. 10, 267-282.
51. Houser, C. R., Swartz, B. E., Walsh, G. ()., and Delgado-Escueta, A. V. (1992). Granule cell disorganization in the dentate gyrus: possible alterations of neuronal migration in human temporal lobe epilepsy. Epilepsy Res., Suppl. 9, 41-48.
52. Hughes, J. R. (1966). Bilateral EEG abnormalities in corresponding areas. Epilepsia 7, 44-52.
53. Kalviainen, R., Salmenpera, T., Partanen, K., Vainio, P., Riekkinen, P., Pitkanen, A. (1998). Recurrent seizures may cause hippocampal damage in temporal lobe epilepsy. Neurology 50, 1377-1382.
54. Kim, J., Guimaraes, P. O., Shen, M. Y., Masukawa, L., and Spencer, D. (1990). Hippocampal neuronal density in temporal lobe epilepsy with and without gliomas. Ada Neuropathol. 80, 41-45.
55. Kinloch, R. A., Treherne, J. M., Furness, L. M., and Hajimohamadreza, I. (1999). The pharmacology of apoptosis. TIPS 20, 35-42.
56. Kotloski, XX., and Sutula, T. (in preparation). Lee, J. W., Andermann, F., Dubeau, F., Bernasconi, A., MacDonald, D., Evans, A., and Reutens, D. C. (1998). Morphometric analysis of the temporal lobe in temporal lobe epilepsy. Epilepsia 39, 727-736.
57. Lehericy, S., Semah, F., Hasboun, D., Dormont, D., Clemenceau, S., Granat, O., Marsault, C., and Baulac, M. (1997). Temporal lobe epilepsy with varying severity-Mri study of 222 patients. Neuroradtology 39, 788-796.
58. Leite, J. P., Nakamura, E. M., Lemos, T., Masur, J., and Cavalheiro, E. A. (1990). Learning impairment in chronic epileptic rats following pilocarpine-induced status epilepticus. Braz.J. Med. Biol. Res. 23, 681-683.
59. Lynch, M. W., Rutecki, P. A., and Sutula, T. P. (1996). The effects of seizures on the brain. Curr. Opm. Neurol. 9, 97-102.
60. Margerison, J. H., and Corsellis, J. A. (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 89, 499-530.
61. Mathern, G. W., Babb, T. L., Vickrey, B. G., Melendez, M., and Pretorius, J. K. (1995). The clinical-pathogenic mechanisms of hippocampal neuron loss and surgical outcomes in temporal lobe epilepsy. Brain 118, 105-118.
62. Mathern, G. W., Babb, T. L., Leite, J. P., Pretorius, K., Yeoman, K. M., and Kuhlman, P. A. (1996). The pathogenic and progressive features of chronic human hippocampal epilepsy. Epilepsy Res. 26, 151-161.
63. Mathern, G. W., Bertram, E. H., 3rd, Babb, T. L., Pretorius, J. K., Kuhlman, P. A., Spradlin, S., and Mendoza, D. (1997). In contrast to kindled seizures, the frequency of spontaneous epilepsy in the limbic status model correlates with greater aberrant fascia dentata excitatory and inhibitory axon sprouting, and increased staining for Nmethyl-D-aspartate, AM PA and GABA (A) receptors. Neuroscience 77, 1003-1019.
64. Mclntyre, D. C., Kelly, M. E., and Dufresne, C. (1999). FAST and SLOW amygdala kindling rat strains: comparison of amygdala, hippocampal, piriform and perirhinal cortex kindling. Epilepsy Res. 35, 197-209.
65. McNamara, J. O. (1994). Cellular and molecular basis of epilepsy. J. Neurosci. 14, 3413-3425.
66. McNamara, J. O. (1999). Emerging insights into the genesis of epilepsy. Nature 399, Suppl. S, A15-A22.
67. Meldrum, B., Vigoureux, R., and Brierley, J. (1973). Systemic factors and epileptic brain damage: prolonged seizures in paralyzed babbons. Arch. Neurol. Psychiatr. 29, 82-87.
68. Mello, L. E., Cavalheiro, E. A., Tan, A. M., Pretorius, J. K., Babb, T. L., and Finch, D. M. (1992). Granule cell dispersion in relation to mossy fiber sprouting, hippocampal cell loss, silent period and seizure frequency in the pilocarpine model of epilepsy. Epilepsy Res., Suppl. 9, 51-59.
69. 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.
70. Mikati, M. A., Holmes, G. L., Chronopoulos, A., Hyde, P., Thurber, S., Gatt, A., Liu, Z., Werner, S., and Stafstrom, C. E. (1994). Phénobarbital modifies seizure-related brain injury in the developing brain. Ann. Neurol. 36, 425-433.
71. Miller, L. J., and Marx, J. (1998). Apoptosis. Science 281, 1301
72. Mody, I., Stanton, P. K., Heinemann, V. (1988). Activation of N-methyl-D-aspartate receptors parallels changes in cellular and synaptic properties of dentate granule cells after kindling. J. Neurophysiol. 59, 1033-1053.
73. Morrell, V. (1959). Experimental epilepsy in animals. Arch, Neural. 1, 141-147.
74. Morrell, F. (I960). Secondary epileptogenic lesions. Epilepsiu 1, 538-560.
75. Morrell, F. (1985). Secondary epileptogenesis in man. Arch. Neural. 42, 318-335.
76. Morrell, F. (1989). Varieties of human secondary epileptogenesis. J. Cliu. Neiirophysial. 6, 227-275.
77. Morrell, F. (1991). The role of secondary epileptogenesis in human epilepsy. Arch. Neural. 48,1221-1224.
78. Morrell, F., and Tsuru, N. (1976). Kindling in the frog: development of spontaneous epileptiform activity. Electraencephalagr. Clin. Neurophysiol. 40, 1-11.
79. Nadler, V., Perry, B., Gentry C., Cotman, C. (1980). Selective reinnervation of hippocampal areas CA1 and the fascia dentata after destruction of GA3-GA4 afférents with kainic acid. Brain Res. 182, 1-9.
80. Okazaki, M. M., Evenson, D. A., and Nadler, J. V. (1995). Hippocampal moss\ fiber sprouting and synapse formation after status epilepticus in rats: visualization after retrograde transport of biocytin.y. Cow;. Neural. 352, 515-534.
81. Otis, T. S., De Koninck, Y., and Mody, I. (1994). Lasting potentiation of inhibition is associated with an increased number of gamma-aminobutyric acid type A receptors activated during miniature inhibitory postsynaptic currents. Proc. Xatl. Acal. Sei. L'.S.A. 91,7698-7702.
82. Parent,]. M., Yu, I. 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. NeuroseJ. 17, 3727-3738.
83. Parent, J. M., Janumpalli, S., McNamara, J. ()., and Lowenstein, D. H. (1998). Increased dentate granule cell neurogenesis following amygdala kindling in the adult rat. Nfurosci. Lett. 247, 9-12.
84. Pinel, J. P. (1978). Experimental epileptogenesis: Kindling-induced epilepsy in rats. Exp. N enrol. 58, 190-202.
85. Pretel, S., Appelgate, G. D., and Piekut, D. (1997). Apoptotic and necrotic cell death following kindling induced seizures. Ada Histachem. 99, 71-79.
86. Proctor, F., Prince, D., and Morrell, F. (1964). Primary and secondary epileptogenic foci produced by discrete freezing of subcortical structures. Trans. Am. Neuml. Assoc. 89, 33-36.
87. Proctor, F., Prince, D., and Morrell, F. (1966). Primai) and secondary spike foci following depth lesions. Arch. Neural. 15, 151-162.
88. Qiao, X., and Noebels, J. L. (1993). Developmental analysis of hippocampal mossy fiber outgrowth in a mutant mouse with inherited spike-wave seizures. J. Neurasci. 13, 4622-4635.
89. Racine, R. J. (1972). Modification of seizure activity by electrical stimulation: II. Motor seizure. Electraencephalagr. Clin. Neurophsial. 32, 281-294.
90. Racine, R. J., Steingart, M., and Mclntyre, D. C. (1999). Development of kindling-prone and kindling-resistant rats: selective breeding and electrophysiological studies. Epilepsy Res. 35, 183-195.
91. Radhakrishnan, K., So, E. L., Silbert, P. L., Jack, C. R., Cascino, G. D., Sharbrough, F. W., and Obrien, P. G. (1998). Predictors of outcome of anterior temporal lobectomy for intractable epilepsy-a multivariate study. Neurology 51, 465-471.
92. Rempel-Clower, N. L., Zola, S. M., Squire, L. R., and Amaral, D. G. (1996). Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation.J. Neurosci. 16, 5233-5255.
93. Represa, A., LaSalle, L. G., and Ben-Ari, Y. (1989a). Hippocampal plasticity in the kindling model of epilepsy in rats. Neurosci. Lett. 99, 345-355.
94. Represa, A., Robain, O., Tremblay, E., and Ben-Ari, Y. (1989b). Hippocampal plasticity in childhood epilepsy. Neurosci. Lett. 99, 351-355.
95. Ribak, C. E., and Peterson, G. M. (1991). Intragranular mossy fibers in rats and gerbils form synapses with the somata and proximal dendrites of basket cells in the dentate gyrus. Hippocampus 1, 355-364.
96. Rutecki, P., Sayin, U., and Sutula, T. (1996). Long-term reduction of inhibition in the dentate gyrus of kindled rats. Soc. Neurosci. Abstr. 22, 187.
97. Sagar, H., and Oxbury, J. (1987). Hippocampal neuronal loss in temporal lobe epilepsy: correlation with early childhood convulsions. Ann. Neural. 22, 334-340.
98. Salmenpera, T., Kalviainen, R., Partanen, K., and Pitkanen, A. (1998). Hippocampal damage caused by seizures in temporal lobe epilepsy. Ijincet 351, 35.
99. Sarkisian, M. R., Tandon, P., Liu, Z., Yang, Y., Hori, A., Holmes, G. L., and Stafstrom, C. E. (1997). Multiple kainic acid seizures in the immature and adult brain: ictal manifestations and long-term effects on learning and memory. Epilepsia 38, 1157-1166.
100. Sass, K.J., Spencer, D. D., Kim.J. H., Westerveld, M., Novelly, R. A., and Lencz, T. (1990). Verbal memory impairment correlates with hippocampal pyramidal cell density. Neurology 40, 1694-1697.
101. Sass, K. J., Westerveld, M., Buchanan, C. P., Spencer, S. S., Kirn, J. H., and Spencer, D. D. (1994). Degree of hippocampal neuron loss determines severity of verbal memory decrease after left anteromesiotemporal lobectomy. Epilepsia 35, 1179-1186.
102. Sass, K.J., Buchanan, G. P., Kraemer, S., Westerveld, M., Kim, J. H., and Spencer, D. D. (1995). Verbal memory impairment resulting from hippocampal neuron loss among epileptic patients with structural lesions. Neurology 45, 2154-2158.
103. Sayin, U., Rutecki, P., and Sutula, T. (1996). Long-term reduction of inhibition develops in GA3 region of kindled rats in association with slowly evolving decrease of inhibition in the dentate gyrus. Epilepsia 37, 75.
104. Sayin, U., Rutecki, P., Sutula T. (1999). Alterations in NMDA dependent currents in granule cells of the dentate gyrus contribute to the induction but not the permanence of kindling. J. Neurophysiol. 81(2), 564-574.
105. Schauwecker, P. E., and Steward, O. (1997). Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc. Natl. Acad. Sei. U.SA. 94, 4103-4108.
106. Scoville, W., and Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. J. Neural. Neurosurg. Psychiatr. 20, 11-21.
107. Semah, F., Picot, M. C., Adam, G., Broglin, D., Arzimanoglou, A., Bazin, B., Gavalcanti, D., and Baulac, M. (1998). Is the underlying cause of epilepsy a major prognostic factor for recurrence? Neurology 51, 1256-1262.
108. Shinnar, S., Berg, A. T., Moshé, S. L., Peux, M., Maytal, J., Kang, H., Goldensohn, E. S., and Hauser, W. A. (1990). Risk of seizure recurrence following a first unprovoked seizure in childhood: a prospective study. Pediatrics 85, 1076-1085.
109. Shinnar, S., Berg, A. T., Moshé, S. L., O'Dell, C., Alemany, M., Newstein, D., Kang, H., Goldensohn, E. S., and Hauser, W. A. (1996). The risk of seizure recurrence after a first unprovoked afebrile seizure in childhood: an extended follow-up. Pediatrics 98, 216-225.
110. Shinnar, S., Berg, A., O'Dell, C., Newstein, D., Moshé, S., and Hauser, W.A. (2000). Predictors of multiple seizures in a cohort of children prospectively followed from the time of their first unprovoked seizure. Ann. Neural. 48(2): 140-147.
111. Silver, J. M., Shin, C., and McNamara, J. O. (1991). Antiepileptogenic effects of conventional anticonvulsants in the kindling model of epilepsy. Ann. Neuml. 29, 356-363.
112. Singh, N. A. et al. (1998). A novel potassium channel gene, KCNQ2, is mutated in an inherited epilepsy of newborns. Nat. Gen. 18, 25-29.
113. 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.
114. Sloviter, R. S. (1992). Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci. Lett. 137, 91-96.
115. Spigelman, I., Van, X. X., Obenaus, A., Lee, E. Y. S., Wasterlain, C. G., and Ribak, C. E. (1998). Dentate granule cells form novel basal dendrites in a rat model of temporal lobe epilepsy. Neuroscience 86, 109-120.
116. Squire, L. R., and Zola, S. M. (1997). Amnesia, memory and brain systems. Philos. Trans. R. Soc. London 352, 1663-1673.
117. Squire, L. R., Amaral, D. G., and Press, G. A. (1990). Magnetic resonance imaging of the hippocampal formation and mammillary nuclei distinguish medial temporal lobe and diencephalic amnesia. J. Neurosci. 10, 3106-3117.
118. Sramka, M., Sedlak, P., and Nadvornik, P. (1977). Observation of kindling phenomenon in treatment of pain by stimulation in thalamus. In Neurosurgical Treatment in Psychiatry, Pain, and Epilepsy (W. H. Sweet éd.), pp. 651-654. Univ. Park Press, Baltimore.
119. Stanfield, B. (1989). Excessive intra- and supragranular mossy fibers in the dentate gyrus of tottering (tgtg) mice. Brain Res. 480, 294-299.
120. Sutula, T. (1990). Experimental models of temporal lobe epilepsy: new insights from the study of kindling and synaptic reorganization. Epilepsia 31, S45-S54.
121. Sutula, T. and Hermann, B. (1999). Progression in mesial temporal lobe epilepsy. Ann. Neural. 45, 553-556.
122. Sutula, T., He, Xiao-Xian, Cavazos, J., and Scott, G. (1988). Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 239, 1147-1150.
123. Sutula, T., Cascino, G., Gavazos, J., Parada, I., and Ramirez, L. (1989). Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neiirol. 31, 322-330.
124. Sutula, T., Gavazos J., Golarai, G. (1992). Alteration of long-lasting structural and functional effects of kainic acid in the hippocampus bv brief treatment with phénobarbital. J. Neurosci. 12: 4173-4187.
125. Sutula, T., Lauersdorf, S., Lynch, M., Jurgella, G., and Woodard, A. (1995). Deficits in radial arm maze performance in kindled rats: evidence for long-lasting memory dysfunction induced by repeated brief seizures. J. Neurosci. 15, 8295-8301.
126. Sutula, T.,Koch, J., Golarai, G., Watanabe, Y., McNamara, J. 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(22): 7398-7406.
127. Sutula, T., Zhang, P., Lynch, M., Sayin, L., Golarai, Ci., and Rod, R. (1998). Synaptic and axonal remodeling of mossy fibers in the hilus and supragranular region of the dentate gyrus in kainate-treated rats.y. Comp. Neural. 390, 578-594.
128. Tasch, E., Gendes, F., Li, L. M., Dubeau, F., Andermann, F., and Arnold, D. L. (1999). Neuroimaging evidence of progressive neuronal loss and dysfunction in temporal lobe epilepsy. Ann. Neural. 45, 568-576.
129. Tauck, D. L., and Nadler, J. V. (1985). Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 5, 1016-1022.
130. Theodore, W. H., Bhatia, S., Hatta, J., Fazilat, S., DeGarli, G., Bookheimer, S. Y., and Gaillard, W. D. (1999). Hippocampal atrophy, epilepsy duration, and febrile seizures in patients with partial seizures. Neurology 52, 132-136.
131. 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. Neural. 43, 413-426.
132. Van Paesschen, W., Connelly, A., King, M. D., Jackson, G. D., and Duncan, J. S. (1997). The spectrum of hippocampal sclerosis: a quantitative magnetic resonance imaging study. Ann. Neural. 41, 41-51.
133. Wada, J. A. (1974). Persistent seizure susceptibility and recurrent spontaneous seizures in kindled cats. Epilepsia 15, 465-478.
134. Wada, J. A. (1975). Effects of tetrahydrocannabinols on kindled amygdaloid seizures and photogenic seizures in Senegalese baboons, Papio papio. Epilepsia 16, 439-448.
135. Wada, J. A. (1984). Limbic kindling in the forebrain-bisected photosensitive baboon, Papio papio. Epilepsia 25, 278-287.
136. Wada, J. A., and Osawa, T. (1976). Spontaneous recurrent seizure state induced by daily electric amygdaloid stimulation in Senegalese baboons (Papio papio). Neurology 26, 273-286.
137. Wallace, R. H., Wang, D. W., Singh, R., Scheffer, I. E., George, A. L., Jr., Phillips, H. A., Saar, K., Reis, A., Johnson, E. W., Sutherland, G. R., Berkovic, S. F., and Mulley, J. C. (1998). Febrile seizures and generalized epilepsy associated with a mutation in the Na+-channel betal subunit gene SCN1B. Nat. Gen. 19, 366-370.
138. Wilder, B. J. (1982). Experimental studies, models, and phylogenetic aspects of secondary epileptogenesis. In Secondary Epileptogenesis (A. Mayersdorf and R. Schmidt, eds.), pp. 27-43. Raven, New York.
139. Wood, E. R., Dudchenko, P. A., and Eichenbaum, H. (1999). The global record of memory in hippocampal neuronal activity. Nature 397, 613-616.
140. Yu, S. P., Yeh, C. H., Strasser, U., Tian, M., and Choi, D. W. (1999). NMDA receptormediated K+ efflux and neuronal apoptosis. Science 284, 336-339.
141. Zhang, L. X., Smith, M. A., Li, X. L., Weiss, S. R. B., and Post, R. M. (1998). Apoptosis of hippocampal neurons after amygdala kindled seizures. Mol. Brain Res. 55, 198-208.