Hypothetical mechanisms for the cellular and neurophysiologic basis of secondary epileptogenesis: Proposed role of synaptic reorganization

Journal of Clinical Neurophysiology

Volumn 14, Issue 2, 1997, Pages 90-101

  Dudek, F Edward ^a   Spitz, Mark ^b  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Epilepsy; Secondary epileptogenesis; Synaptic reorganization

Indexed keywords

DENTATE GYRUS; EPILEPTOGENESIS; EXCITATORY POSTSYNAPTIC POTENTIAL; HUMAN; LATENT PERIOD; NERVE FIBER GROWTH; REVIEW; SYNAPTIC INHIBITION; TEMPORAL LOBE; TEMPORAL LOBE EPILEPSY;

ANIMALS; DENTATE GYRUS; EPILEPSY; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; KAINIC ACID; NERVE NET; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 0031394539     PISSN: 07360258     EISSN: None     Source Type: Journal    
DOI: 10.1097/00004691-199703000-00002     Document Type: Review

References (66)

1. Babb TL, Brown WJ, Pretorius JK, Kupfer WR, Crandall PH. Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus. J Neurosci 1989;9:2562-74.
2. Babb TL, Kupfer WR, Pretorius JK, Crandall PH, Levesque MF. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Epilepsia 1991;42:351-63.
3. Bekenstein JW, Lothman EW. Dormancy of inhibitory interneurons in a model of temporal lobe epilepsy. Science 1993;259: 97-100.
4. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 1985;14:375-403.
5. Buckmaster PS, Wenzel HJ, Kunkel DD, Schwartzkroin PA. Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo. J Comp Neurol 1996;366:270-92.
6. Buhl EH, Otis TS, Mody I. Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science 1996;211:369-73.
7. Cavalheiro EA, Richie DA, Le Gal La Salle G. Long-term effects of intrahippocampal kainic acid injection in rats: a method for inducing spontaneous recurrent seizures. Electroencephalogr Clin Neurophysiol 1982;53:581-9.
8. Cavazos JE, Sutula TP. Progressive neuronal loss induced by kindling: a possible mechanism for mossy fiber synaptic reorganization in hippocampal sclerosis. Brain Res 1990;527:1-6.
9. Christian EP, Dudek FE. Characteristics of local excitatory circuits studied with glutamate microapplication in the CA3 area of rat hippocampal slices. J Neurophysiol 1988;59:90-109.
10. Cibula JE, Gilmore RL. Secondary epileptogenesis in humans. J Clin Neurophysiol 1997;14:111-27.
11. Cronin J, Dudek FE. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res 1988;474:181-4.
12. Cronin J, Obenaus A, House CR, Dudek FE. Electrophysiology of dentate granule cells after kainate-induced synaptic reorganization of the mossy fibers. Brain Res 1992;573:305-10.
13. Davenport CJ, Brown WJ, Babb TL. GABAergic neurons are spared after intrahippocampal kainate in the rat. Epilepsy Res 1990a;5:28-42.
14. Davenport CJ, Brown WJ, Babb TL. Sprouting of GABAergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat. Exp Neurol 1990b;109:180-90.
15. de Lanerolle NC, Kim JH, Robbins RJ, Spencer DD. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 1989;495:387-95.
16. Dudek FE, Snow RW, Taylor CP. Role of electrical interactions in synchronization of epileptiform bursts. In: Delgado-Escueta AV, Ward Jr. AA, Woodbury DM, Porter RJ, eds. Basic mechanisms of the epilepsies: molecular and cellular approaches. New York: Raven Press, 1986:593-617. (Advances in neurology; vol 44).
17. Engel J, Wilson CL. Evidence for enhanced synaptic inhibition in epilepsy. In: Nistico G, Morselli PL, Lloyd KG, Fariello RG, Engel J Jr., eds. Neurotransmitters, seizures, and epilepsy III. New York: Raven Press, 1986:1-13.
18. Forster FM. Reflex epilepsy, behavioral therapy and conditioned reflexes. Springfield: Thomas, 1977.
19. Franck JE, Pokorny J, Kunkel DD, Schwartzkroin PA. Physiologic and morphologic characteristics of granule cell circuitry in human epileptic hippocampus. Epilepsia 1995;36:543-58.
20. Golarai G, Sutula T. Functional alterations in the dentate gyrus after induction of long-term potentiation, kindling, and mossy fiber sprouting. J Neurophysiol 1996;75:343-53.
21. B receptors. J Neurosci 1996;16:4250-60.
22. Houser CR, Miyashiro JE, Swartz BE, Walsh GO, Rich JR, Delgado-Escueta AV. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J Neurosci 1990;10:267-82.
23. Isokawa M, Fried I. Extracellular slow negative transient in the dentate gyrus of human epileptic hippocampus in vitro. Neuroscience 1995;72:31-7.
24. Isokawa M, Levesque MF, Babb TL, Engel J. Single mossy fiber axonal systems of human dentate granule cells studied in hippocampal slices from patients with temporal lobe epilepsy. J Neurosci 1993;13:1511-22.
25. Isokawa-Akesson M, Wilson C, Babb TL. Inhibition in synchronously firing human hippocampal neurons. Epilepsy Res 1989;3:236-47.
26. Jefferys JGR. Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol Rev 1995;75:690-723.
27. Larner AJ. Axonal sprouting and synaptogenesis in temporal lobe epilepsy: possible pathogenetic and therapeutic roles of neurite growth inhibitory factors. Seizure 1995;4:249-58.
28. Masukawa LM, Urono K, Sperling M, O'Connor MJ, Burdette LJ. The functional relationship between antidromically evoked field responses of the dentate gyrus and mossy fiber reorganization in temporal lobe epileptic patients. Brain Res 1992;579: 119-27.
29. Mathern GW, Cifuentes F, Leite JP, Pretorius JK, Babb TL. Hippocampal EEG excitability and chronic spontaneous seizures are associated with aberrant synaptic reorganization in the rat intrahippocampal kainate model. Electroencephalogr Clin Neurophysiol 1993;87:326-39.
30. McNamara JO. Cellular and molecular basis of epilepsy. J Neurosci 1994;14:3413-25.
31. Meier CL, Dudek FE. Spontaneous and stimulation-induced synchronized burst afterdischarges in the isolated CA1 of kainate-treated rats. J Neurophysiol 1996;76:2231-9.
32. Miles R, Wong RKS. Single neurons can initiate synchronized population discharge in the hippocampus. Nature 1983;306:371-3.
33. Miles R, Wong RKS. Latent synaptic pathways revealed after tetanic stimulation in the guinea pig hippocampus. Nature 1987a;329:724-6.
34. Miles R, Wong RKS. Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J Physiol (Lond) 1987b;388: 611-29.
35. Milgram NW, Yearwood T, Khurgel M, Ivy GO, Racine R. Changes in inhibitory processes in the hippocampus following recurrent seizures induced by systemic administration of kainic acid. Brain Res 1991;551:236-46.
36. Mody I. The molecular basis of kindling. Brain Pathol 1993;3:395-403.
37. Morrell F. Experimental focal epilepsy in animals. Arch Neurol 1959;1:141-7.
38. Morrell F. Secondary epileptogenic lesions. Epilepsia 1960;1:538-60.
39. Morrell F, Smith MC, Detoledo-Morrell L. Secondary epileptogenesis and kindling. In: Wylie E, ed. The treatment of epilepsy: principles and practice. Philadelphia: Lea & Febiger, 1993: 126-44.
40. Nadler JV. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci 1981;29:2031-42.
41. Nadler JV, Perry BW, Cotman CW. Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature 1978;271:676-7.
42. Nadler JV, Perry BW, Cotman CW. Selective reinnervation of hippocampal area CAl and the fascia dentata after destruction of CA3-CA4 afferents with kainic acid. Brain Res 1980;182:1-9.
43. 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: 4470-85.
44. O'Brien TJ, Hogan RE, Sedal L, Murrie V, Cook MJ. Tooth-brushing epilepsy: a report of a case with structural and functional imaging and electrophysiology demonstrating a right frontal focus. Epilepsia 1996;37:694-7.
45. Okazaki MM, Evenson DA, Nadler JV. Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: visualization after retrograde transport of biocytin. J Comp Neurol 1995;352:515-34.
46. Perez Y, Morin Y, Beaulie C, Lacaille J. Axonal sprouting of CA1 pyramidal cells in hyperexcitable hippocampal slices of kainate-treated rats. Eur J Neurosci 1996;8:736-48.
47. Pisa M, Sanberg PR, 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.
48. Prince DA, Tseng G. Epileptogenesis in chronically injured cortex: in vitro studies. J Neurophysiol 1993;69:1276-91.
49. Represa A, Jorquera I, Le Gal La Salle G, Ben-Ari Y. Epilepsy induced collateral sprouting of hippocampal mossy fibers: does it induce the development of ectopic synapses with granule cell dendrites? Hippocampus 1993;3:257-68.
50. Ribak CE. Axon terminals of GABAergic chandelier cells are lost at epileptic foci. Brain Res 1985;326:251-60.
51. Ribak CE. Contemporary methods in neurocytology and their application to the study of epilepsy. In: Delgado-Escueta AV, Ward Jr AA, Woodbury DM, Porter RJ, eds. Basic mechanisms of the epilepsies: molecular and cellular approaches. New York: Raven Press, 1986:739-64. (Advances in neurology; vol 44).
52. Salin P, Tseng GF, Hoffman S, Parada I, Prince DA. Axonal sprouting in layer V pyramidal neurons of chronically injured cerebral cortex. J Neurosci 1995;15:8234-45.
53. Schwartzkroin PA. Basic research in the setting of an epilepsy surgery center. In: Engel J, ed. Surgical treatment of the epilepsies. New York: Raven Press, 1993:755-73.
54. Sloviter RS. Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 1987;235: 73-6.
55. 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;1:41-66.
56. Sloviter RS. Possible functional consequences of synaptic reorganization in the dentate gyms of kainate-treated rats. Neurosci Lett 1992;137:91-6.
57. Sloviter RS. The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy. Ann Neurol 1994;35:640-54.
58. Sperk G. Kainic acid seizures in the rat. Prog Neurobiol 1994;42:1-32.
59. Sutula T, Cascino G, Cavazos J, Parado I, Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 1989;26:321-30.
60. Tauck DL, Nadler JV. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 1985;5:1016-22.
61. Tuff LP, Racine RJ, Adamec R. The effects of kindling on GABA-mediated inhibition in the dentate gyrus of the rat. I. Pairedpulse depression. Brain Res 1983;277:79-90.
62. Turner DA, Wheal HV. Excitatory synaptic potentials in kainic acid-denervated rat CA1 pyramidal neurons. J Neurosci 1991;11:2786-94.
63. Wenzel HJ, Wooley CS, Schwartzkroin PA. Kainic acid-induced mossy fiber sprouting and synapse formation in the rat dentate gyrus. Soc Neurosci Abstr 1995;21:1572.
64. Williamson A, Telfein AE, Spencer DD. Prolonged GABA responses in dentate granule cells in slices isolated from patients with temporal lobe sclerosis. J Neurophysiol 1995;74:378-87.
65. Wuarin JP, Dudek FE. Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate-treated epileptic rats. J Neurosci 1996;16:4438-48.
66. Zhang N, Houser CR. Dynorphin immunoreactivity in the dentate gyrus in human temporal lobe epilepsy: an electron microscopic study of reorganized mossy fiber synapses. Soc Neurosci Abstr 1995;21:1962.