The effects of seizures on the brain

Current Opinion in Neurology

Volumn 9, Issue 2, 1996, Pages 97-102

  Lynch, Michael W ^a   Rutecki, Paul A ^b,c   Sutula, Thomas P ^b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c WILLIAM S MIDDLETON MEMORIAL VETERANS HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTROPHIN; PROTEIN C FOS;

BRAIN FUNCTION; CELL DEATH; CELL FUNCTION; CELL STRUCTURE; GENE EXPRESSION; HUMAN; KINDLING; NERVE CELL PLASTICITY; SEIZURE; SHORT SURVEY; SYNAPTIC TRANSMISSION;

EID: 0029973462     PISSN: 13507540     EISSN: None     Source Type: Journal    
DOI: 10.1097/00019052-199604000-00007     Document Type: Short Survey

References (70)

1. Khrestchatisky M, Ferhat L, Charton G, Bernard A, Pollard H, Represa A, Ben-Ari Y: Molecular correlates between reactive and developmental plasticity in the rat hippocampus. J Neurobiol 1995, 26:426-436.
2. Hosford DA, Simonato M, Cao Z, Garcia-Cairasco N, Silver JM, Butler L, Shin C, McNamara JO: Differences in the anatomic distribution of immediate-early gene expression in amygdala and angular bundle kindling development. J Neurosci 1995, 15:2513-2523.
3. Kasof GM, Mandelzys A, Maika SD, Hammer RE, Curran T, Morgan JI: Kainic acid-induced neuronal death is associated with DNA damage and a unique immediate-early gene response in c-fos-lacZ transgenic rats. J Neurosci 1995, 15:4238-4249. Using β-galactosidase to monitor c-fos expression and using terminal transferase biotinylated-uridine triphosphate nick end labelling (TUNEL procedure) to monitor cell death in transgenic rats, the authors compared the effects of seizures (induced by systemic pentylenetetrazol) with the effects of seizures plus neuronal death (caused by systemic kainic acid). The prolonged expression of cytoplasmic Fos-lacZ in vulnerable regions of the hippocampus is shown to be a strong (but not absolute) predictor of cell death in kainate-treated rats.
4. -/-), the authors provide evidence that tissue plasminogen activator in the hippocampus is produced by microglia. Moreover, tissue plasminogen activator appears to play a role in kainate-induced neuronal degeneration and seizure susceptibility.
5. Hope BT, Kelz MB, Duman RS, Nestler EJ: Chronic electroconvulsive seizure (ECS) treatment results in expression of a long-lasting AP-1 complex in brain with altered composition and characteristics. J Neurosci 1994, 14:4318-4328.
6. Chen Z-L, Yoshida S, Kato K, Momota Y, Suzuki J, Tanaka T, Ito J, Nishino H, Aimoto S, Kiyama H, Shiosaka S: Expression and activity-dependent changes of a novel limbic-serine protease gene in the hippocampus. J Neurosci 1995, 15:5088-5097.
7. Link W, Konietzko U, Kauselmann G, Krug M, Schwanke B: Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci USA 1995, 92:5734-5738.
8. Yamagata K, Sanders LK, Kaufmann WE, Yee W, Barnes CA, Nathans D, Worley PF: rheb, a growth factor- and synaptic activity-regulated gene, encodes a novel ras-related protein. J Biol Chem 1994, 269:16333-16339.
9. Lindvall O, Kokaia Z, Bengzon J, Elmér E, Kokaia M: Neurotrophins and brain insults. Trends Neurosci 1994, 17:490-496. Review of neurotrophin changes after brain insults (including seizures, ischemia, hypoglycemia and focal trauma) and hypotheses regarding the induced functional effects.
10. Lo DC: Neurotrophic factors and synaptic plasticity. Neuron 1995, 15:979-981.
11. Thoenen H: Neurotrophins and neuronal plasticity. Science 1995, 270:593-598.
12. Kokaia Z, Metsis M, Kokaia M, Bengzon J, Elmér E, Smith M-L, Timmusk T, Siesjö BK, Persson H, Lindvall O: Brain insults in rats induce increased expression of the BDNF gene through differential use of multiple promoters. Eur J Neurosci 1994, 6:587-596.
13. Timmusk T, Lendahl U, Funakoshi H, Arenas E, Persson H, Metsis M: Identification of brain-derived neurotrophic factor promoter regions mediating tissue-specific, axotomy-, and neuronal activity-induced expression in transgenic mice. J Cell Biol 1995, 128:185-199.
14. Wetmore C, Olson L, Bean AJ: Regulation of brain-derived neurotrophic factor (BDNF) expression and release from hippocampal neurons is mediated by non-NMDA type glutamate receptors. J Neurosci 1994, 14:1688-1700.
15. Van der Zee CEEM, Rashid K, Le K, Moore K-A, Stanisz J, Diamond J, Racine RJ, Fahnestock M: Intraventricular administration of antibodies to nerve growth factor retards kindling and blocks mossy fiber sprouting in adult rats. J Neurosci 1995, 15:5316-5323.
16. Rashid K, Van der Zee CEEM, Ross GM, Chapman CA, Stanisz J, Riopelle RJ, Racine RJ, Fahnestock M: A nerve growth factor peptide retards seizure development and inhibits neuronal sprouting in a rat model of epilepsy. Proc Natl Acad Sci USA 1995, 92:9495-9499. A demonstration that preventing NGF binding to its receptor (by intraventricular infusion of a peptide that mimics the putative trkA binding domain of the NGF molecule) inhibits kindling-induced epileptogenesis and mossy fiber sprouting.
17. Kokaia M, Ernfors P, Kokaia Z, Elmer E, Jaenisch R, Lindvall O: Suppressed epileptogenesis in BDNF mutant mice. Exp Neurol 1995, 133:215-224.
18. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T: Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci USA 1995, 92:8856-8860.
19. Kang H, Schuman EM: Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 1995, 267:1658-1662.
20. Levine ES, Dreyfus CF, Black IB, Rummer MR: Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc Natl Acad Sci USA 1995, 92:8074-8077.
21. Cavazos JE, Das I, Sutula TP: Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J Neurosci 1994, 14: 3106-3121.
22. Meldrum BS, Bruton CJ: Epilepsy. In Greenfield's Neuropathology, edn 5. Edited by Adams JH, Duchen LW. New York: Oxford University Press; 1992:1246-1283.
23. Schreiber SS, Baudry M: Selective neuronal vulnerability in the hippocampus - a role for gene expression? Trends Neurosci 1995, 18:446-451.
24. van Lockeren Campagne M, Lucassen PJ, Vermeulen JP, Balázs P: NMDA and kalnate induce internucleosomal DNA cleavage associated with both apoptotic and necrotic cell death in the neonatal rat brain. Eur J Neurosci 1995, 7:1627-1640.
25. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P: Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondria) function. Neuron 1995, 15:961-973.
26. Sakhi S, Bruce A, Sun N, Tocco G, Baudry M, Schreiber SS: p53 induction is associated with neuronal damage in the central nervous system. Proc Natl Acad Sci USA 1994, 91:7525-7529. Following systemic kainic acid injection in rats, expression of the p53 tumor suppressor gene is induced in cells exhibiting morphological evidence of neuronal injury. The authors speculate thai p53, which is normally important in the regulation of cell proliferation, may be pathological when overexpressed in postmitotic neurons.
27. Mathern GW, Babb TL, Vickery BG, Melendez M, Pretorius JK: The clinicalpathogenic mechanism of hippocampal neuron loss and surgical outcomes in temporal lobe epilepsy. Brain 1995, 118:105-118.
28. Lipton SA, Rosenberg PA: Excitatory amino acids as a final common pathway for neurologic disorders. New Engl J Med 1994, 330:613-622.
29. Glass M, Dragunow M: Neurochemical and morphological changes associated with human epilepsy. Brain Res Rev 1995, 21:29-41.
30. Vreugdenhil M, Wadman WJ: Kindling-induced long-lasting enhancement of calcium current in hippocampal CA1 area of the rat: relation to calcium-dependent inactivation. Neuroscience 1994, 59:105-114.
31. Lowensfein DH, Gwinn RR Seren MS, Simon RP, McIntosh TK: Increased expression of mRNA encoding calbindin-D28K, the glucose-regulated proteins, or the 72 kDa heat-shock protein in three models of acute CNS injury. Mol Brain Res 1994, 22:299-308.
32. 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.
33. Sutula T, Cavazos J, Golarai G: Alteration of long-lasting structural and functional effects of kainic acid in the hippocampus by brief treatment with phenobarbital. J Neurosci 1992, 12:4173-4187.
34. Niquet J, Jorquera I, Faissner A, Ben-Ari Y, Represa A: Gliosis and axonal sprouting in the hippocampus of epileptic rats are associated with an increase of tenascin-C immunoreactivity. J Neurocytol 1995, 24:611-624.
35. Khurgel M, Switzer RC, Teskey GC, Spiller AE, Racine RJ, Ivy GO: Activation of astrocytes during epileptogenesis in the absence of neuronal degeneration. Neurobiol Disease 1995, 2:23-35.
36. Represa A, Niquet J, Pollard H, Ben-Ari V: Cell death, gliosis, and synaptic remodeling in the hippocampus of epileptic rats. J Neurobiol 1995, 26:413-425. A review of seizure-induced alterations of hippocampal morphology, with particular attention paid to changes in cytoskeleton proteins and the glial reaction that may shape axonal outgrowth and reactive synaptogenesis. Part of a special 'Activity-dependent forms of plasticity' issue edited by Ben-Ari that includes articles by many top investigators.
37. Holtzman DM, Lowenstein DH: Selective inhibition of axon outgrowth by antibodies to NGF in a model of temporal lobe epilepsy. J Neurosci 1995, 15:7062-7070.
38. 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, 352:515-534. The first definitive demonstration of granule cell-granule cell synapses through concurrent labelling of mossy fiber boutons and granule cell dendrites in rats treated with systemic pilocarpine, suggesting the seizure-induced formation of a recurrent excitatory circuit in the dentate gyrus.
39. Golarai G, Sutula TP: Functional alterations in the dentate gyrus after induction of long-term potentiation, kindling, and mossy fiber sprouting. J Neurophysiol 1996, 75:343-353. Using Timm histochemistry to detect mossy fiber sprouting and current-source density analysis to detect evoked membrane currents, the authors note alterations in rats examined 1 month after the last kindling-induced seizure that are co-localized and consistent with excitatory transmission by the sprouted mossy fibers.
40. Cavazos JE, Golarai G, Sutula TP: Mossy fiber reorganization induced by kindling: time course of development progression, and permanence. J Neurosci 1991, 11:2795-2803.
41. Franck JE, Pokomy J, Kunkel DD, Schwartzkroin PA: Physiologic and morphologic characteristics of granule cell circuitry in human epileptic hippocampus. Epilepsia 1995, 36:543-558.
42. Mathern GW, Pretorius JK, Babb TL: Quantified patterns of mossy fiber sprouting and neuron densities in hippocampal and lesional seizures. J Neurosurg 1995, 82:211-219.
43. Bundman MC, Pico RM, Gall CM: Ultrastructural plasticity of the dentate gyrus granule cells following recurrent limbic seizures: I. Increase in somatic spines. Hippocampus 1994, 4:601-610.
44. Drakew A, Müller M, Gähwiler BH, Thompson SM, Frotscher M: Spine loss in experimental epilepsy: quantitative light and electron microscopic analysis of intracellularly stained CA3 pyramidal cells in hippocampal slice cultures. Neuroscience 1996, 70:31-45.
45. Sloviter RS: The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy. Ann Neurol 1994, 35:640-654.
46. Mangan PS, Rempe OA, Lothman EW: Changes in inhibitory neurotransmission in the CA1 region and dentate gyrus in a chronic model of temporal lobe epilepsy. J Neurophysiol 1995, 74:829-840.
47. Schwarzer C, Sperk G: Hippocampal granule cells express glutamic acid decarboxylase-67 after limbic seizures in the rat. Neuroscience 1995, 69:705-709. A report of a transient but marked increase in the expression of one molecular form of glutamate acid decarboxylase-67, the rate-limiting enzyme of GABA synthesis, in the constitutively glutamatergic dentate granule cells after kainic acid injection. This raises the possibility that mossy fibers may mediate an endogenous anticonvulsive mechanism.
48. Schwarzer C, Williamson JM, Lothman EW, Vezzani A, Sperk G: Somatostatin, neuropeptide Y, neurokinin B, and cholecystokinin immunoreactivity in two chronic models of temporal lobe epilepsy. Neuroscience 1995, 69:831-845.
49. Williamson A, Telfeian AE, Spencer DD: Prolonged GABA responses in dentate granule cells in slices isolated from patients with temporal lobe sclerosis. J Neurophysiol 1995, 74:378-387
50. During MJ, Ryder KM, Spencer DD: Hippocampal GABA transporter function in temporal-lobe epilepsy. Nature 1995, 376:174-177. This paper describes the use of a microdialysis probe to demonstrate decreased glutamate-induced GABA release in human epileptogenic hippocampus versus contralateral nonepileptogenic hippocampus. Glutamate induced release is shown to be mediated in part by transporters which are decreased in kindled rat hippocampi, suggesting insufficient GABA release as a result of transporter loss in temporal lobe epilepsy patients.
51. A receptor subunit mRNA levels in dentate gyrus granule cells following recurrent kindling-induced seizures. Mol Brain Res 1994, 23:323-332.
52. A receptor subunit mRNAs in hippocampal pyramidal and granular neurons in the kindling model of epileptogenesis: an in situ hybridization study. Mol Brain Res 1995, 31:33-47.
53. 35S]t-butylbicyclophosphorothionate binding in kindled rat hippocampus shows different changes in CA1 area and fascia dentata. Neuroscience 1995, 66:547-554.
54. Otis TS, De Koninck Y, Mody I: Lasting potentiation of inhibition is associated with an increased number of gamma-aminobutyric acid type A receptors activated during miniature inhibitory postsynaptic currents. Proc Natl Acad Sci USA 1994, 91:7698-7702.
55. A receptors.
56. HCO3 because of more efficient buffering of the bicarbonate flux.
57. Köhr G, De Koninck Y, Mody I: Properties of NMDA receptor channels in neurons acutely isolated from epileptic (kindled) rats. J Neurosci 1993, 13:3612-3627.
58. Köhr G, Mody I: Kindling increases M-methyl-D-aspartate potency at single N-methyl-D-aspartate channels in dentate gyrus granule cells. Neuroscience 1994, 62:975-981.
59. Lothman EW, Rempe DA, Mangan PS: Changes in excitatory neurotransmission in the CA1 region and dentate gyrus in a chronic model of temporal lobe epilepsy. J Neurophysiol 1995, 74:841-848. One of a series of three consecutively published papers by this group that demonstrates the regional heterogeneity of physiological changes in hippocampal circuitry following self-sustaining limbic status epilepticus, a model of temporal lobe epilepsy. This study suggests an enhancement of ionotropic glutamatergic excitation in the CA1 and dentate gyrus regions that is accompanied by diminished GABAergic inhibition only in CA1, yielding greater hyperresponsiveness in CA1 than in the dentate.
60. Martin D, McNamara JO, Nadler JV: Kindling enhances sensitivity of CA3 hippocampal pyramidal cells to NMDA. J Neurosci 1992, 12:1928-1935.
61. Nadler JV, Thompson MA, McNamara JO: Kindling reduces sensitivity of CA3 hippocampal pyramidal cells to competitive NMDA receptor antagonists. Neuropharmacology 1994, 33:147-1 53.
62. Kraus JE, Yeh G-C, Bonhaus DW, Nadler JV, McNamara JO: Kindling induces the long-lasting expression of a novel population of NMDA receptors in hippocampal region CA3. J Neurosci 1994, 14: 4196-4205.
63. A receptor gene expression in adult rat hippocampus: an in situ hybridization study. J Neurosci 1994, 14:2697-2707.
64. Kamphuis W, De Rijk TC, Talamini LM, Lopes da Silva FH: Rat hippocampal kindling induces changes in the glutamate receptor mRNA expression patterns in dentate granule neurons. Eur J Neurosci 1994, 6:1119-1127.
65. Jones-Gotman M, Smith ML, Zatorre RJ: Neuropsychological testing for localizing and lateralizing the epileptogenic region. In Surgical Treatment of the Epilepsies, edn. 2. Edited by Engel J. New York: Raven Press; 1993:245-261.
66. Hermann B, Wyler A, Somes G, Berry A, Dohan F: Pathological status of the mesial temporal lobe predicts memory outcome from left anterior temporal lobectomy. Neurosurg 1992, 31:652-657.
67. Zola-Morgan S, Squire LR: Neuroanatomy of memory. Ann Rev Neurosci 1993, 16:547-563.
68. Liu Z, Gatt A, Werner SJ, Mikati MA, Holmes GL: Long-term behavioral deficits following pilocarpine seizures in immature rats. Epilepsy Res 1994, 19:191-204.
69. Mikati MA, Holmes GL, Chronopoulos A, Hyde P, Thurber S, Gatt A, Liu Z, Werner S, Stafstrom CE: Phenobarbital modifies seizure-related brain injury in the developing brain. Ann Neurol 1994, 36:425-433.
70. Sutula T, Lauersdorf S, Lynch M, Jurgella C, Woodard A: Deficits in radial arm maze performance in kindled rats: evidence for long-lasting memory dysfunction induced by repeated brief seizures. J Neurosci 1995, 15:8295-8301. A demonstration that kindled rats have a deficit in the ability to successfully repeat a criterion performance in a radial arm maze task when tested 1 month after the last evoked seizure. The deficit is strongly correlated with the number of evoked seizures.