Epilepsy Research
Volume 26, Issue 1 , Pages 207-218 , December 1996

Vulnerability and plasticity of the GABA system in the pilocarpine model of spontaneous recurrent seizures

  • Carolyn R. Houser

      Affiliations

    • Corresponding Author InformationCorresponding author.
    • Brain Research Institute and Department of Neurobiology, University of California at Los Angeles, Los Angeles, CA 90095, USA
    • Comprehensive Epilepsy Program, Neurology and Research Services, VA Medical Center, West Los Angeles, Wadsworth Division, Los Angeles, CA 90073, USA
    • ,
  • Monique Esclapez

      Affiliations

    • Brain Research Institute and Department of Neurobiology, University of California at Los Angeles, Los Angeles, CA 90095, USA

Received 31 October 1995 ,Accepted 15 March 1996.

References 

  1. Babb TL, Pretorius JK, Kupfer WR, Crandall PH. Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus. J. Neurosci. 1989;9:2562–2574
  2. Bekenstein JW, Lothman EW. Dormancy of inhibitory interneurons in a model of temporal lobe epilepsy. Science. 1993;259:97–100
  3. Buckmaster PS, Schwartzkroin PA. Physiological and morphological heterogeneity of dentate gyrus-hilus interneurons in the gerbil hippocampus in vivo. Eur. J. Neurosci. 1995;7:1393–1402
  4. Cavalheiro EA, Fernandes MJ, Turski L, Naffah-Mazzacoratti MG. Spontaneous recurrent seizures in rats: Amino acid and monoamine determination in the hippocampus. Epilepsia. 1994;35:1–11
  5. Cavalheiro EA, Leite JP, Bortolotto ZA, Turski WA, Ikonomidou C, Tuski L. Long-term effects of pilocarpine in rats: structural damage of the brain triggers kindling and spontaneous recurrent seizures. Epilepsia. 1991;32:778–782
  6. Chang Y-C, Gottlieb DI. Characterization of the proteins purified with monoclonal antibodies to glutamic acid decarboxylase. J. Neurosci. 1988;8:2123–2130
  7. Cronin J, Dudek FE. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res. 1988;474:181–184
  8. 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;573:305–310
  9. Davenport CJ, Brown WJ, Babb TL. Sprouting of GABAergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat. Exp. Neurol. 1990;109:180–190
  10. Davenport CJ, Brown WJ, Babb TL. GABAergic neurons are spared after intrahippocampal kainate in the rat. Epilepsy Res. 1990;5:28–42
  11. DeLanerolle NC, Kim JH, Robbins RJ, Spencer DD. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res. 1989;495:387–395
  12. During MJ, Ryder KM, Spencer DD. Hippocampal GABA transporter function in temporal-lobe epilepsy. Nature. 1995;376:174–177
  13. Erlander MG, Tillakaratne NJK, Feldblum S, Patel N, Tobin AJ. Two genes encode distinct glutamate decarboxylases. Neuron. 1991;7:91–100
  14. Esclapez M, Houser CR. Somatostatin neurons are a subpopulation of GABA neurons in the rat dentate gyrus: Evidence from co-localization of pre-prosomatostatin and glutamate decarboxylase mRNAs. Neuroscience. 1994;64:339–355
  15. Esclapez M, Tillakaratne NJK, Kaufman DL, Tobin AJ, Houser CR. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J. Neurosci. 1994;14:1834–1855
  16. Esclapez M, Tillakaratne NJK, Tobin AJ, Houser CR. Comparative localization of mRNAs encoding two forms of glutamic acid decarboxylase with nonradioactive in situ hybridization methods. J. Comp. Neurol. 1993;331:339–362
  17. Franck JE, Kunkel DD, Baskin DG, Schwartzkroin PA. Inhibition in kainate-lesioned hyperexcitable hippocampi: Physiologic, autoradiographic, and immunocytochemical observations. J. Neurosci. 1988;8:1991–2002
  18. Freund TF, Buzsáki G, Leon A, Baimbridge KG, Somogyi P. Relationship of neuronal vulnerability and calcium binding protein immunoreactivity in ischemia. Exp. Brain Res. 1990;83:55–66
  19. Friedman LK, Pellegrini-Giampietro DE, Sperber EF, Bennett MVL, Moshé SL, Zukin RS. Kainate-induced status epilepticus alters glutamate and GABA-A receptor gene expression in adult rat hippocampus: An in situ hybridization study. J. Neurosci. 1994;14:2697–2707
  20. Halasy K, Somogyi P. Subdivision in the multiple GABAergic innervation of granule cells in the dentate gyrus of the rat hippocampus. Eur. J. Neurosci. 1993;5:411–429
  21. Han Z-S, Buhl EH, Lörinczi Z, Somogyi P. A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur. J. Neurosci. 1993;5:395–410
  22. Heinemann U, Beck H, Dreier JP, Stabel J, Zhang CL. The dentate gyrus as a regulated gate for the propagation of epileptiform activity. In:  Ribak CE,  Gall CM,  Mody I editor. The Dentate Gyrus and Its Role in Seizures Epilepsy Res.. Amsterdam: Elsevier; 1992;p. 273–280 Suppl. 7
  23. Houser CR. GABA neurons in seizures disorders: A review of immonocytochemical studies. J. Neurochem. 1991;16:295–308
  24. Houser CR. Morphological changes in the dentate gyrus in human temporal lobe epilepsy. Epilepsy Res. Suppl. 1992;7:223–234
  25. Houser CR, Esclapez M. GAD65 mRNA and protein labeling are increased in remaining hippocampal GABA neurons in a model of temporal lobe epilepsy. Soc. Neurosci. Abstr. 1994;20:408
  26. Houser CR, Esclapez M. Localization of mRNAs encoding two forms of glutamic acid decarboxylase in the rat hippocampal formation. Hippocampus. 1994;5:530–545
  27. Houser CR, Esclapez M, Fritschy JM, Möhler H. Decreased expression of the α5 subunit of the GABA-A receptor in a model of temporal lobe epilepsy. Soc. Neurosci. Abstr. 1995;21:1475
  28. 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;10:267–282
  29. Johansen FF, Zimmer J, Diemer NH. Early loss of somatostatin neurons in dentate hilus after cerebral ischemia in the rat precedes CA1 pyramidal cell loss. Acta Neuropathol. (Berlin). 1987;73:110–114
  30. Kamphuis W, DeRijk TC, Lopes da Silva FH. GABA-A receptor β1–3 subunit gene expression in the hippocampus of kindled rats. Neurosci. Lett. 1994;174:5–8
  31. Kapur J, Lothman EW. Loss of inhibition procedes delayed spontaneous seizures in the hippocampus after tetanic electrical stimulation. J. Neurophysiol. 1989;61:427–434
  32. Kapur J, Michelson HB, Buterbaugh GG, Lothman EW. Evidence for a chronic loss of inhibition in the hippocampus after kindling: Electrophysiological studies. Epilepsy Res. 1989;4:90–99
  33. Kaufman DL, Houser CR, Tobin AJ. Two forms of the γ-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. J. Neurochem. 1991;56:720–723
  34. Kokaia M, Pratt GD, Elmér E, Bengzon J, Fritschy J-M, Kokaia Z, et al. Biphasic differential changes of GABA-A receptor subunit mRNA levels in dentate gyrus granule cells following recurrent kindling-induced seizures. Mol. Brain Res. 1994;23:323–332
  35. Kosaka T, Wu J-Y, Benoit R. GABAergic neurons containing somatostatin-like immunoreactivity in the rat hippocampus and dentate gyrus. Exp. Brain Res. 1988;71:388–398
  36. Köhler C. Neuronal degeneration after intracerebral injections of excitotoxins. A histological analysis of kainic acid, ibotenic acid and quinolic acid lesions in the rat brain. In: 2nd ed..  Fuxe K,  Roberts P,  Schwarcz R editor. Excitotoxins, Wenner-Gren Center International Symposium Series. Vol. 39:London: Macmillan; 1983;p. 99–111
  37. Lancaster B, Wheal HV. Chronic failure of inhibition of the CA1 area of the hippocampus following kainic acid lesions of the CA3/4 area. Brain Res. 1984;295:317–324
  38. Liu Z, Nagao T, Desjardins GC, Gloor P, Avoli M. Quantitative evaluation of neuronal loss in the dorsal hippocampus in rats with long-term pilocarpine seizures. Epilepsy Res. 1994;17:237–247
  39. Lothman EW, Stringer JL, Bertram EH. The dentate gyrus as a control point for seizures in the hippocampus and beyond. In:  Ribak CE,  Gall CM,  Mody I editor. The Dentate Gyrus and Its Role in Seizures. Epilepsy Res.. Amsterdam: Elsevier; 1991;p. 301–313 Suppl. 7
  40. Lowenstein DH, Thomas DJ, Smith DH, McIntosh TK. Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. J. Neurosci. 1992;12:4846–4853
  41. Margerison JH, Corsellis JAN. Epilepsy and the temporal lobes: a clinical encephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain. 1966;89:499–530
  42. Mathern GW, Babb TL, Pretorius JK, Leite JP. Reactive synaptogenesis and neuron densities for neuropeptide Y., somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. J. Neurosci. 1995;15:3990–4004
  43. Mello LEAM, Cavalheiro EA, Tan AM, Kupfer WR, Pretorius JK, Babb TL, et al. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: Cell loss and mossy fiber sprouting. Epilepsia. 1993;34:985–995
  44. Müller W, Misgeld U. Picrotoxin- and 4-aminopyridine-induced activity in hilar neurons in the guinea pig hippocampal slice. J. Neurophysiol. 1991;65:141–147
  45. Nadler JV, Perry BW, Gentry C, Cotman CW. Fate of the hippocampal mossy fiber projection after destruction of its postsynaptic targets with intraventricular kainic acid. J. Comp. Neurol. 1981;196:549–569
  46. 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;13:4470–4485
  47. Ribak CE, Seress L. Five types of basket cell in the hippocampal dentate gyrus: a combined Golgi and electron microscopic study. J. Neurocytol. 1983;12:577–597
  48. Scharfman HE, Schwartzkroin PA. Responses of cells of the rat fascia dentata to prolonged stimulation of the perforant path: sensitivity of hilar cells and changes in granule cell excitability. Neuroscience. 1990;35:491–504
  49. 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
  50. Sloviter RS. ‘Epileptic’ brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain. Res. Bull. 1983;10:675–697
  51. Sloviter RS. Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science. 1987;235:73–76
  52. 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
  53. Sloviter RS, Brisman JL. Lateral inhibition and granule cell synchrony in the rat hippocampal dentate gyrus. J. Neurosci. 1995;15:811–820
  54. Somogyi P, Hodgson AJ, Smith AD, Nunzi MG, Gorio A, Wu J-Y. Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin-immunoreactive material. J. Neurosci. 1984;4:2590–2603
  55. Soriano E, Frotscher M. Mossy cells of the rat fascia dentata are glutamate-immunoreactive. Hippocampus. 1994;4:65–69
  56. Sperk G, Marksteiner J, Gruber B, Bellmann R, Mahata M, Ortler M. Functional changes in neuropeptide Y- and somatostatin-containing neurons induced by limbic seizures in the rat. Neuroscience. 1992;50:831–846
  57. Staley KJ, Soldo BL, Proctor WR. Ionic mechanisms of neuronal excitation by inhibitory GABA-A receptors. Science. 1995;269:977–981
  58. Sutula T, Xiao-Xian H, Cavazos J, Scott G. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science. 1988;239:1147–1150
  59. Turski WA, Cavalheiro EA, Schwarz M, Czuczwar SJ, Keinrok Z, Turski L. Limbic seizures produced by pilocarpine in rats: a behavioural, electroencephalographic and neuropathological study. Behav. Brain Res. 1983;9:315–336

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Epilepsy Research
Volume 26, Issue 1 , Pages 207-218 , December 1996

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