Epilepsy Research
Volume 31, Issue 1 , Pages 13-27 , June 1998

Physiological analysis of Rasmussen's encephalitis: patch clamp recordings of altered inhibitory neurotransmitter function in resected frontal cortical tissue

  • John W Gibbs III

      Affiliations

    • Department of Anatomy, Medical College of Virginia, Virginia Commonwealth University, Richmond, VA 23298-0599, USA
    • ,
  • Lawrence D Morton

      Affiliations

    • Department of Neurology, Medical College of Virginia, Virginia Commonwealth University, PO Box 980599, Richmond, VA 23298-0599, USA
    • MCV Comprehensive Epilepsy Institute of Virginia Commonwealth University, Richmond, VA 23298-0599, USA
    • ,
  • Barbara Amaker

      Affiliations

    • Department of Pathology, Medical College of Virginia, Virginia Commonwealth University, Richmond, VA 23298-0599, USA
    • ,
  • John D Ward

      Affiliations

    • Department of Neurosurgery, Medical College of Virginia, Virginia Commonwealth University, Richmond, VA 23298-0599, USA
    • MCV Comprehensive Epilepsy Institute of Virginia Commonwealth University, Richmond, VA 23298-0599, USA
    • ,
  • Kathryn L Holloway

      Affiliations

    • Department of Neurosurgery, Medical College of Virginia, Virginia Commonwealth University, Richmond, VA 23298-0599, USA
    • MCV Comprehensive Epilepsy Institute of Virginia Commonwealth University, Richmond, VA 23298-0599, USA
    • ,
  • Douglas A Coulter

      Affiliations

    • Department of Neurology, Medical College of Virginia, Virginia Commonwealth University, PO Box 980599, Richmond, VA 23298-0599, USA
    • Department of Anatomy, Medical College of Virginia, Virginia Commonwealth University, Richmond, VA 23298-0599, USA
    • MCV Comprehensive Epilepsy Institute of Virginia Commonwealth University, Richmond, VA 23298-0599, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 804 8283391; fax: +1 804 8286373; e-mail: dcoulter@gems.vcu.edu

Received 14 October 1997 ,Revised 17 December 1997 ,Accepted 13 February 1998.

References 

  1. Andrews PI, Dichter MA, Berkovic SF, Newton MR, McNamara JO. Plasmapheresis in Rasmussen's encephalitis. Neurology. 1996;46:242–246
  2. Angelotti TP, Macdonald RL. Assembly of GABAA receptors: α1ß1 and α1ß1γ2S subunits produce unique ion channels with dissimilar single-channel properties. J. Neurosci. 1993;13:1429–1440
  3. Antel JP, Rasmussen T. Rasmussen's encephalitis and the new hat. Neurology. 1996;46:9–11
  4. Ashwood TJ, Wheal HV. Loss of inhibition in the CA1 region of the kainic acid lesioned hippocampus is not associated with changes in postsynaptic responses to GABA. Brain Res. 1986;367:390–394
  5. Avoli M, Olivier A. Bursting in human epileptogenic neocortex is depressed by an by an N-methyl-D-aspartate antagonist. Neurosci. Lett. 1987;76:249–254
  6. Bormann J, Hamill OP, Sakmann B. Mechanism of anion permeation through channels gated by glycine and γ-aminobutyric acid in mouse cultured neurons. J. Physiol. London. 1987;385:243–286
  7. Buhl EH, Otis TS, Mody I. Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science. 1996;271:369–373
  8. De Deyn P, Marescau B, Macdonald RL. Epilepsy and the GABA-hypothesis: a brief review and some examples. Acta Neurol. Belgium. 1990;90:65–81
  9. De Lean A, Munson PJ, Robard D. Simultaneous analysis of families of sigmoidal curves: Application to bioassay, radioligand assay, and physiological dose-response curves. Am. J. Physiol. 1987;235:E97–E102
  10. Dreifuss FE, Penry JK, Rose SW, Kupferberg HF, Dyken P, Sato S. Serum clonazepam concentrations in children with absence seizures. Neurology. 1975;25:255–258
  11. Franck JE, Schwartzkroin PA. Do kainate lesioned hippocampi become epileptogenic?. Brain Res. 1985;329:309–313
  12. Gibbs III JW, Berkow Schroder G, Coulter DA. GABAA receptor function in developing rat thalamic reticular neurons: whole-cell recordings of GABA-mediated currents and modulation by clonazepam. J. Neurophysiol. 1996;76:2568–2579
  13. Gibbs III JW, Berkow Schroder G, Morton L, Coulter DA. Physiological analysis of Rasmussen's encephalitis: patch clamp recordings of altered inhibitory neurotransmitter function in resected frontal cortical tissue. Epilepsia (Abstract). 1996;37(Suppl. 5):79
  14. Gibbs III JW, Zhang Y-F, Kao C-Q, Holloway KL, Oh K-S, Coulter DA. Characterization of GABAA receptor function in human temporal cortical neurons. J. Neurophysiol. 1996;75:1458–1471
  15. Gibbs III JW, Shumate M, Coulter DA. Differential epilepsy- associated alterations in postsynaptic GABAA receptor function in dentate granule and CA1 neurons. J. Neurophysiol. 1997;77:1924–1938
  16. Gibbs III JW, Sombati S, DeLorenzo RJ, Coulter DA. Epileptogenesis-associated reduction in functional GABAA receptor density and benzodiazepine modulation in a hippocampal culture model of chronic spontaneous seizures. J. Neurophysiol. 1997;77:2139–2152
  17. 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
  18. Jay V, Becker LE, Otsubo H, Cortez M, Hwang P, Hoffman HJ, et al. Chronic encephalitis and epilepsy (Rasmussen's encephalitis): detection of cytomegalovirus and herpes simplex virus I by the polymerase chain reaction and in situ hybridization. Neurology. 1995;45:108–117
  19. Kamphuis W, De Rijk TC, Lopes da Silva FH. Expression of GABAA 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
  20. Kapur J, Coulter DA. Experimentally-induced status epilepticus acutely alters GABA receptor function in CA1 pyramidal neurons. Ann. Neurol. 1995;38:893–900
  21. Kapur J, Macdonald RL. Rapid seizure-induced reduction of benzodiazepine and Zn2+ sensitivity of hippocampal dentate granule cell GABAA receptors. J. Neurosci. 1997;17:7532–7540
  22. 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
  23. Kokaia M, Pratt GD, Elmer E, Bengzon J, Fritschy J-M, Kokaia Z, et al. Biphasic differential changes of GABAA receptor subunit mRNA levels in dentate gyrus granule cells following recurrent kindling-induced seizures. Mol. Brain Res. 1994;23:323–332
  24. Krauss GL, Campbell RN, Roche KW, Huganir RH, Niedermeyer E. Chronic steroid-responsive encephalitis without antibodies to glutamate receptor GluR3. Neurology. 1996;46:247–249
  25. Köhr G, Mody I. Kindling increases in N-methyl-D-aspartate potency at single N-methyl-D-aspartate channels in dentate gyrus granule cells. Neuroscience. 1994;62:975–981
  26. Lin, D.D., Shumate, M.D., Gibbs III, J.W., Holloway, K.L., Coulter, D.A., 1997. GABAAergic function of epileptic human dentate granule cells: comparison with GABA alterations evident in a rat model of temporal lobe epilepsy. Epilepsia (American Epilepsy Society Abstracts), 38 (S8), S9.
  27. 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
  28. Macdonald RW, Olsen R. GABAA receptor channels. Ann. Rev. Neurosci. 1994;17:569–602
  29. Mangan PS, Rempe DA, Lothman EW. Changes in inhibitory neurotransmission in the CA1 region and the dentate gyrus in a chronic model of temporal lobe epilepsy. J. Neurophysiol. 1995;74:829–840
  30. Martin D, McNamara JO, Nadler JV. Kindling enhances sensitivity of CA3 hippocampal pyramidal cells to NMDA. J. Neurosci. 1992;12:1928–1935
  31. McLachlan RS, Levin S, Blume WT. Treatment of Rasmussen's syndrome with ganciclovir. Neurology. 1996;47:925–928
  32. Noebels JL. Targeting epilepsy genes. Neuron. 1996;16:241–244
  33. Oh K-S, Lee C-J, Gibbs JW, Coulter DA. Postnatal development of GABAA receptor function in somatosensory thalamus and cortex: whole-cell voltage-clamp recordings in acutely isolated rat neurons. J. Neurosci. 1995;15:1341–1351
  34. Oliver MW, Miller JJ. Alteration of inhibitory processes in the dentate gyrus following kindling-induced epilepsy. Exp. Brain Res. 1985;57:443–447
  35. Power C, Poland SD, Blume WT, Girvin JP, Rice GPA. Cytomegalovirus and Rasmusssen's encephalitis. Lancet. 1990;336:1282–1284
  36. Reid SA, Palovcik RA. Spontaneous epileptiform discharges in isolated human cortical slices from epileptic patients. Neurosci. Lett. 1989;98:200–204
  37. Rempe DA, Mangan PS, Lothman EW. Regional heterogeneity of pathophysiological alterations in CA1 and dentate gyrus in a chronic model of temporal lobe epilepsy. J. Neurophysiol. 1995;74:816–828
  38. Rice AC, Rafiq A, Shapiro SM, Jakoi EM, Coulter DA, DeLorenzo RJ. Long-lasting reduction of inhibitory function and GABAA subunit mRNA expression in a model of temporal lobe epilepsy. Proc. Natl. Acad. Sci. USA. 1996;93:9665–9669
  39. Rikhter, T.Y., Zhang, Y.-F., Shumate, M.D., Morris, T.A., Blair, R.E., DeLorenzo, R.J., Coulter, D.A., 1997. Regionally distinct alterations in GABAA receptor mRNA expression in hippocampus of chronically epileptic pilocarpine-treated animals. Epilepsia (American Epilepsy Society Abstracts), 38 (S8), S9–S10.
  40. Roberts, E., 1986. Failure of GABAergic inhibition: a key to local and global seizures. In: Delgado-Escueta, A.V., Ward, A.A. Jr., Woodbury, D.M., Porter, R.J. (Eds.), Basic Mechanisms of the Epilepsies: Molecular and Cellular Approaches. Advances of Neurology, Raven Press, New York.
  41. Rogers SW, Andrews PI, Gahring LC, Whisenand T, Cauley K, Crain B, et al. Autoantibodies to glutamate receptor GluR3 in Rasmussen's encephalitis. Science. 1994;265:648–651
  42. Rogers SW, Twyman RE, Gahring LC. The role of autoimmunity to glutamate receptors in neurological disease. Mol. Med. Today. 1996;2:76–81
  43. Rogers SW. Central nervous system autoimmunity in human diseases. Soc. Neurosci. Abstr. 1996;22:489
  44. Schwartzkroin PA, Knowles WD. Intracellular study of human epileptic cortex: in vitro maintenance of epileptiform activity?. Science. 1984;223:709–712
  45. Schwartzkroin PA, Turner DA, Knowles WD, Wyler AR. Studies of human and monkey `epileptic' neocortex in the in vitro slice preparation. Ann. Neurol. 1983;13:249–257
  46. Schwarzer C, Tsunashima K, Wanzenböck C, Fuchs K, Sieghart W, Sperk G. GABAA receptor subunits in the rat hippocampus II: altered distribution in kainic acid-induced temporal lobe epilepsy. Neuroscience. 1997;80:1001–1017
  47. Shumate, M.D., Lin, D.D, Gibbs III, J.W., Holloway, K.L., Coulter, D.A. 1998. GABAA receptor function in epileptic human dentate granule cells: comparison to epileptic and control rat. Epilepsy Res., in press.
  48. Sigel E, Baur R, Trube G, Möhler H, Malherbe P. The effect of subunit composition of rat brain GABAA receptors on channel function. Neuron. 1990;5:703–711
  49. Sloviter RS. Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci. Lett. 1992;137:91–96
  50. Stelzer A, Slater NT, ten Bruggencate G. Activation of NMDA receptors blocks GABAergic inhibition in an in vitro model of epilepsy. Nature. 1987;326:698–701
  51. Tauck DL, Nadler JV. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 1985;5:1016–1022
  52. Titulaer MNG, Kamphuis W, Pool CW, van Heerikhuize JJ, Lopes da Silva FH. Kindling induces time-dependent and regional specific changes in the [3H]muscimol binding in the rat hippocampus: a quantitative autoradiographic study. Neuroscience. 1994;59:817–826
  53. Titulaer MNG, Ghijsen WEJM, Kamphius W, De Rijk TC, Lopes da Silva FH. Opposite changes in GABAA receptor function in the CA1–3 area and fascia dentata of kindled rat hippocampus. J. Neurochem. 1985;64:2615–2621
  54. Tsunashima K, Schwarzer C, Kirchmair E, Sieghart W, Sperk G. GABAA receptor subunits in the rat hippocampus III: altered messenger RNA expression in kainic acid-induced epilepsy. Neuroscience. 1997;80:1019–1032
  55. Twyman RE, Gahring LC, Spiess J, Rogers SW. Glutamate receptor antibodies activate a subset of receptors and reveal an agonist binding site. Neuron. 1995;14:755–762
  56. Villemure, J.-G., Andermann, F., Rasmussen, T.B., 1998. Hemispherectomy for the treatment of epilepsy due to chronic encephalitis. In: Andermann, F. (Ed.), Chronic Encephalitis and Epilepsy: Rasmussen's Syndrome. Butterworth-Heinemann, Boston, pp. 235–241.
  57. Walton NY, Treiman DM. Response of status epilepticus induced by lithium and pilocarpine to treatment with diazepam. Exp. Neurol. 1988;108:61–70

PII: S0920-1211(98)00009-6

Epilepsy Research
Volume 31, Issue 1 , Pages 13-27 , June 1998

Article Tools

* Image Usage & Resolution