Epilepsy Research
Volume 31, Issue 3 , Pages 211-230 , August 1998

Paired pulse suppression and facilitation in human epileptogenic hippocampal formation

  • C.L Wilson

      Affiliations

    • Department of Neurology, 2155 Reed Neurological Research Center, UCLA School of Medicine, Los Angeles, CA 90024, USA
    • The Brain Research Institute, Center for the Health Sciences, University of California, Los Angeles CA 90095, USA
    • Reed Neurological Research Center, Center for the Health Sciences, University of California, Los Angeles CA 90095, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 310 8250576; fax: +1 310 2068461; e-mail: clwilson@ucla.edu
    • ,
  • S.U Khan

      Affiliations

    • Department of Neurobiology, Center for the Health Sciences, University of California, Los Angeles, CA 90095 USA
    • ,
  • J Engel Jr.

      Affiliations

    • Department of Neurology, 2155 Reed Neurological Research Center, UCLA School of Medicine, Los Angeles, CA 90024, USA
    • Department of Neurobiology, Center for the Health Sciences, University of California, Los Angeles, CA 90095 USA
    • The Brain Research Institute, Center for the Health Sciences, University of California, Los Angeles CA 90095, USA
    • Reed Neurological Research Center, Center for the Health Sciences, University of California, Los Angeles CA 90095, USA
    • ,
  • M Isokawa

      Affiliations

    • The Brain Research Institute, Center for the Health Sciences, University of California, Los Angeles CA 90095, USA
    • ,
  • T.L Babb

      Affiliations

    • Departments of Neuroscience and Neurology, The Cleveland Clinic Foundation, Cleveland, OH 44195, USA
    • ,
  • E.J Behnke

      Affiliations

    • The Brain Research Institute, Center for the Health Sciences, University of California, Los Angeles CA 90095, USA

Received 10 April 1998 ,Revised 11 May 1998 ,Accepted 11 May 1998.

References 

  1. Amaral DG. A Golgi study of cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 1978;182:851–914
  2. Babb TL, Kupfer WR. Phagocytic and metabolic reactions to intracerebral electrical stimulation of rat brain. Exp. Neurol. 1984;86:183–197
  3. Babb TL, Brown WJ, Pretorius J, Davenport C, Lieb JP, Crandall PH. Temporal lobe volumetric cell densities in temporal lobe epilepsy. Epilepsia. 1984;25:729–740
  4. Babb TL, Mariani E, Seidner KA, Mutafyan G, Halgren E, Wilson CL, et al. A circuit for safe diagnostic electrical stimulation of the human brain. Neurol. Res. 1980;2:181–197
  5. Babb TL, Pretorius JK, Kupfer WR, Crandall PH. Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus. J. Neurosci. 1989;9:2562–2574
  6. Bekenstein JW, Lothman EW. Electrophysiological characterization of associational pathway termination on dentate gyrus granule cells in the rat. Hippocampus. 1991;1:399–404
  7. Braak E, Strotkamp B, Braak H. Parvalbumin-immunoreactive structures in the hippocampus of the human adult. Cell Tissue Res. 1991;264:33–48
  8. Buckmaster PS, Dudek FE. Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J. Comp. Neurol. 1997;385:385–404
  9. Buzsáki G. Feed-forward inhibition in the hippocampal formation. Prog. Neurobiol. 1984;22:131–153
  10. Cornish SM, Wheal HV. Long-term loss of paired pulse inhibition in the kainic acid-lesioned hippocampus of the rat. Neuroscience. 1989;28:563–571
  11. Cronin J, Obenaus A, Houser C, Dudek FE. Electrophysiology of dentate granule cells after kainate-induced synaptic reorganization of the mossy fibers. Brain Res. 1992;573:305–310
  12. Davies CH, Davies SN, Collingridge GL. Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. J. Physiol. 1990;424:513–531
  13. Engel J. Excitation and inhibition in epilepsy. Can. J. Neurol. Sci. 1996;23:167–174
  14. Engel J, Henry TR, Risinger MW, Mazziotta JC, Sutherling WW, Lévesque MF, et al. Presurgical evaluation for partial epilepsy: relative contributions of chronic depth-electrode recordings versus FDG-PET and scalp-sphenoid ictal EEG. Neurology. 1990;40:1670–1677
  15. Esclapez M, Houser CR. Somatostatin neurons are a subpopulation of GABA neurons in the rat dentate gyrus: evidence from colocalization of pre-prosomatostatin and glutamate decarboxylase messenger RNAs. Neuroscience. 1995;64:339–355
  16. Franck JE, Schwartzkroin P. Do kainate-lesioned hippocampi become epileptogenic?. Brain Res. 1985;329:309–313
  17. Franck JE, Kunkel DD, Baskin DG, Schwartzkroin PA. Inhibition in kainate-lesioned epileptogenic hippocampi: physiologic, autoradiographic and immunocytochemical observation. J. Neurosci. 1988;8:1991–2002
  18. Goddard G, McIntyre D, Leech C. A permanent change in brain function resulting from daily electrical stimulation. Exp. Neurol. 1969;25:295–330
  19. Goodman JH, Sloviter RS. Evidence for commissurally projecting parvalbumin-immunoreactive basket cells in the dentate gyrus of the rat. Hippocampus. 1992;2:13–22
  20. Guimaraes P, Kim JH, de Lanerolle NC. A quantitative evaluation of hippocampal neuronal loss in temporal lobe epilepsy with and without primary glial tumor. J. Neuropathol. Exp. Neurol. 1988;47:372–373
  21. Henry TR, Mazziotta JC, Engel J. Christenson, P.D., Zhang, J.X., Phelps, M.E., Kuhl, D.E. 90. Quantifying interictal metabolic activity in human temporal lobe epilepsy. J. Cereb. Blood Flow Metab. 1990;100:748–757
  22. Houser CR. GABA neurons in seizure disorders: a review of immunocytochemical studies. Neurochem. Res. 1991;16:295–308
  23. Isokawa M, Fried I. Extracellular slow negative transient in the dentate gyrus of human epileptic hippocampus in vitro. Neuroscience. 1996;72:31–37
  24. Kamphius W, Lopes da Silva FH, Wadman WJ. Changes in local evoked potentials in the rat hippocampus (CA1) during kindling epileptogenesis. Brain Res. 1988;440:205–215
  25. Kamphius W, Gorter JA, Wadman WJ, Lopes da Silva FH. Hippocampal kindling leads to different changes in paired-pulse depression of local evoked field potentials in CA1 area and in fascia dentata. Neurosci. Lett. 1992;141:101–105
  26. Kapur J, Lothman EW. NMDA receptor activation mediates the loss of GABAergic inhibition induced by recurrent seizures. Epilepsy Res. 1990;5:103–111
  27. 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
  28. King GL, Dingledine R, Giacchino JL, McNamara JO. Abnormal neuronal excitability in hippocampal slices from kindled rats. J. Neurophysiol. 1985;54:1295–1304
  29. Lévesque MF, Zhang JX, Wilson CL, Behnke EJ, Harper RM, Lufkin RB, et al. Stereotactic investigation of limbic epilepsy using a multimodal image analysis system. J. Neurosurg. 1990;73:792–797
  30. Lopes da Silva, F.H., 1987. Hippocampal kindling: physiological evidence for progressive disinhibition. In: Wolf, P., Dam, M., Janz, D., Dreifuss, F.E. (Eds.), Advances in Epileptology. Raven Press, New York, pp. 57–62.
  31. Lothman EW, Bertram EH, Kapur J, Stringer JL. Recurrent spontaneous hippocampal seizures in the rat as a chronic sequela to limbic status epilepticus. Epilepsy Res. 1990;6:110–119
  32. Lothman EW, Bertram EH, Stringer JL. Functional anatomy of hippocampal seizures. Prog. Neurobiol. 1991;37:1–82
  33. Maru E, Goddard GV. Alteration in dentate neuronal activities associated with perforant path kindling. III. Enhancement of synaptic inhibition. Exp. Neurol. 1987;96:46–60
  34. Masukawa LM, Wang H, O'Connor MJ, Uruno K. Prolonged field potentials evoked by 1 Hz stimulation in the dentate gyrus of temporal lobe epileptic human brain slices. Brain Res. 1996;721:132–139
  35. 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
  36. Meier CL, Dudek FE. Spontaneous and stimulation-induced synchronized burst afterdischarges in the isolated CA1 of kainate-treated rats. J. Neurosci. 1996;76:2231–2239
  37. Milgram NW, Michael M, Cammisuli S, Head E, Ferbinteanu J, Reid C, et al. Development of spontaneous seizures over extended electrical kindling. II. Persistence of dentate inhibitory suppression. Brain Res. 1995;670:112–120
  38. 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;551:236–246
  39. Nathan T, Jensen MS, Lambert JDC. GABAB receptors play a major role in paired-pulse facilitation in area CA1 of the rat hippocampus. Brain Res. 1990;531:55–65
  40. 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
  41. Oliver MW, Miller JJ. Inhibitory processes of hippocampal CA1 pyramidal neurons following kindling-induced epilepsy in the rat. Can. J. Physiol. Pharmacol. 1985;63:872–878
  42. Rausche G, Sarvey JM, Heinemann U. Slow synaptic inhibition in relation to frequency habituation in dentate granule cells of rat hippocampal slices. Exp. Brain Res. 1989;78:233–242
  43. Ribak CE, Nitsch R, Seress LJ. Proportion of parvalbumin-positive basket cells in the GABAergic innervation of pyramidal and granule cells of the rat hippocampal formation. J. Comp. Neurol. 1990;300:449–461
  44. Rutecki PA, Grossman RG, Armstrong D, Irish-Loewen S. Electrophysiological connections between the hippocampus and entorhinal cortex in patients with complex partial seizures. J. Neurosurg. 1989;70:667–675
  45. Scharfman HE, Schwartzkroin PA. Consequences of prolonged afferent stimulation of the rat fascia dentata: epileptiform activity in area CA3 of hippocampus. Neuroscience. 1990;35:505–517
  46. Schwartzkroin, P.A., 1983. Local circuit considerations and intrinsic neuronal properties involved in hyperexcitability and cell synchronization. In: Jasper, H.H., Van Gelder, N.M. (Eds.), Basic Mechanisms of Neuronal Hyperexcitability. A.R. Liss, New York, pp. 75–108.
  47. Schwartzkroin PA, Scharfman HE, Sloviter RS. Similarities in circuitry between Ammon's horn and dentate gyrus: local interactions and parallel processing. Prog. Brain Res. 1990;83:269–286
  48. Sclabassi RJ, Eriksson JL, Port RL, Robinson GB, Berger TW. Nonlinear systems analysis of the hippocampal perforant path-dentate projection. I. Theoretical and interpretational considerations. J. Neurophysiol. 1988;60:1066–1076
  49. Shirasaka Y, Wasterlain CG. Chronic epileptogenicity following focal status epilepticus. Brain Res. 1994;655:33–44
  50. Shirasaka Y, Wasterlain CG. The effect of urethane anesthesia on evoked potentials in dentate gyrus. Eur. J. Pharmacol. 1995;282:11–17
  51. Sloviter RS. Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science. 1987;235:73–76
  52. Sloviter RS. Feedforward and feedback inhibition of hippocampal principal cell activity evoked by perforant path stimulation: GABA-mediated mechanisms that regulate excitability in vivo. Hippocampus. 1991;1:31–40
  53. 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
  54. Sloviter RS. Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci. Lett. 1992;137:91–96
  55. Sloviter RS, Lowenstein DH. Heat shock protein expression in vulnerable cells of the rat hippocampus as an indicator of excitation-induced neuronal stress. J. Neurosci. 1992;12:3004–3009
  56. Sloviter RS, Dean E, Sollas AL, Goodman JH. Apoptosis and necrosis induced in different hippocampal neuron populations by repetititve perforant path stimulation in the rat. J. Comp. Neurol. 1996;366:516–533
  57. Stringer JL, Lothman EW. Repetitive seizures cause an increase in paired-pulse inhibition in the dentate gyrus. Neurosci. Lett. 1989;105:91–95
  58. Swanson LW, Wyss JM, Cowan WM. An autoradiographic study of the organization of intra-hippocampal association pathways in the rat. J. Comp. Neurol. 1978;181:681–716
  59. Talairach, J., David, M., Tournoux, P., 1958. L'exploration Chirurgicale Stéréotaxique du Lobe Temporale dans L'épilepsie Temporale: Repérage Anatomique Stéréotaxique et Technique Chirurgicale. Masson et Cie, Paris.
  60. Tuff LP, Racine RJ, Adamec R. The effects of kindling on GABA-mediated inhibition in the dentate gyrus of the rat. I. Paired pulse depression. Brain Res. 1983;277:79–90
  61. Uruno K, O'Connor MJ, Masukawa LM. Effects of bicuculline and baclofen on paired-pulse depression in the dentate gyrus of epileptic patients. Brain Res. 1995;695:163–172
  62. Vives KP, Spencer DD, McCarthy G. In vivo paired pulse study of inhibition in the human hippocampus. Soc. Neurosci. Abstr. 1994;20:1449
  63. Williamson A, Spencer DD. Zinc reduces dentate granule cell hyperexcitability in epileptic humans. Neuroreport. 1995;6:1562–1564
  64. Williamson A, Spencer SS, Spencer DD. Depth electrode studies and intracellular dentate granule cell recordings in temporal lobe epilepsy. Ann. Neurol. 1995;38:778–787
  65. 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
  66. Wilson CL, Isokawa-Akesson M, Babb TL, Crandall PH. Functional connections in the human temporal lobe: I. Analysis of limbic system pathways using neuronal activity evoked by electrical stimulation. Exp. Brain Res. 1990;82:279–292
  67. Wilson CL, Isokawa-Akesson M, Babb TL, Lévesque MF, Engel J. Functional connnections in the human temporal lobe. II. Evidence for a loss of functional linkage between contralateral limbic structures. Exp. Brain Res. 1991;85:174–187
  68. Zhang JX, Lévesque MF, Wilson CL, Harper RM, Engel J, Lufkin R, et al. Multimodality imaging of brain structures for steroactic surgery. Radiology. 1990;175:435–441
  69. Zhao D, Leung LS. Hippocampal kindling induced paired-pulse depression in the dentate gyrus and paired-pulse facilitation in CA3. Brain Res. 1992;582:163–167

PII: S0920-1211(98)00063-1

Epilepsy Research
Volume 31, Issue 3 , Pages 211-230 , August 1998

Article Tools

* Image Usage & Resolution