Stimulus and potassium-induced epileptiform activity in the human dentate gyrus from patients with and without hippocampal sclerosis

Journal of Neuroscience

Volumn 24, Issue 46, 2004, Pages 10416-10430

  Gabriel, Siegrun ^a   Njunting, Marleisje ^a   Pomper, Joern K ^a   Merschhemke, Martin ^c   Sanabria, Emilio R G ^d   Eilers, Alexander ^a   Kivi, Anatol ^a   Zeller, Melanie ^a   Meencke, Heinz Joachim ^c   Cavalheiro, Esper A ^d   Heinemann, Uwe ^a   Lehmann, Thomas Nicolas ^a,b  

^a Institute of Physiology   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c Evangelisches Krankhs Konigin E H   (Germany)

^d FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Ammon's horn sclerosis; Bicuculline; High potassium; Hippocampus; Ictaform events; Mesial temporal lobe epilepsy; Mossy fiber sprouting

Indexed keywords

CALCIUM ION; POTASSIUM ION;

ADULT; ARTICLE; BRAIN SLICE; DENTATE GYRUS; EPILEPTIC DISCHARGE; GRANULE CELL; HIPPOCAMPUS; HUMAN; MAJOR CLINICAL STUDY; MOSSY FIBER; PRIORITY JOURNAL; SCLEROSIS; SEIZURE THRESHOLD; TEMPORAL LOBE EPILEPSY;

ADULT; CALCIUM; DENTATE GYRUS; ELECTROPHYSIOLOGY; EPILEPSY, TEMPORAL LOBE; EXCITATORY AMINO ACID ANTAGONISTS; EXTRACELLULAR FLUID; FLUOROMETRY; HIPPOCAMPUS; HUMANS; MOSSY FIBERS, HIPPOCAMPAL; NEURONS; POTASSIUM; RECEPTORS, GLUTAMATE; SCLEROSIS; SYNAPSES;

EID: 20844458948     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2074-04.2004     Document Type: Article

References (88)

1. Babb TL, Brown WJ, Pretorius JK, Davenport CJ, Lieb JP, Crandall PH (1984) Temporal lobe volumetric cell densities in temporal lobe epilepsy. Epilepsia 25:729-740.
2. Babb TL, Kupfer WR, Pretorius JK, Crandall PH, Lévesque MF (1991) Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience 42:351-363.
3. Babb TL, Mathern GW, Leite JP, Pretorius JK, Yeoman KM, Kuhlman PA (1996) Glutamate AMPA receptors in the fascia dentata of human and kainate rat hippocampal epilepsy. Epilepsy Res 26:193-205.
4. Baumgartner C, Elger CE, Hufnagel A, Oppel F, Runge U, Schramm J, Stefan H, Steinhoff BJ, Wieser HG, Zentner J (2000) Qualitätsrichtlinien auf dem Gebiet der prächirurgischen Epilepsiediagnostik und operativen Epilepsietherapie. Akt Neurol 27:88-89.
5. Beck H, Blümcke I, Kral T, Clusmann H, Schramm J, Wiestler OD, Heinemann U, Elger CE (1996) Properties of a delayed rectifier potassium current in dentate granule cells isolated from the hippocampus of patients with chronic temporal lobe epilepsy. Epilepsia 37:892-901.
6. Bordey A, Spencer DD (2004) Distinct electrophysiological alterations in dentate gyrus versus CA1 glial cells from epileptic humans with temporal lobe sclerosis. Epilepsy Res 59:107-122.
7. Bragin A, Engel Jr J, Wilson CL, Fried I, Mathern GW (1999) Hippocampal and entorhinal cortex high-frequency oscillations (100-500 Hz) in human epileptic brain and in kainic acid-treated rats with chronic seizures. Epilepsia 40:127-137.
8. Bragin A, Wilson CL, Engel Jr J (2000) Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clusters: a hypothesis. Epilepsia 41 [Suppl 6]:S144-S152.
9. Buckmaster PS, Zhang GF, Yamawaki R (2002) Axon sprouting in a model of temporal lobe epilepsy creates a predominantly excitatory feedback circuit. J Neurosci 22:6650-6658.
10. Cavazos JE, Zhang PS, Qazi R, Sutula TP (2003) Ultrastructural features of sprouted mossy fiber synapses in kindled and kainic acid-treated rats. J Comp Neurol 458:272-292.
11. Cohen I, Navarro V, Clemenceau S, Baulac M, Miles R (2002) On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298:1418-1421.
12. Cronin J, Obenaus A, Houser CR, Dudek FE (1992) Electrophysiology of dentate granule cells after kainate-induced synaptic reorganization of the mossy fibers. Brain Res 573:305-310.
13. de Lanerolle NC, Kim JH, Robbins RJ, Spencer DD (1989) Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 495:387-395.
14. de Lanerolle NC, Brines M, Williamson A, Kim JH, Spencer DD (1992) Neurotransmitters and their receptors in human temporal lobe epilepsy. Epilepsy Res Suppl 7:235-250.
15. de Lanerolle NC, Kim JH, Williamson A, Spencer SS, Zaveri HP, Eid T, Spencer DD (2003) A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories. Epilepsia 44:677-687.
16. Dreier JP, Heinemann U (1991) Regional and time dependent variations of low magnesium induced epileptiform activity in rat temporal cortex. Exp Brain Res 87:581-596.
17. El Bahh B, Lespinet V, Lurton D, Coussemacq M, Le Gal LS, Rougier A (1999) Correlations between granule cell dispersion, mossy fiber sprouting, and hippocampal cell loss in temporal lobe epilepsy. Epilepsia 40:1393-1401.
18. Engel Jr J (1987a) New concepts of the epileptic focus. In: The epileptic focus (Wieser HG, Speckmann E-J, Engel Jr J, eds), pp 83-94. London: Libbey.
19. Engel Jr J (1987b) Outcome with respect to epileptic seizures. In: Surgical treatment of the epilepsies (Engel Jr J, ed), pp 553-572. New York: Raven.
20. Engel Jr J (1990) The Hans Berger Lecture: functional explorations of the human epileptic brain and their therapeutic implications. Electroencephalogr Clin Neurophysiol 76:296-316.
21. European Federation of Neurological Societies Task Force (2000) Presurgical evaluation for epilepsy surgery-European standards. Eur J Neurol 7:119-122.
22. Franck JE, Pokorny J, Kunkel DD, Schwartzkroin PA (1995) Physiologic and morphologic characteristics of granule cell circuitry in human epileptic hippocampus. Epilepsia 36:543-558.
23. Furtinger S, Pirker S, Czech T, Baumgartner C, Ransmayr G, Sperk G (2001) Plasticity of Y1 and Y2 receptors and neuropeptide Y fibers in patients with temporal lobe epilepsy. J Neurosci 21:5804-5812.
24. 0 and field potentials in dentate gyrus and area CA1 of human epileptic hippocampus. Neurosci Lett 249:91-94.
25. Hardison JL, Okazaki MM, Nadler JV (2000) Modest increase in extracellular potassium unmasks effect of recurrent mossy fiber growth. J Neurophysiol 84:2380-2389.
26. Houser CR, Miyashiro JE, Swartz BE, Walsh GO, Rich JR, Delgado-Escueta AV (1990) Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J Neurosci 10:267-282.
27. Isokawa M, Fried I (1996) Extracellular slow negative transient in the dentate gyrus of human epileptic hippocampus in vitro. Neuroscience 72:31-37.
28. Isokawa M, Lévesque MF, Babb TL, Engel Jr J (1993) Single mossy fiber axonal systems of human dentate granule cells studied in hippocampal slices from patients with temporal lobe epilepsy. J Neurosci 13:1511-1522.
29. Isokawa M, Lévesque MF, Fried I, Engel Jr J (1997) Glutamate currents in morphologically identified human dentate granule cells in temporal lobe epilepsy. J Neurophysiol 77:3355-3369.
30. - accumulation and depletion in cultured rat midbrain neurons. J Neurosci 19:4695-4704.
31. Jones RSG, Heinemann U (1987) Abolition of the orthodromically evoked IPSP of CA1 pyramidal cells before the EPSP during washout of calcium from hippocampal slices. Exp Brain Res 65:676-680.
32. Jones RSG, Lambert JDC (1990) The role of excitatory amino acid receptors in the propagation of epileptiform discharges from the entorhinal cortex to the dentate gyrus in vitro. Exp Brain Res 80:310-322.
33. Kim JH, Guimaraes PO, Shen MY, Masukawa LM, Spencer DD (1990) Hippocampal neuronal density in temporal lobe epilepsy with and without gliomas. Acta Neuropathol Berl 80:41-45.
34. King D, Bronen RA, Spencer DD, Spencer SS (1997) Topographic distribution of seizure onset and hippocampal atrophy: relationship between MRI and depth EEG. Electroencephalogr Clin Neurophysiol 103:692-697.
35. o in human epileptic non-sclerotic and sclerotic hippocampal area CA1. Eur J Neurosci 12:2039-2048.
36. Lehmann TN, Gabriel S, Kovacs R, Eilers A, Kivi A, Schulze K, Lanksch WR, Meencke HJ, Heinemann U (2000) Alterations of neuronal connectivity in area CA1 of hippocampal slices from temporal lobe epilepsy patients and from pilocarpine-treated epileptic rats. Epilepsia 41 [Suppl 6]:S190-S194.
37. Lehmann T-N, Gabriel S, Eilers A, Njunting M, Kovacs R, Schulze K, Lanksch WR, Heinemann U (2001) Fluorescent tracer in pilocarpine-treated rats shows widespread aberrant hippocampal neuronal activity. Eur J Neurosci 14:83-95.
38. Lothman EW, Stringer JL, Bertram EH (1992) The dentate gyrus as a control point for seizures in the hippocampus and beyond. In: The dentate gyrus and its role in seizures (Ribak CE, Gall CM, Mody I, eds), pp 273-280. Amsterdam: Elsevier Science.
39. Lurton D, El Bahh B, Sundström LE, Rougier A (1998) Granule cell dispersion is correlated with early epileptic events in human temporal lobe epilepsy. J Neurol Sci 154:133-136.
40. o in cat cortex. Exp Brain Res 17:190-205.
41. Lynch M, Sutula T (2000) Recurrent excitatory connectivity in the dentate gyrus of kindled and kainic acid-treated rats. J Neurophysiol 83:693-704.
42. Maglóczky Z, Wittner L, Borhegyi Z, Halász P, Vajda J, Czirják S, Freund TF (2000) Changes in the distribution and connectivity of interneurons in the epileptic human dentate gyrus. Neuroscience 96:7-25.
43. Masukawa LM, Higashima M, Kim JH, Spencer DD (1989) Epileptiform discharges evoked in hippocampal brain slices from epileptic patients. Brain Res 493:168-174.
44. Masukawa LM, Uruno K, Sperling MR, O'Connor MJ, Burdette LJ (1992) The functional relationship between antidromically evoked field responses of the dentate gyrus and mossy fiber reorganization in temporal lobe epileptic patients. Brain Res 579:119-127.
45. Masukawa LM, O'Connor WM, Lynott J, Burdette LJ, Uruno K, McGonigle P, O'Connor MJ (1995) Longitudinal variation in cell density and mossy fiber reorganization in the dentate gyrus from temporal lobe epileptic patients. Brain Res 678:65-75.
46. Masukawa LM, Wang HW, O'Connor MJ, Uruno K (1996) Prolonged field potentials evoked by 1 Hz stimulation in the dentate gyrus of temporal lobe epileptic human brain slices. Brain Res 721:132-139.
47. Masukawa LM, O'Connor WM, Burdette LJ, McGonigle P, Sperling MR, O'Connor MJ, Uruno K (1997) Mossy fiber reorganization and its possible physiological consequences in the dentate gyrus of epileptic humans. Adv Neurol 72:53-68.
48. Masukawa LM, Burdette LJ, McGonigle P, Wang H, O'Connor W, Sperling MR, O'Connor MJ, Uruno K (1999) Physiological and anatomical correlates of the human dentate gyrus: consequences or causes of epilepsy. Adv Neurol 79:781-794.
49. Mathern GW, Babb TL, Pretorius JK, Leite JP (1995) Reactive synaptogenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. J Neurosci 15:3990-4004.
50. Mathern GW, Kuhlman PA, Mendoza D, Pretorius JK (1997a) Human fascia dentata anatomy and hippocampal neuron densities differ depending in the epileptic syndrome and age at first seizure. J Neuropathol Exp Neurol 56:199-212.
51. Mathern GW, Pretorius JK, Kornblum HI, Mendoza D, Lozada A, Leite JP, Chimelli LMC, Fried I, Sakamoto AC, Assirati JA, Lévesque MF, Adelson PD, Peacock WJ (1997b) Human hippocampal AMPA and NMDA mRNA levels in temporal lobe epilepsy patients. Brain 120:1937-1959.
52. Mathern GW, Pretorius JK, Mendoza D, Leite JP, Chimelli L, Born DE, Fried I, Assirati JA, Ojemann GA, Adelson PD, Cahan LD, Kornblum HI (1999) Hippocampal N-methyl-D-aspartate receptor subunit mRNA levels in temporal lobe epilepsy patients. Ann Neurol 46:343-358.
53. Mello LEAM, Cavalheiro EA, Tan AM, Kupfer WR, Pretorius JK, Babb TL, Finch DM (1993) Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34:985-995.
54. Mikuni N, Babb TL, Wylie C, Ying Z (2000) NMDAR1 receptor proteins and mossy fibers in the fascia dentata during rat kainate hippocampal epileptogenesis. Exp Neurol 163:271-277.
55. Misgeld U, Deisz RA, Dodt HU, Lux HD (1986) The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science 232:1413-1415.
56. Molnar P, Nadler JV (1999) Mossy fiber-granule cell synapses in the normal and epileptic rat dentate gyrus studied with minimal laser photostimulation. J Neurophysiol 82:1883-1894.
57. 2+ influx because of a loss of calbindin-D(28k) in temporal lobe epilepsy. J Neurosci 20:1831-1836.
58. Okazaki MM, Nadler JV (2001) Glutamate receptor involvement in dentate granule cell epileptiform activity evoked by mossy fiber stimulation. Brain Res 915:58-69.
59. Okazaki MM, Molnar P, Nadler JV (1999) Recurrent mossy fiber pathway in rat dentate gyrus: synaptic currents evoked in presence and absence of seizure-induced growth. J Neurophysiol 81:1645-1660.
60. Pan E, Stringer JL (1997) Role of potassium and calcium in the generation of cellular bursts in the dentate gyrus. J Neurophysiol 77:2293-2299.
61. Patrylo PR, Dudek FE (1998) Physiological unmasking of new glutamatergic pathways in the dentate gyrus of hippocampal slices from kainate-induced epileptic rats. J Neurophysiol 79:418-429.
62. Patrylo PR, Schweitzer JS, Dudek FE (1994) Potassium-dependent prolonged field bursts in the dentate gyrus: effects of extracellular calcium and amino acid receptor antagonists. Neuroscience 61:13-19.
63. Patrylo PR, Schweitzer JS, Dudek FE (1999a) Abnormal responses to perforant path stimulation in the dentate gyrus of slices from rats with kainate-induced epilepsy and mossy fiber reorganization. Epilepsy Res 36:31-42.
64. Patrylo PR, Van den Pol AN, Spencer DD, Williamson A (1999b) NPY inhibits glutamatergic excitation in the epileptic human dentate gyrus. J Neurophysiol 82:478-483.
65. Remy S, Gabriel S, Urban BW, Dietrich D, Lehmann TN, Elger CE, Heinemann U, Beck H (2003) A novel mechanism underlying drug resistance in chronic epilepsy. Ann Neurol 53:469-479.
66. Scharfman HE, Sollas AL, Berger RE, Goodman JH (2003) Electrophysiological evidence of monosynaptic excitatory transmission between granule cells after seizure-induced mossy fiber sprouting. J Neurophysiol 90:2536-2547.
67. Scheibel ME, Crandall PH, Scheibel AB (1974) The hippocampal dentate complex in temporal lobe epilepsy. Epilepsia 15:55-80.
68. Schweitzer JS, Williamson A (1995) Relationship between synaptic activity and prolonged field bursts in the dentate gyrus of the rat hippocampal slice. J Neurophysiol 74:1947-1952.
69. Schweitzer JS, Patrylo PR, Dudek FE (1992) Prolonged field bursts in the dentate gyrus: dependence on low calcium, high potassium, and nonsynaptic mechanisms. J Neurophysiol 68:2016-2025.
70. Staba RJ, Wilson CL, Bragin A, Fried I, Engel Jr J (2002) Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J Neurophysiol 88:1743-1752.
71. Sutula TP, Cascino G, Cavazos JE, Parada I, Ramirez L (1989) Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 26:321-330.
72. Swanson TH, Sperling MR, O'Connor MJ (1998) Strong paired pulse depression of dentate granule cells in slices from patients with temporal lobe epilepsy. J Neural Transm 105:613-625.
73. Tauck DL, Nadler JV (1985) Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 5:1016-1022.
74. Urban L, Aitken PG, Crain BJ, Friedman AH, Somjen GG (1993) Correlation between function and structure in "epileptic" human hippocampal tissue maintained in vitro. Epilepsia 34:54-60.
75. Uruno K, O'Connor MJ, Masukawa LM (1994) Alterations of inhibitory synaptic responses in the dentate gyrus of temporal lobe epileptic patients. Hippocampus 4:583-593.
76. Wenzel HJ, Woolley CS, Robbins CA, Schwartzkroin PA (2000) Kainic acid-induced mossy fiber sprouting and synapse formation in the dentate gyrus of rats. Hippocampus 10:244-260.
77. Williamson A, Spencer DD, Shepherd GM (1993) Comparison between the membrane and synaptic properties of human and rodent dentate granule cells. Brain Res 622:194-202.
78. Williamson A, Spencer SS, Spencer DD (1995) Depth electrode studies and intracellular dentate granule cell recordings in temporal lobe epilepsy. Ann Neurol 38:778-787.
79. Williamson A, Patrylo PR, Spencer DD (1999) Decrease in inhibition in dentate granule cells from patients with medial temporal lobe epilepsy. Ann Neurol 45:92-99.
80. Wilson CL, Khan SU, Engel Jr J, Isokawa M, Babb TL, Behnke EJ (1998) Paired pulse suppression and facilitation in human epileptogenic hippocampal formation. Epilepsy Res 31:211-230.
81. Wittner L, Magloczky Z, Borhegyi Z, Halasz P, Toth S, Eross L, Szabo Z, Freund TF (2001) Preservation of perisomatic inhibitory input of granule cells in the epileptic human dentate gyrus. Neuroscience 108:587-600.
82. Wozny C, Kivi A, Lehmann TN, Dehnicke C, Heinemann U, Behr J (2003) Comment on "On the origin of interictal activity in human temporal lobe epilepsy in vitro." Science 301:463.
83. Wuarin J-P, Dudek FE (1996) Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate- treated epileptic rats. J Neurosci 16:4438-4448.
84. Wuarin J-P, Dudek FE (2001) Excitatory synaptic input to granule cells increases with time after kainate treatment. J Neurophysiol 85:1067-1077.
85. Wyler AR, Dohan FC, Schweitzer JB, Berry AD (1992) A grading system for mesial temporal pathology (hippocampal sclerosis) from anterior temporal lobectomy. J Epilepsy 5:220-225.
86. Xiong ZQ, Stringer JL (2001) Prolonged bursts occur in normal calcium in hippocampal slices after raising excitability and blocking synaptic transmission. J Neurophysiol 86:2625-2628.
87. Ying Z, Babb TL, Comair YG, Bushey M, Touhalisky K (1998) Increased densities of AMPA GluR1 subunit proteins and presynaptic mossy fiber sprouting in the fascia dentata of human hippocampal epilepsy. Brain Res 798:239-246.
88. Zhang N, Houser CR (1999) Ultrastructural localization of dynorphin in the dentate gyrus in human temporal lobe epilepsy: a study of reorganized mossy fiber synapses. J Comp Neurol 405:472-490.