In vivo laminar electrophysiology co-registered with histology in the hippocampus of patients with temporal lobe epilepsy

Experimental Neurology

Volumn 187, Issue 2, 2004, Pages 310-318

  Ulbert, István ^a,b   Maglóczky, Zsófia ^c   Eross, Loránd ^d   Czirják, Sándor ^e   Vajda, János ^e   Bognár, László ^e   Tóth, Szabolcs ^d   Szabó, Zerind ^d   Halász, Péter ^f   Fabó, Dániel ^f   Halgren, Eric ^b,g   Freund, Tamás F ^c   Karmos, George ^a  

^a INSTITUTE FOR PSYCHOLOGY   (Hungary)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^d MAV Hospital   (Hungary)

^e NATIONAL INSTITUTE OF NEUROSURGERY   (Hungary)

^f NATIONAL INSTITUTE OF PSYCHIATRY AND NEUROLOGY   (Hungary)

^g INSERM   (France)

Author keywords

Bursting unit; CA1; DG; Hippocampus; Histology; Human; Interictal spike; Laminar electrophysiology; Temporal lobe epilepsy

Indexed keywords

ANESTHESIA; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CLINICAL ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; ELECTRIC POTENTIAL; ELECTRODE; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTRAOPERATIVE PERIOD; MALE; OSCILLATION; PRIORITY JOURNAL; SCHOOL CHILD; TEMPORAL CORTEX; TEMPORAL LOBE EPILEPSY; TEMPORAL LOBECTOMY;

ACTION POTENTIALS; ADOLESCENT; ELECTRODES, IMPLANTED; ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGY; EPILEPSY, TEMPORAL LOBE; HIPPOCAMPUS; HUMANS; INTRAOPERATIVE PERIOD; MALE; MICROELECTRODES; MIDDLE AGED; NEUROSURGICAL PROCEDURES; SEIZURES;

EID: 2342494764     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2003.12.003     Document Type: Article

References (55)

1. Alarcon G., Garcia Seoane J.J., Binnie C.D., Martin Miguel M.C., Juler J., Polkey C.E., Elwes R.D., Ortiz Blasco J.M. Origin and propagation of interictal discharges in the acute electrocorticogram. Implications for pathophysiology and surgical treatment of temporal lobe epilepsy. Brain. 120(Pt 12):1997;2259-2282
2. Amaral D.G., Insausti R. Hippocampal Formation. 1990;Academic Press, New York
3. Babb T.L., Carr E., Crandall P.H. Analysis of extracellular firing patterns of deep temporal lobe structures in man. Electroencephalogr. Clin. Neurophysiol. 34:1973;247-257
4. Babb T.L., Wilson C.L., Isokawa-Akesson M. Firing patterns of human limbic neurons during stereoencephalography (SEEG) and clinical temporal lobe seizures. Electroencephalogr. Clin. Neurophysiol. 66:1987;467-482
5. Barna J.S., Arezzo J.C., Vaughan H.G. Jr. A new multielectrode array for the simultaneous recording of field potentials and unit activity. Electroencephalogr. Clin. Neurophysiol. 52:1981;494-496
6. Bodizs R., Kantor S., Szabo G., Szucs A., Eross L., Halasz P. Rhythmic hippocampal slow oscillation characterizes REM sleep in humans. Hippocampus. 11:2001;747-753
7. Bragin A., Csicsvari J., Penttonen M., Buzsaki G. Epileptic afterdischarge in the hippocampal-entorhinal system: current source density and unit studies. Neuroscience. 76:1997;1187-1203
8. Bragin A., Hetke J., Wilson C.L., Anderson D.J., Engel J. Jr., Buzsaki G. Multiple site silicon-based probes for chronic recordings in freely moving rats: implantation, recording and histological verification. J. Neurosci. Methods. 98:2000;77-82
9. Bragin A., Wilson C.L., Engel J. Jr. Rate of interictal events and spontaneous seizures in epileptic rats after electrical stimulation of hippocampus and its afferents. Epilepsia. 43(Suppl. 5):2002;81-85
10. Bragin A., Wilson C.L., Staba R.J., Reddick M., Fried I., Engel J. Jr. Interictal high-frequency oscillations (80-500 Hz) in the human epileptic brain: entorhinal cortex. Ann. Neurol. 52:2002;407-415
11. Buckmaster P.S., Zhang G.F., Yamawaki R. Axon sprouting in a model of temporal lobe epilepsy creates a predominantly excitatory feedback circuit. J. Neurosci. 22:2002;6650-6658
12. Buzsaki G., Czopf J., Kondakor I., Kellenyi L. Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: current-source density analysis, effects of urethane and atropine. Brain Res. 365:1986;125-137
13. Caplan J.B., Madsen J.R., Schulze-Bonhage A., Aschenbrenner-Scheibe R., Newman E.L., Kahana M.J. Human theta oscillations related to sensorimotor integration and spatial learning. J. Neurosci. 23:2003;4726-4736
14. Cohen I., Navarro V., Clemenceau S., Baulac M., Miles R. On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science. 298:2002;1418-1421
15. Cohen A.S., Lin D.D., Quirk G.L., Coulter D.A. Dentate granule cell GABA(A) receptors in epileptic hippocampus: enhanced synaptic efficacy and altered pharmacology. Eur. J. Neurosci. 17:2003;1607-1616
16. Colder B.W., Wilson C.L., Frysinger R.C., Chao L.C., Harper R.M., Engel J. Jr. Neuronal synchrony in relation to burst discharge in epileptic human temporal lobes. J. Neurophysiol. 75:1996;2496-2508
17. Csicsvari J., Jamieson B., Wise K.D., Buzsaki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron. 37:2003;311-322
18. de Lanerolle N.C., Eid T., von Campe G., Kovacs I., Spencer D.D., Brines M. Glutamate receptor subunits GluR1 and GluR2/3 distribution shows reorganization in the human epileptogenic hippocampus. Eur. J. Neurosci. 10:1998;1687-1703
19. Duvernoy H.M. The Human Hippocampus. 1998;Springer-Verlag, Berlin
20. Freeman J.A., Nicholson C. Experimental optimization of current source-density technique for anuran cerebellum. J. Neurophysiol. 38:1975;369-382
21. Halgren E. Firing of human hippocampal units in relation to voluntary movements. Hippocampus. 1:1991;153-161
22. Halgren E., Babb T.L., Crandall P.H. Activity of human hippocampal formation and amygdala neurons during memory testing. Electroencephalogr. Clin. Neurophysiol. 45:1978;585-601
23. Henze D.A., Borhegyi Z., Csicsvari J., Mamiya A., Harris K.D., Buzsaki G. Intracellular features predicted by extracellular recordings in the hippocampus in vivo. J. Neurophysiol. 84:2000;390-400
24. Herrick I.A., Craen R.A., Gelb A.W., McLachlan R.S., Girvin J.P., Parrent A.G., Eliasziw M., Kirkby J. Propofol sedation during awake craniotomy for seizures: electrocorticographic and epileptogenic effects. Anesth. Analg. 84:1997;1280-1284
25. Hosain S., Nagarajan L., Fraser R., Van Poznak A., Labar D. Effects of nitrous oxide on electrocorticography during epilepsy surgery. Electroencephalogr. Clin. Neurophysiol. 102:1997;340-342
26. Isokawa-Akesson M., Wilson C.L., Babb T.L. Inhibition in synchronously firing human hippocampal neurons. Epilepsy Res. 3:1989;236-247
27. Kahana M.J., Seelig D., Madsen J.R. Theta returns. Curr. Opin. Neurobiol. 11:2001;739-744
28. Kobayashi M., Buckmaster P.S. Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy. J. Neurosci. 23:2003;2440-2452
29. Leijten F.S., Teunissen N.W., Wieneke G.H., Knape J.T., Schobben A.F., van Huffelen A.C. Activation of interictal spiking in mesiotemporal lobe epilepsy by propofol-induced sleep. J. Clin. Neurophysiol. 18:2001;291-298
30. Lim C., Blume H.W., Madsen J.R., Saper C.B. Connections of the hippocampal formation in humans: I. The mossy fiber pathway. J. Comp. Neurol. 385:1997;325-351
31. Lim C., Mufson E.J., Kordower J.H., Blume H.W., Madsen J.R., Saper C.B. Connections of the hippocampal formation in humans: II. The endfolial fiber pathway. J. Comp. Neurol. 385:1997;352-371
32. Magloczky Z., Wittner L., Borhegyi Z., Halasz P., Vajda J., Czirjak S., Freund T.F. Changes in the distribution and connectivity of interneurons in the epileptic human dentate gyrus. Neuroscience. 96:2000;7-25
33. Manninen P.H., Burke S.J., Wennberg R., Lozano A.M., El Beheiry H. Intraoperative localization of an epileptogenic focus with alfentanil and fentanyl. Anesth. Analg. 88:1999;1101-1106
34. Margerison J.H., Corsellis J.A. Epilepsy and the temporal lobes. A clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain. 89:1966;499-530
35. McGuire G., El-Beheiry H., Manninen P., Lozano A., Wennberg R. Activation of electrocorticographic activity with remifentanil and alfentanil during neurosurgical excision of epileptogenic focus. Br. J. Anaesth. 91:2003;651-655
36. McKhann G.M. II, Schoenfeld-McNeill J., Born D.E., Haglund M.M., Ojemann G.A. Intraoperative hippocampal electrocorticography to predict the extent of hippocampal resection in temporal lobe epilepsy surgery. J. Neurosurg. 93:2000;44-52
37. Mehta A.D., Ulbert I., Schroeder C.E. Intermodal selective attention in monkeys. I: Distribution and timing of effects across visual areas. Cereb. Cortex. 10:2000;343-358
38. Mehta A.D., Ulbert I., Schroeder C.E. Intermodal selective attention in monkeys. II: Physiological mechanisms of modulation. Cereb. Cortex. 10:2000;359-370
39. Nicholson C., Freeman J.A. Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. J. Neurophysiol. 38:1975;356-368
40. O'Keefe J., Burgess N. Theta activity, virtual navigation and the human hippocampus. Trends Cogn. Sci. 3:1999;403-406
41. Polkey C.E., Binnie C.D., Janota I. Acute hippocampal recording and pathology at temporal lobe resection and amygdalo-hippocampectomy for epilepsy. J. Neurol. Neurosurg. Psychiatry. 52:1989;1050-1057
42. Prince D.A., Jacobs K. Inhibitory function in two models of chronic epileptogenesis. Epilepsy Res. 32:1998;83-92
43. Ravagnati L., Halgren E., Babb T.L., Crandall P.H. Activity of human hippocampal formation and amygdala neurons during sleep. Sleep. 2:1979;161-173
44. Staba R.J., Wilson C.L., Bragin A., Fried I., Engel J. Jr. Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J. Neurophysiol. 88:2002;1743-1752
45. Staba R.J., Wilson C.L., Fried I., Engel J. Jr. Single neuron burst firing in the human hippocampus during sleep. Hippocampus. 12:2002;724-734
46. Sutula T., Cascino G., Cavazos J., Parada I., Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 26:1989;321-330
47. Towers S.K., LeBeau F.E., Gloveli T., Traub R.D., Whittington M.A., Buhl E.H. Fast network oscillations in the rat dentate gyrus in vitro. J. Neurophysiol. 87:2002;1165-1168
48. Tran T.A., Spencer S.S., Marks D., Javidan M., Pacia S., Spencer D.D. Significance of spikes recorded on electrocorticography in nonlesional medial temporal lobe epilepsy. Ann. Neurol. 38:1995;763-770
49. Ulbert I., Halgren E., Heit G., Karmos G. Multiple microelectrode- recording system for human intracortical applications. J. Neurosci. Methods. 106:2001;69-79
50. Ulbert I., Karmos G., Heit G., Halgren E. Early discrimination of coherent versus incoherent motion by multiunit and synaptic activity in human putative MT+. Hum. Brain Mapp. 13:2001;226-238
51. Williamson A., Spencer S.S., Spencer D.D. Depth electrode studies and intracellular dentate granule cell recordings in temporal lobe epilepsy. Ann. Neurol. 38:1995;778-787
52. Williamson A., Telfeian A.E., Spencer D.D. Prolonged GABA responses in dentate granule cells in slices isolated from patients with temporal lobe sclerosis. J. Neurophysiol. 74:1995;378-387
53. Williamson A., Patrylo P.R., Spencer D.D. Decrease in inhibition in dentate granule cells from patients with medial temporal lobe epilepsy. Ann. Neurol. 45:1999;92-99
54. Wittner L., Magloczky Z., Borhegyi Z., Halasz P., Toth S., Eross L., Szabo Z., Freund T.F. Preservation of perisomatic inhibitory input of granule cells in the epileptic human dentate gyrus. Neuroscience. 108:2001;587-600
55. Wyler A.R., Ojemann G.A., Ward A.A. Jr. Neurons in human epileptic cortex: correlation between unit and EEG activity. Ann. Neurol. 11:1982;301-308