In vivo neuronal firing patterns during human epileptiform discharges replicated by electrical stimulation

Clinical Neurophysiology

Volumn 123, Issue 9, 2012, Pages 1736-1744

  Alarcón, Gonzalo ^a,b   Martinez, Juan ^c   Kerai, Shashivadan V ^a   Lacruz, Maria E ^a   Quiroga, Rodrigo Quian ^c,d   Selway, Richard P ^e   Richardson, Mark P ^a   García Seoane, Jorge J ^b   Valentín, Antonio ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

^d OTTO VON GUERICKE UNIVERSITY   (Germany)

^e KING S COLLEGE HOSPITAL   (United Kingdom)

Author keywords

Epilepsy; Epileptiform discharge; Extracellular recording; Human; In vivo; Pathophysiology; Single pulse electrical stimulation; Single unit activity; SPES

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; ELECTRODE; ELECTROENCEPHALOGRAPHY; ELECTROSTIMULATION; EPILEPTIC DISCHARGE; FEMALE; HUMAN; IN VIVO STUDY; LATENT PERIOD; MALE; MICROELECTRODE; NERVE CELL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SINGLE PULSE ELECTRICAL STIMULATION;

ACTION POTENTIALS; ADULT; BRAIN; BRAIN WAVES; ELECTRIC STIMULATION; ELECTRODES, IMPLANTED; ELECTROENCEPHALOGRAPHY; EPILEPSY; FEMALE; HUMANS; MALE; MIDDLE AGED; NEURONS; YOUNG ADULT;

EID: 84864399215     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2012.02.062     Document Type: Article

References (33)

1. Aarts J.H., Binnie C.D., Smit A.M., Wilkins A.J. Selective cognitive impairment during focal and generalized epileptiform EEG activity. Brain 1984, 107:293-308.
2. Alarcon G., Garcia Seoane J.J., Binnie C.D., Martin Miguel M.C., Juler J., Polkey C.E., et al. Origin and propagation of interictal discharges in the acute electrocorticogram. Implications for pathophysiology and surgical treatment of temporal lobe epilepsy. Brain 1997, 120:2259-2282.
3. Alarcon G., Guy C.N., Binnie C.D., Walker S.R., Elwes R.D., Polkey C.E. Intracerebral propagation of interictal activity in partial epilepsy: implications for source localization. J Neurol Neurosurg Psychiatry 1994, 57:435-449.
4. Alarcon G., Valentin A., Lacruz M.E., Fitzgerald T., Richardson M.P., Quiroga R.Q., et al. Single cell electrical activity during human spontaneous interictal epileptiform discharges and responses to single pulse electrical stimulation (SPES). Eur J Neurol 2008, 15(Suppl. 3):304.
5. Avoli M., Olivier A. Electrophysiological properties and synaptic responses in the deep layers of the human epileptogenic neocortex in vitro. J Neurophysiol 1989, 61:589-606.
6. Babb T.L., Crandall P.H. Epileptogenesis of human limbic neurons in psychomotor epileptics. Electroencephalogr Clin Neurophysiol 1976, 40:225-243.
7. Babb T.L., Carr E., Crandall P.H. Analysis of extracellular firing patterns of deep temporal lobe structures in man. Electroencephalogr Clin Neurophysiol 1973, 34:247-257.
8. Brown J.T., Randall A.D. Activity-dependent depression of the spike after-depolarization generates long-lasting intrinsic plasticity in hippocampal CA3 pyramidal neurons. J Physiol 2009, 587:1265-1281.
9. Calvin W.H., Sypert G.W., Ward A.A. Structured timing patterns within bursts from epileptic neurons in undrugged monkey cortex. Exp Neurol 1968, 21:535-549.
10. Calvin W.H., Ojemann G.A., Ward A.A. Human cortical neurons in epileptogenic foci: comparison of inter-ictal firing patterns to those of "epileptic" neurons in animals. Electroencephalogr Clin Neurophysiol 1973, 34:337-351.
11. Colder B.W., Wilson C.L., Frysinger R.C., Harper R.M., Engel J. Interspike intervals during interictal periods in human temporal lobe epilepsy. Brain Res 1996, 719:96-103.
12. de Curtis M., Avanzini G. Interictal spikes in focal epileptogenesis. Prog Neurobiol 2001, 63:541-567.
13. Flanagan D., Valentin A., Garcia Seoane J.J., Alarcon G., Boyd S.G. Single-pulse electrical stimulation helps to identify epileptogenic cortex in children. Epilepsia 2009, 50:1793-1803.
14. Fried I., Wilson C.L., Maidment N.T., Engel J., Behnke E., Fields T.A., et al. Cerebral microdialysis combined with single-neuron and electroencephalographic recording in neurosurgical patients. Technical note. J Neurosurg 1999, 91:697-705.
15. Goldenshon E.S., Purpura D.P. Intracellular potentials of cortical neurons during focal epileptogenic discharges. Science 1963, 139:840-842.
16. Isokawa-Akesson M., Wilson C.L., Babb T.L. Inhibition in synchronously firing human hippocampal neurons. Epilepsy Res 1989, 3:236-247.
17. Jefferys J.G. Chronic epileptic foci in vitro in hippocampal slices from rats with the tetanus toxin epileptic syndrome. J Neurophysiol 1989, 62:458-468.
18. Jefferys J.G. Models and mechanisms of experimental epilepsies. Epilepsia 2003, 44(Suppl. 12):44-50.
19. Jiruska P., Csicsvari J., Powell A.D., Fox J.E., Chang W.C., Vreugdenhil M., et al. High-frequency network activity, global increase in neuronal activity, and synchrony expansion precede epileptic seizures in vitro. J Neurosci 2010, 30:5690-5701.
20. Keller C.J., Truccolo W., Gale J.T., Eskandar E., Thesen T., Carlson C., et al. Heterogeneous neuronal firing patterns during interictal epileptiform discharges in the human cortex. Brain 2010, 133:1668-1681.
21. Lacruz M.E., Garcia Seoane J.J., Valentin A., Selway R., Alarcon G. Frontal and temporal functional connections of the living human brain. Eur J Neurosci 2007, 26:1357-1370.
22. Lacruz M.E., Valentin A., Seoane J.J., Morris R.G., Selway R.P., Alarcon G. Single pulse electrical stimulation of the hippocampus is sufficient to impair human episodic memory. Neuroscience 2010, 170:623-632.
23. Lebovitz R.M. Autorhythmicity of spontaneous interictal spike discharge at hippocampal penicillin foci. Brain Res 1979, 172:35-55.
24. McCormick D.A. GABA as an inhibitory neurotransmitter in human cerebral cortex. J Neurophysiol 1989, 62:1018-1027.
25. Pavlov I., Kullmann D.M. How much inhibition in an epileptiform burst?. J Physiol 2010, 588:17-18.
26. Quiroga R.Q., Nadasdy Z., Ben-Shaul Y. Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput 2004, 16:1661-1687.
27. Schwartzkroin P.A., Turner D.A., Knowles W.D., Wyler A.R. Studies of human and monkey "epileptic" neocortex in the in vitro slice preparation. Ann Neurol 1983, 13:249-257.
28. Valentin A., Anderson M., Alarcon G., Seoane J.J., Selway R., Binnie C.D., et al. Responses to single pulse electrical stimulation identify epileptogenesis in the human brain in vivo. Brain 2002, 125:1709-1718.
29. Valentin A., Alarcon G., Garcia-Seoane J.J., Lacruz M.E., Nayak S.D., Honavar M., et al. Single-pulse electrical stimulation identifies epileptogenic frontal cortex in the human brain. Neurology 2005, 65:426-435.
30. Valentin A., Alarcon G., Honavar M., Garcia Seoane J.J., Selway R.P., Polkey C.E., et al. Single pulse electrical stimulation for identification of structural abnormalities and prediction of seizure outcome after epilepsy surgery: a prospective study. Lancet Neurol 2005, 4:718-726.
31. van 't Klooster M.A., Zijlmans M., Leijten F.S., Ferrier C.H., van Putten M.J., Huiskamp G.J. Time-frequency analysis of single pulse electrical stimulation to assist delineation of epileptogenic cortex. Brain 2011, 134:2855-2866.
32. Wittner L., Huberfeld G., Clemenceau S., Eross L., Dezamis E., Entz L., et al. The epileptic human hippocampal cornu ammonis 2 region generates spontaneous interictal-like activity in vitro. Brain 2009, 132:3032-3046.
33. Wyler A.R., Ojemann G.A., Ward A.A. Neurons in human epileptic cortex: correlation between unit and EEG activity. Ann Neurol 1982, 11:301-308.