High-frequency synaptic input contributes to seizure initiation in the low-[Mg2+] model of epilepsy

European Journal of Neuroscience

Volumn 19, Issue 5, 2004, Pages 1361-1372

  Lasztóczi, Bálint ^a   Antal, Károly ^a   Nyikos, Lajos ^a   Emri, Zsuzsa ^a   Kardos, Julianna ^a  

^a CHEMICAL RESEARCH CENTER   (Hungary)

Author keywords

High frequency oscillation; Hippocampus; Rat; Seizure like event; Synchronization

Indexed keywords

MAGNESIUM ION;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN SLICE; CELL SYNCHRONIZATION; CLONIC SEIZURE; CONTROLLED STUDY; ELECTRIC POTENTIAL; EPILEPSY; HIPPOCAMPUS; MEMBRANE POTENTIAL; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SEIZURE; SYNAPTIC TRANSMISSION; TONIC SEIZURE; VOLTAGE CLAMP;

ANIMALS; DISEASE MODELS, ANIMAL; EPILEPSY; HIPPOCAMPUS; MAGNESIUM; MALE; RATS; RATS, WISTAR; SEIZURES; SYNAPTIC TRANSMISSION;

EID: 1642364827     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03231.x     Document Type: Article

References (50)

1. Albowitz, B., König, P. & Kuhnt, U. (1997) Spatiotemporal distribution of intracellular calcium transients during epileptiform activity in guinea pig hippocampal slices. J. Neurophysiol., 77, 491-501.
2. Allen, P.J., Fish, D.R. & Smith, S.J.M. (1992) Very high frequency rhythmic activity during SEEG suppression in frontal lobe epilepsy. Electroencephalogr. Clin. Neurophysiol., 82, 155-159.
3. Anderson, W.W., Lewis, D.V., Swartzwelder, H.S. & Wilson, W.A. (1986) Magnesium-free medium activates seizure-like events in the rat hippocampal slice. Brain. Res., 398, 215-219.
4. Bikson, M., Fox, J.E. & Jefferys, J.G.R. (2003) Neuronal aggregates formation underlies spatiotemporal dynamics of nonsynaptic seizure initiation. J. Neurophysiol., 89, 2330-2333.
5. Bragin, A., Engel, J. Jr, Wilson, C.L., Fried, I. & Buzsáki, G. (1999a) High-frequency oscillations in human brain. Hippocampus, 9, 137-142.
6. Bragin, A., Engel, J. Jr, Wilson, C.L., Fried, I. & Mathern, G.W. (1999b) 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.
7. Bragin, A., Engel, J. Jr, Wilson, C.L., Vizentin, E. & Mathern, G.W. (1999c) Electrophysiologic analysis of a chronic seizure model after unilateral hippocampal KA injection. Epilepsia, 40, 1210-1221.
8. Bragin, A., Mody, I., Wilson, C.L. & Engel, J. Jr (2002a) Local generation of fast ripples in epileptic brain. J. Neurosci., 22, 2012-2021.
9. Bragin, A., Wilson, C.L. & Engel, J. Jr (2000) Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clusters: a hypothesis. Epilepsia, 41, S144-S152.
10. Bragin, A., Wilson, C.L., Staba, R.J., Reddick, M., Fried, I. & Engel, J. Jr (2002b) Interictal high-frequency oscillations (80-500 Hz) in the human epileptic brain: entorhinal cortex. Ann. Neurol., 52, 407-415.
11. Buzsáki, G., Horváth, Z., Urioste, R., Hetke, J. & Wise, K. (1992) High-frequency network oscillation in the hippocampus. Science, 256, 1025-1027.
12. Chorbak, J.J. & Buzsáki, G. (1996) High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J. Neurosci., 16, 30-56.
13. Csicsvari, J., Hirase, H., Czurkó, A., Mamiya, A. & Buzsáki, G. (1999a) Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J. Neurosci., 19, 274-287.
14. Csicsvari, J., Hirase, H., Czurkó, A., Mamiya, A. & Buzsáki, G. (1999b) Fast network oscillations in the hippocampal CA1 region of the behaving rat. J. Neurosci., 19, 1-4.
15. DeCurtis, M., Radici, C. & Forti, M. (1999) Cellular mechanisms underlying spontaneous interictal spikes in an acute model of focal cortical epileptogenesis. Neuroscience, 88, 107-117.
16. Di Garbo, A., Barbi, M. & Chillemi, S. (2002) Synchronization in a network of fast-spiking interneurons. Biosystems, 67, 45-53.
17. Draguhn, A., Traub, R.D., Bibbig, A. & Schmitz, D. (2000) Ripple (approximately 200 Hz) oscillations in temporal structures. J. Clin. Neurophysiol., 17, 361-376.
18. Draguhn, A., Traub, R.D., Schmitz, D. & Jefferys, J.G.R. (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature, 394, 189-192.
19. Duckrow, R.B. & Spencer, S.S. (1992) Regional coherence and transfer of ictal activity during seizure onset in the medial temporal lobe. Electroencephalogr. Clin. Neurophysiol., 82, 415-422.
20. Fisher, R.S., Webber, W.R., Lesser, R.P., Arroyo, S. & Uematsu, S. (1992) High-frequency EEG activity at the start of seizures. J. Clin. Neurophysiol., 9, 441-448.
21. Fricker, D., Verheugen, J.A.H. & Miles, R. (1999) Cell-attached measurement of the firing threshold of rat hippocampal neurons. J. Physiol., 517, 791-804.
22. Gabor, D. (1946) Theory of communication. J. IEE., 93, 429-457.
23. Galarreta, M. & Hestrin, S. (2001) Spike transmission and synchrony detection in networks of GABAergic interneurons. Science, 292, 2295-2299.
24. 2+ induced epileptiform activity in rat hippocampal and entorhinal cortex slices during adolescence. Dev. Brain. Res., 87, 145-152.
25. Grenier, F., Timofeev, I. & Steriade, M. (2003) Neocortical very fast oscillations (ripples, 80-200 Hz) during seizures: intracellular correlates. J. Neurophysiol., 89, 841-852.
26. Jones, M.S., MacDonald, K.D., Choi, B., Dudek, F.E. & Barth, D.S. (2000) Intracellular correlates of fast (>200 Hz) electrical oscillations in rat somatosensory cortex. J. Neurophysiol., 84, 1505-1518.
27. Khosravani, H., Carlen, P.L. & PereZ. Velazquez, J.L. (2003) The control of seizure-like activity in the rat hippocampal slice. Biophys. J., 84, 687-695.
28. 2+ in rat hippocampal slices depends on gap junctional coupling. Neuroscience, 105, 579-587.
29. 2+ fluctuations in organotypic hippocampal slice cultures. Neuroreport, 11, 2107-2111.
30. Lasztóczi, B., Kovács, R., Nyikos, L. & Kardos, J. (2002) A glutamate receptor subtype antagonist inhibits seizures in rat hippocampal slices. Neuroreport, 13, 351-356.
31. McCormick, D.A. & Contreras, D. (2001) On the cellular and network bases of epileptic seizures. Annu. Rev. Physiol., 63, 815-846.
32. Mormann, F., Kreuz, T., Andrzejak, R.G., David, P., Lehnertz, K. & Elger, C.E. (2003) Epileptic seizures are preceded by a decrease in synchronization. Epilepsy. Res., 53, 173-185.
33. Mormann, F., Lehnertz, K., David, P. & Elger, C.E. (2000) Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients. Physica. D., 144, 358-369.
34. Nyikos, L., Lasztóczi, B., Antal, K., Kovács, R. & Kardos, J. (2003) Desynchronisation of spontaneously recurrent experimental seizures proceeds with a single rhythm. Neuroscience, 121, 705-717.
35. Pacia, S.V. & Ebersole, J.S. (1997) Intracranial EEG substrates of scalp ictal patterns from temporal lobe foci. Epilepsia, 38, 642-654.
36. Palva, J.M., Lamsa, K., Rauvala, H., Kaila, K. & Taira, T. (2000) Fast network oscillations in the newborn rat hippocampus in vitro. J. Neurosci., 20, 1170-1178.
37. Panter, P. (1965) Modulation, Noise and Spectral Analysis. McGraw-Hill, New York.
38. Regehr, W.G. & Tank, D.W. (1992) Calcium concentration dynamics produced by synaptic activation of CA1 hippocampal pyramidal cells. J. Neurosci., 12, 4202-4223.
39. Schmitz, D., Schuchmann, S., Fisahn, A., Draguhn, A., Buhl, E.H., Petrasch-Parwez, E., Dermietzel, R., Heinemann, U. & Traub, R.D. (2001) Axo-axonal coupling: a novel mechanism for ultrafast neuronal communication. Neuron, 31, 831-840.
40. Schreiber, T. & Schmitz, A. (2000) Surrogate time series. Physica. D., 142, 346-382.
41. Staba, R.J., Wilson, L.C., Bragin, A., Fried, I. & Engel, J. (2002) Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J. Neurophysiol., 88, 1743-1752.
42. Straub, H., Köhling, R., Frieler, A., Grigat, M. & Speckmann, E.-J. (2000) Contribution of L-type calcium channels to epileptiform activity in hippocampal and neocortical slices of guinea-pigs. Neuroscience, 95, 63-72.
43. 2+ dynamics in recurrent seizure-like events. Eur. J. Neurosci., 12, 3893-3899.
44. Tancredi, V., Hwa, G.G.C., Zona, C., Brancati, A. & Avoli, M. (1990) Low magnesium epileptogenesis in the rat hippocampal slice: electrophysiological and pharmacological features. Brain. Res., 511, 280-290.
45. Traub, R.D. & Bibbig, A. (2000) A model of high-frequency ripples in the hippocampus based on synaptic coupling plus axon-axon gap junctions between pyramidal neurons. J. Neurosci., 20, 2086-2093.
46. Traub, R.D., Draguhn, A., Whittington, M.A., Baldeweg, T., Bibbig, A., Buhl, E.H. & Schmitz, D. (2002) Axonal gap junctions between principal neurones: a novel source of network oscillations, and perhaps epileptogenesis. Rev. Neurosci., 13, 1-30.
47. 2+ in the rat hippocampal slice. J. Physiol., 478, 379-393.
48. Traub, R.D., Whittington, M.A., Buhl, E.H., LeBeau, F.E.N., Bibbig, A., Boyd, S., Cross, H. & Baldweg, T. (2001) A possible role for gap junction in generation of very fast EEG oscillations preceding the onset of, and perhaps initiating, seizures. Epilepsia, 42, 153-170.
49. Walther, H., Lambert, J.D.C., Jones, R.S.G., Heinemann, U. & Hamon, B. (1986) Epileptiform activity in combined slices of the hippocampus, subiculum and entorhinal cortex during perfusion with low magnesium medium. Neurosci. Lett., 69, 156-161.
50. Ylinen, A., Bragin, A., Nádasdy, Z., Jandó, G., Szabó, I., Sik, A. & Buzsáki, G. (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci., 15, 30-46.