Computational modeling of high-frequency oscillations at the onset of neocortical partial seizures: From 'altered structure' to 'dysfunction'

NeuroImage

Volumn 52, Issue 3, 2010, Pages 1109-1122

  Molaee Ardekani, Behnam ^a,b   Benquet, Pascal ^c   Bartolomei, Fabrice ^a,d,e   Wendling, Fabrice ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c UNIVERSITÉ DE RENNES 1   (France)

^d TIMONE HOSPITAL   (France)

^e AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Chirp; Fast inhibitory interneurons; Fast onset activity; Focal seizures; High gamma; Neural mass model; Partial epilepsy

Indexed keywords

ARTICLE; ARTIFICIAL NEURAL NETWORK; BRAIN CORTEX; BRAIN FUNCTION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEEDBACK SYSTEM; FOCAL EPILEPSY; GABAERGIC TRANSMISSION; MATHEMATICAL ANALYSIS; MATHEMATICAL MODEL; NEURAL MASS MODEL; NEUROTRANSMISSION; OSCILLATION; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION; BIOLOGICAL MODEL; ELECTROENCEPHALOGRAPHY; HUMAN; NEOCORTEX; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNAPTIC POTENTIAL;

ELECTROENCEPHALOGRAPHY; EPILEPSY, PARTIAL, SENSORY; HUMANS; MODELS, NEUROLOGICAL; NEOCORTEX; NEURAL NETWORKS (COMPUTER); SYNAPTIC POTENTIALS;

EID: 77954385490     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2009.12.049     Document Type: Article

References (81)

1. Alarcon G., Binnie C.D., Elwes R.D., Polkey C.E. Power spectrum and intracranial EEG patterns at seizure onset in partial epilepsy. Electroencephalogr. Clin. Neurophysiol. 1995, 94(5):326-337.
2. Allen P.J., Fish D.R., Smith S.J. Very high-frequency rhythmic activity during SEEG suppression in frontal lobe epilepsy. Electroencephalogr. Clin. Neurophysiol. 1992, 82(2):155-159.
3. Bacci A., Rudolph U., Huguenard J.R., Prince D.A. Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses. J. Neurosci. 2003, 23(29):9664-9674.
4. Bancaud J., Talairach J. Methodology of stereo EEG exploration and surgical intervention in epilepsy. Rev. Otoneuroophtalmol. 1973, 45(4):315-328.
5. Bancaud J., Angelergues R., Bernouilli C., Bonis A., Bordas-Ferrer M., Bresson M., Buser P., Covello L., Morel P., Szikla G., et al. Functional stereotaxic exploration (SEEG) of epilepsy. Electroencephalogr. Clin. Neurophysiol. 1970, 28(1):85-86.
6. Bartolomei F., Guye M., Gavaret M., Regis J., Wendling F., Raybaud C., Chauvel P. The presurgical evaluation of epilepsies. Rev. Neurol. (Paris) 2002, 158(5 Pt. 2). 4S55-4S64.
7. Bartolomei F., Chauvel P., Wendling F. Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. Brain 2008, 131(Pt. 7):1818-1830.
8. Bartos M., Vida I., Frotscher M., Meyer A., Monyer H., Geiger J.R., Jonas P. Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc. Natl. Acad. Sci. U. S. A. 2002, 99(20):13222-13227.
9. Bartos M., Vida I., Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 2007, 8(1):45-56.
10. Bojak I., Liley D.T. Modeling the effects of anesthesia on the electroencephalogram. Phys. Rev. E Stat. Nonlin. Soft Matter. Phys. 2005, 71(4 Pt 1):041902.
11. Breakspear M., Roberts J.A., Terry J.R., Rodrigues S., Mahant N., Robinson P.A. A unifying explanation of primary generalized seizures through nonlinear brain modeling and bifurcation analysis. Cereb. Cortex 2006, 16(9):1296-1313.
12. Buhl E.H., Halasy K., Somogyi P. Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 1994, 368(6474):823-828.
13. Buzsaki G., Geisler C., Henze D.A., Wang X.J. Interneuron diversity series: circuit complexity and axon wiring economy of cortical interneurons. Trends Neurosci. 2004, 27(4):186-193.
14. Cossart R., Dinocourt C., Hirsch J.C., Merchan-Perez A., De Felipe J., Ben-Ari Y., Esclapez M., Bernard C. Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat. Neurosci. 2001, 4(1):52-62.
15. Czeiger D., White E.L. Synapses of extrinsic and intrinsic origin made by callosal projection neurons in mouse visual cortex. J. Comp. Neurol. 1993, 330(4):502-513.
16. Deco G., Jirsa V.K., Robinson P.A., Breakspear M., Friston K. The dynamic brain: from spiking neurons to neural masses and cortical fields. PLoS Comput. Biol. 2008, 4(8):e1000092.
17. DeFelipe J., Farinas I. The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol. 1992, 39(6):563-607.
18. Deisz R.A. The GABA(B) receptor antagonist CGP 55845A reduces presynaptic GABA(B) actions in neocortical neurons of the rat in vitro. Neuroscience 1999, 93(4):1241-1249.
19. Elhanany E., White E.L. Intrinsic circuitry: synapses involving the local axon collaterals of corticocortical projection neurons in the mouse primary somatosensory cortex. J. Comp. Neurol. 1990, 291(1):43-54.
20. Fisher R.S., Webber W.R., Lesser R.P., Arroyo S., Uematsu S. High-frequency EEG activity at the start of seizures. J. Clin. Neurophysiol. 1992, 9(3):441-448.
21. Freeman W.J. Models of the dynamics of neural populations. Electroencephalogr. Clin. Neurophysiol. Suppl 1978, (34):9-18.
22. Freund T.F., Buzsaki G. Interneurons of the hippocampus. Hippocampus 1996, 6(4):347-470.
23. Freund T.F., Katona I. Perisomatic inhibition. Neuron 2007, 56(1):33-42.
24. Fujiwara-Tsukamoto Y., Isomura Y., Kaneda K., Takada M. Synaptic interactions between pyramidal cells and interneurone subtypes during seizure-like activity in the rat hippocampus. J. Physiol. 2004, 557(Pt 3):961-979.
25. Galarreta M., Hestrin S. Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex. Proc. Natl. Acad. Sci. U. S. A. 2002, 99(19):12438-12443.
26. Gnatkovsky V., Librizzi L., Trombin F., de Curtis M. Fast activity at seizure onset is mediated by inhibitory circuits in the entorhinal cortex in vitro. Ann. Neurol. 2008, 64(6):674-686.
27. Gupta A., Wang Y., Markram H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 2000, 287(5451):273-278.
28. Hardie J.B., Pearce R.A. Active and passive membrane properties and intrinsic kinetics shape synaptic inhibition in hippocampal CA1 pyramidal neurons. J. Neurosci. 2006, 26(33):8559-8569.
29. Jansen B.H.R.V. Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns. Biol. Cybern 1995, 73(4):357-366.
30. Jansen B.H.Z.G., Brandt M.E. A neurophysiologically-based mathematical model of flash visual evoked potentials. Biol. Cybern. 1993, 68(3):275-283.
31. Jirsa V.K., Haken H. Field theory of electromagnetic brain activity. Phys. Rev. Lett. 1996, 77(5):960-963.
32. Johnson R.R., Burkhalter A. Microcircuitry of forward and feedback connections within rat visual cortex. J. Comp. Neurol. 1996, 368(3):383-398.
33. Juhasz C., Asano E., Shah A., Chugani D.C., Batista C.E., Muzik O., Sood S., Chugani H.T. Focal decreases of cortical GABAA receptor binding remote from the primary seizure focus: what do they indicate?. Epilepsia 2009, 50(2):240-250.
34. Kapur A., Pearce R.A., Lytton W.W., Haberly L.B. GABAA-mediated IPSCs in piriform cortex have fast and slow components with different properties and locations on pyramidal cells. J. Neurophysiol. 1997, 78(5):2531-2545.
35. Keller A., Asanuma H. Synaptic relationships involving local axon collaterals of pyramidal neurons in the cat motor cortex. J. Comp. Neurol. 1993, 336(2):229-242.
36. Kidd F.L., Isaac J.T. Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature 1999, 400(6744):569-573.
37. Kisvarday Z.F., Eysel U.T. Cellular organization of reciprocal patchy networks in layer III of cat visual cortex (area 17). Neuroscience 1992, 46(2):275-286.
38. Kisvarday Z.F., Adams C.B., Smith A.D. Synaptic connections of axo-axonic (chandelier) cells in human epileptic temporal cortex. Neuroscience 1986, 19(4):1179-1186.
39. Krook-Magnuson E., Huntsman M.M. The transience of interneuron circuit diversity just "sped" up. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(43):16723-16724.
40. Lee S.A., Spencer D.D., Spencer S.S. Intracranial EEG seizure-onset patterns in neocortical epilepsy. Epilepsia 2000, 41(3):297-307.
41. Lopes da Silva F.H., Hoeks A., Smits H., Zetterberg L.H. Model of brain rhythmic activity. The alpha-rhythm of the thalamus. Kybernetik 1974, 15(1):27-37.
42. Lopes da Silva F.H., van Rotterdam A., Barts P., van Heusden E., Burr W. Models of neuronal populations: the basic mechanisms of rhythmicity. Prog. Brain Res. 1976, 45:281-308.
43. Lopes da Silva F., Blanes W., Kalitzin S.N., Parra J., Suffczynski P., Velis D.N. Epilepsies as dynamical diseases of brain systems: basic models of the transition between normal and epileptic activity. Epilepsia 2003, 44(Suppl. 12):72-83.
44. Markram H., Toledo-Rodriguez M., Wang Y., Gupta A., Silberberg G., Wu C. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 2004, 5(10):793-807.
45. Molaee-Ardekani B., Senhadji L., Shamsollahi M.B., Vosoughi-Vahdat B., Wodey E. Brain activity modeling in general anesthesia: enhancing local mean-field models using a slow adaptive firing rate. Phys. Rev. E Stat. Nonlin. Soft Matter. Phys. 2007, 76(4 Pt 1):041911.
46. Nettleton J.S., Spain W.J. Linear to supralinear summation of AMPA-mediated EPSPs in neocortical pyramidal neurons. J. Neurophysiol. 2000, 83(6):3310-3322.
47. Nunez P.L. The brain wave function: a model for the EEG. Math. Biosci. 1974, 21:279-297.
48. Palma E., Esposito V., Mileo A.M., Di Gennaro G., Quarato P., Giangaspero F., Scoppetta C., Onorati P., Trettel F., Miledi R. Expression of human epileptic temporal lobe neurotransmitter receptors in Xenopus oocytes: an innovative approach to study epilepsy. Proc. Natl. Acad. Sci. U. S. A. 2002, 99(23):15078-15083.
49. Palma E., Ragozzino D.A., Di Angelantonio S., Spinelli G., Trettel F., Martinez-Torres A., Torchia G., Arcella A., Di Gennaro G., Quarato P.P. Phosphatase inhibitors remove the run-down of gamma-aminobutyric acid type A receptors in the human epileptic brain. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(27):10183-10188.
50. Palma E., Torchia G., Limatola C., Trettel F., Arcella A., Cantore G., Di Gennaro G., Manfredi M., Esposito V., Quarato P.P. BDNF modulates GABAA receptors microtransplanted from the human epileptic brain to Xenopus oocytes. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(5):1667-1672.
51. Palma E., Roseti C., Maiolino F., Fucile S., Martinello K., Mazzuferi M., Aronica E., Manfredi M., Esposito V., Cantore G. GABA(A)-current rundown of temporal lobe epilepsy is associated with repetitive activation of GABA(A) "phasic" receptors. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(52):20944-20948.
52. Pearce R.A. Physiological evidence for two distinct GABAA responses in rat hippocampus. Neuron 1993, 10(2):189-200.
53. Penttonen M., Kamondi A., Acsady L., Buzsaki G. Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur. J. Neurosci. 1998, 10(2):718-728.
54. Price C.J., Cauli B., Kovacs E.R., Kulik A., Lambolez B., Shigemoto R., Capogna M. Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J. Neurosci. 2005, 25(29):6775-6786.
55. Rennie C.J., Wright J.J., Robinson P.A. Mechanisms of cortical electrical activity and emergence of gamma rhythm. J. Theor. Biol. 2000, 205(1):17-35.
56. Robinson P.A., Rennie C.J., Rowe D.L. Dynamics of large-scale brain activity in normal arousal states and epileptic seizures. Phys. Rev. E Stat. Nonlin Soft Matter. Phys. 2002, 65(4 Pt 1):041924.
57. Robinson P.A., Rennie C.J., Rowe D.L., O'Connor S.C., Wright J.J., Gordon E., Whitehouse R.W. Neurophysical modeling of brain dynamics. Neuropsychopharmacology 2003, 28(Suppl. 1):S74-S79.
58. Schiff S.J., Colella D., Jacyna G.M., Hughes E., Creekmore J.W., Marshall A., Bozek-Kuzmicki M., Benke G., Gaillard W.D., Conry J. Brain chirps: spectrographic signatures of epileptic seizures. Clin. Neurophysiol. 2000, 111(6):953-958.
59. Simon A., Olah S., Molnar G., Szabadics J., Tamas G. Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. J. Neurosci. 2005, 25(27):6278-6285.
60. Somogyi P. A specific 'axo-axonal' interneuron in the visual cortex of the rat. Brain Res. 1977, 136(2):345-350.
61. Somogyi P., Tamas G., Lujan R., Buhl E.H. Salient features of synaptic organisation in the cerebral cortex. Brain Res. Brain Res. Rev. 1998, 26(2-3):113-135.
62. Steyn-Ross M.L., Steyn-Ross D.A., Sleigh J.W. Modelling general anaesthesia as a first-order phase transition in the cortex. Prog. Biophys. Mol. Biol. 2004, 85(2-3):369-385.
63. Suffczynski P., Kalitzin S., Lopes Da Silva F.H. Dynamics of non-convulsive epileptic phenomena modeled by a bistable neuronal network. Neuroscience 2004, 126(2):467-484.
64. Talairach J., Bancaud J., Bonis A., Szikla G., Trottier S., Vignal J.P., Chauvel P., Munari C., Chodkievicz J.P. Surgical therapy for frontal epilepsies. Adv. Neurol. 1992, 57:707-732.
65. Tamas G., Lorincz A., Simon A., Szabadics J. Identified sources and targets of slow inhibition in the neocortex. Science 2003, 299(5614):1902-1905.
66. Thomson A.M., Deuchars J. Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. Cereb. Cortex 1997, 7(6):510-522.
67. Thomson A.M., West D.C., Hahn J., Deuchars J. Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. J. Physiol. 1996, 496(Pt 1):81-102.
68. Timofeev I., Steriade M. Neocortical seizures: initiation, development and cessation. Neuroscience 2004, 123(2):299-336.
69. Traub R.D. Fast oscillations and epilepsy. Epilepsy Curr. 2003, 3(3):77-79.
70. Traub R.D., Whittington M.A., Colling S.B., Buzsaki G., Jefferys J.G. Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J. Physiol. 1996, 493(Pt 2):471-484.
71. Traub R.D., Whittington M.A., Buhl E.H., LeBeau F.E., Bibbig A., Boyd S., Cross H., Baldeweg T. A possible role for gap junctions in generation of very fast EEG oscillations preceding the onset of, and perhaps initiating, seizures. Epilepsia 2001, 42(2):153-170.
72. Tsai T.Y., Choi Y.S., Ma W., Pomerening J.R., Tang C., Ferrell J.E. Robust, tunable biological oscillations from interlinked positive and negative feedback loops. Science 2008, 321(5885):126-129.
73. Uva L., Librizzi L., Wendling F., de Curtis M. Propagation dynamics of epileptiform activity acutely induced by bicuculline in the hippocampal-parahippocampal region of the isolated Guinea pig brain. Epilepsia 2005, 46(12):1914-1925.
74. Wang Y., Gupta A., Markram H. Anatomical and functional differentiation of glutamatergic synaptic innervation in the neocortex. J. Physiol. Paris 1999, 93(4):305-317.
75. Wendling F., Bellanger J.J., Bartolomei F., Chauvel P. Relevance of nonlinear lumped-parameter models in the analysis of depth-EEG epileptic signals. Biol. Cybern 2000, 83(4):367-378.
76. Wendling F., Bartolomei F., Bellanger J.J., Chauvel P. Interpretation of interdependencies in epileptic signals using a macroscopic physiological model of the EEG. Clin. Neurophysiol. 2001, 112(7):1201-1218.
77. Wendling F., Bartolomei F., Bellanger J.J., Chauvel P. Epileptic fast activity can be explained by a model of impaired GABAergic dendritic inhibition. Eur. J. Neurosci. 2002, 15(9):1499-1508.
78. Wendling F., Bartolomei F., Bellanger J.J., Bourien J., Chauvel P. Epileptic fast intracerebral EEG activity: evidence for spatial decorrelation at seizure onset. Brain 2003, 126(Pt. 6):1449-1459.
79. Wendling F., Hernandez A., Bellanger J.J., Chauvel P., Bartolomei F. Interictal to ictal transition in human temporal lobe epilepsy: insights from a computational model of intracerebral EEG. J. Clin. Neurophysiol. 2005, 22(5):343-356.
80. Wilson H.R.C.J. A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue. Kybernetik 1973, 13:55-80.
81. Zsiros V., Maccaferri G. Electrical coupling between interneurons with different excitable properties in the stratum lacunosum-moleculare of the juvenile CA1 rat hippocampus. J. Neurosci. 2005, 25(38):8686-8695.