System characterization of neuronal excitability in the hippocampus and its relevance to observed dynamics of spontaneous seizure-like transitions

Journal of Neural Engineering

Volumn 7, Issue 3, 2010, Pages

  Zalay, Osbert C ^a   Serletis, Demitre ^a,b,c   Carlen, Peter L ^a,b,c   Bardakjian, Berj L ^a,d  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BEFORE AND AFTER; CELL RECORDING; CONTROL STUDIES; DYNAMIC BALANCE; EPILEPTIFORM ACTIVITY; EPILEPTOGENESIS; EXPERIMENTAL MODELS; EXTRACELLULAR; FIRST ORDER KERNEL; GAUSSIAN WHITE NOISE; IN-VITRO; INPUT-OUTPUT; INTERMITTENCY; NETWORK MODELS; NEURONAL ACTIVATION; OSCILLATOR NETWORKS; QUANTITATIVE MEASURES; SECOND ORDERS; SPECTRAL ENERGY; SYSTEM CHARACTERIZATION; SYSTEM KERNEL; VOLTERRA KERNELS;

MATHEMATICAL MODELS; POTASSIUM; WHITE NOISE;

PHYSIOLOGICAL MODELS;

MAGNESIUM ION; POTASSIUM ION;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; DYNAMICS; EPILEPSY; EPILEPTIC DISCHARGE; EPILEPTOGENESIS; EXTRACELLULAR SPACE; FEEDBACK SYSTEM; HIPPOCAMPUS; IN VITRO STUDY; KERNEL METHOD; MATHEMATICAL MODEL; MOUSE; NERVE CELL; NERVE CELL EXCITABILITY; NONHUMAN; OSCILLATOR; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SEIZURE; SPECTROSCOPY; WHITE NOISE; WHOLE CELL; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; BIOLOGICAL RHYTHM; C57BL MOUSE; HUMAN; NERVE CELL NETWORK; PATHOPHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL CLOCKS; HIPPOCAMPUS; HUMANS; MICE; MICE, INBRED C57BL; MODELS, NEUROLOGICAL; NERVE NET; SEIZURES;

EID: 77952354677     PISSN: 17412560     EISSN: 17412552     Source Type: Journal    
DOI: 10.1088/1741-2560/7/3/036002     Document Type: Article

References (61)

1. Bardakjian B L and Diamant N E 1994 A mapped clock oscillator model for transmembrane electrical rhythmic activity in excitable cells J. Theor. Biol. 166 225-35
2. Bazhenov M, Timofeev I, Frohlich F and Sejnowski T J 2008 Cellular and network mechanisms of electrographic seizures Drug Discov. Today Dis. Models 5 45-57
3. Behrens C J, Van Den Boom L P and Heinemann U 2007 Effects of the GABA(A) receptor antagonists bicuculline and gabazine on stimulus-induced sharp wave-ripple complexes in adult rat hippocampus in vitro Eur. J. Neurosci. 25 2170-81
4. Bergey G K and Franaszczuk P J 2001 Epileptic seizures are characterized by changing signal complexity Clin. Neurophysiol. 112 241-9
5. Binder D K and Steinhauser C 2006 Functional changes in astroglial cells in epilepsy Glia 54 358-68
6. Borck C and Jefferys J G 1999 Seizure-like events in disinhibited ventral slices of adult rat hippocampus J. Neurophysiol. 82 2130-42
7. Buzsaki G 2002 Theta oscillations in the hippocampus Neuron 33 325-40
8. Buzsaki G and Draguhn A 2004 Neuronal oscillations in cortical networks Science 304 1926-9
9. Carvalho T P and Buonomano D V 2009 Differential effects of excitatory and inhibitory plasticity on synaptically driven neuronal input-output functions Neuron 61 774-85
10. Chakravarthy N, Tsakalis K, Sabesan S and Iasemidis L 2009 Homeostasis of brain dynamics in epilepsy: a feedback control systems perspective of seizures Ann. Biomed. Eng. 37 565-85
11. Chiu A W, Jahromi S S, Khosravani H, Carlen P L and Bardakjian B L 2006 The effects of high-frequency oscillations in hippocampal electrical activities on the classification of epileptiform events using artificial neural networks J. Neural Eng. 3 9-20
12. Derchansky M, Jahromi S S, Mamani M, Shin D S, Sik A and Carlen P L 2008 Transition to seizures in the isolated immature mouse hippocampus: a switch from dominant phasic inhibition to dominant phasic excitation J. Physiol. 586 477-94
13. Derchansky M, Rokni D, Rick J T, Wennberg R, Bardakjian B L, Zhang L, Yarom Y and Carlen P L 2006 Bidirectional multisite seizure propagation in the intact isolated hippocampus: the multifocality of the seizure 'focus' Neurobiol. Dis. 23 312-28
14. Derchansky M, Shahar E, Wennberg R A, Samoilova M, Jahromi S S, Abdelmalik P A, Zhang L and Carlen P L 2004 Model of frequent, recurrent, and spontaneous seizures in the intact mouse hippocampus Hippocampus 14 935-47
15. Djukic B, Casper K B, Philpot B D, Chin L S and McCarthy K D 2007 Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation J. Neurosci. 27 11354-65
16. Dreier J P and Heinemann U 1991 Regional and time dependent variations of low Mg2+ induced epileptiform activity in rat temporal cortex slices Exp. Brain Res. 87 581-96
17. Dudek F E and Staley K J 2007 How does the balance of excitation and inhibition shift during epileptogenesis? Epilepsy Curr. 7 86-8
18. Frohlich F, Bazhenov M, Iragui-Madoz V and Sejnowski T J 2008 Potassium dynamics in the epileptic cortex: new insights on an old topic Neuroscientist 14 422-33
19. Fujiwara-Tsukamoto Y, Isomura Y and Takada M 2006 Comparable GABAergic mechanisms of hippocampal seizurelike activity in posttetanic and low-Mg2+ conditions J. Neurophysiol. 95 2013-19
20. Gaiarsa J L, Caillard O and Ben-Ari Y 2002 Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance Trends Neurosci. 25 564-70
21. Goutagny R, Jackson J and Williams S 2009 Self-generated theta oscillations in the hippocampus Nat. Neurosci. 12 1491-3
22. Grebogi C, Ott E and Yorke J A 1983 Crises, sudden changes in chaotic attractors, and transient chaos Phys. D: Nonlinear Phenom. 7 181-200
23. Grebogi C, Ott E and Yorke J A 1986 Critical exponent of chaotic transients in nonlinear dynamical systems Phys. Rev. Lett. 57 1284-7
24. Hasselmo M E, Schnell E and Barkai E 1995 Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3 J. Neurosci. 15 5249-62
25. Hooke R and Jeeves T A 1961 'Direct search' solution of numerical and statistical problems JACM 8 212-29
26. Iasemidis L D 2003 Epileptic seizure prediction and control IEEE Trans. Biomed. Eng. 50 549-58
27. Iasemidis L D, Pardalos P M, Shiau D S, Chaovalitwongse W, Narayanan K, Kumar S, Carney P R and Sackellares J C 2003a Prediction of human epileptic seizures based on optimization and phase changes of brain electrical activity Optim. Meth. Softw. 18 81-104
28. Iasemidis L D, Principe J C and Sackellares J C 2000 Measurement and quantification of spatiotemporal dynamics of human epileptic seizures Nonlinear Biomedical Signal Processing ed M Akay (Piscataway, NJ: IEEE Press) pp 294-318
29. Iasemidis L D, Shiau D S, Chaovalitwongse W, Sackellares J C, Pardalos P M, Principe J C, Carney P R, Prasad A, Veeramani B and Tsakalis K 2003b Adaptive epileptic seizure prediction system IEEE Trans. Biomed. Eng. 50 616-27
30. Iasemidis L D, Shiau D S, Sackellares J C, Pardalos P M and Prasad A 2004 Dynamical resetting of the human brain at epileptic seizures: application of nonlinear dynamics and global optimization techniques IEEE Trans. Biomed. Eng. 51 493-506
31. + conditions in an in vitro model of epilepsy J. Biol. Phys. 36 95-107
32. Khalilov I, Esclapez M, Medina I, Aggoun D, Lamsa K, Leinekugel X, Khazipov R and Ben-Ari Y 1997 A novel in vitro preparation: the intact hippocampal formation Neuron 19 743-9
33. Kim U, Sanchez-Vives M V and McCormick D A 1997 Functional dynamics of GABAergic inhibition in the thalamus Science 278 130-4
34. Kubota D, Colgin L L, Casale M, Brucher F A and Lynch G 2003 Endogenous waves in hippocampal slices J. Neurophysiol. 89 81-9
35. Marder E and Thirumalai V 2002 Cellular, synaptic and network effects of neuromodulation Neural. Netw. 15 479-93
36. Marmarelis V Z 1993 Identification of nonlinear biological systems using Laguerre expansions of kernels Ann. Biomed. Eng. 21 573-89
37. Marple S L 1999 Computing the discrete-time 'analytic' signal via FFT IEEE Trans. Signal Process. 47 2600-3
38. Marty A and Llano I 2005 Excitatory effects of GABA in established brain networks Trends Neurosci. 28 284-9
39. Nair S P, Shiau D S, Principe J C, Iasemidis L D, Pardalos P M, Norman W M, Carney P R, Kelly K M and Sackellares J C 2009 An investigation of EEG dynamics in an animal model of temporal lobe epilepsy using the maximum Lyapunov exponent Exp. Neurol. 216 115-21
40. Ogura H 1985 Estimation of Wiener kernels of a nonlinear system and a fast algorithm using digital laguerre filters Proc. 15th NIBB Conf. (Okazaki, Japan) pp 14-62
41. Ottman R, Annegers J F, Risch N, Hauser W A and Susser M 1996 Relations of genetic and environmental factors in the etiology of epilepsy Ann. Neurol. 39 442-9
42. Palmini A, Andermann F, Olivier A, Tampieri D, Robitaille Y, Andermann E and Wright G 1991 Focal neuronal migration disorders and intractable partial epilepsy: a study of 30 patients Ann. Neurol. 30 741-9
43. Park E H and Durand D M 2006 Role of potassium lateral diffusion in non-synaptic epilepsy: a computational study J. Theor. Biol. 238 666-82
44. Poolos N P and Kocsis J D 1990 Elevated extracellular potassium concentration enhances synaptic activation of N-methyl-D-aspartate receptors in hippocampus Brain Res. 508 7-12
45. Rutecki P A, Lebeda F J and Johnston D 1985 Epileptiform activity induced by changes in extracellular potassium in hippocampus J. Neurophysiol. 54 1363-74
46. Schaffer W M, Kendall B E, Tidd C W and Olsen L F 1993 Transient periodicity and episodic predictability in biological dynamics IMA J. Math. Appl. Med. Biol. 10 227-47
47. Scharfman H E 2007 The neurobiology of epilepsy Curr. Neurol. Neurosci. Rep. 7 348-54
48. Strata F 1998 Intrinsic oscillations in CA3 hippocampal pyramids: physiological relevance to theta rhythm generation Hippocampus 8 666-79
49. Suffczynski P, Kalitzin S and Lopes Da Silva F H 2004 Dynamics of non-convulsive epileptic phenomena modeled by a bistable neuronal network Neuroscience 126 467-84
50. Suffczynski P, Lopes da Silva F, Parra J, Velis D and Kalitzin S 2005 Epileptic transitions: model predictions and experimental validation J. Clin. Neurophysiol. 22 288-99
51. Sutula T, Cascino G, Cavazos J, Parada I and Ramirez L 1989 Mossy fiber synaptic reorganization in the epileptic human temporal lobe Ann. Neurol. 26 321-30
52. Szabo K G, Lai Y C, Tel T and Grebogi C 1996 Critical exponent for gap filling at crisis Phys. Rev. Lett. 77 3102-5
53. Traynelis S F and Dingledine R 1988 Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice J. Neurophysiol. 59 259-76
54. Trujillo L, Olague G, Legrand P and Lutton E 2007 Regularity based descriptor computed from local image oscillations Opt. Exp. 15 6140-5
55. Varela J A, Sen K, Gibson J, Fost J, Abbott L F and Nelson S B 1997 A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex J. Neurosci. 17 7926-40
56. Walz W 2000 Role of astrocytes in the clearance of excess extracellular potassium Neurochem. Int. 36 291-300
57. Wilson M and Bower J M 1992 Cortical oscillations and temporal interactions in a computer simulation of piriform cortex J. Neurophysiol. 67 981-95
58. Wu C, Shen H, Luk W P and Zhang L 2002 A fundamental oscillatory state of isolated rodent hippocampus J. Physiol. 540 509-27
59. Yaari Y, Konnerth A and Heinemann U 1986 Nonsynaptic epileptogenesis in the mammalian hippocampus in vitro: II. Role of extracellular potassium J. Neurophysiol. 56 424-38
60. Zalay O C and Bardakjian B L 2008 Mapped clock oscillators as ring devices and their application to neuronal electrical rhythms IEEE Trans. Neural Syst. Rehabil. Eng. 16 233-44
61. Zalay O C and Bardakjian B L 2009 Theta phase precession and phase selectivity: a cognitive device description of neural coding J. Neural Eng. 6 036002