Regulating absence seizures by tri-phase delay stimulation applied to globus pallidus internal

doi:10.1007/s10483-022-2896-7

摘要/Abstract

摘要： In this paper, a reduced globus pallidus internal (GPI)-corticothalamic (GCT) model is developed, and a tri-phase delay stimulation (TPDS) with sequentially applying three pulses on the GPI representing the inputs from the striatal $D_{1}$ neurons, subthalamic nucleus (STN), and globus pallidus external (GPE), respectively, is proposed. The GPI is evidenced to control absence seizures characterized by 2Hz-4,Hz spike and wave discharge (SWD). Hence, based on the basal ganglia-thalamocortical (BGCT) model, we firstly explore the triple effects of $D_{1}$-GPI, GPE-GPI, and STN-GPI pathways on seizure patterns. Then, using the GCT model, we apply the TPDS on the GPI to potentially investigate the alternative and improved approach if these pathways to the GPI are blocked. The results show that the striatum $D_{1}$, GPE, and STN can indeed jointly and significantly affect seizure patterns. In particular, the TPDS can effectively reproduce the seizure pattern if the $D_{1}$-GPI, GPE-GPI, and STN-GPI pathways are cut off. In addition, the seizure abatement can be obtained by well tuning the TPDS stimulation parameters. This implies that the TPDS can play the surrogate role similar to the modulation of basal ganglia, which hopefully can be helpful for the development of the brain-computer interface in the clinical application of epilepsy.

关键词: epileptic absence seizure, spike and wave discharge (SWD), tri-phase delay stimulation (TPDS), mean field model, seizure control

Abstract: In this paper, a reduced globus pallidus internal (GPI)-corticothalamic (GCT) model is developed, and a tri-phase delay stimulation (TPDS) with sequentially applying three pulses on the GPI representing the inputs from the striatal $D_{1}$ neurons, subthalamic nucleus (STN), and globus pallidus external (GPE), respectively, is proposed. The GPI is evidenced to control absence seizures characterized by 2Hz-4,Hz spike and wave discharge (SWD). Hence, based on the basal ganglia-thalamocortical (BGCT) model, we firstly explore the triple effects of $D_{1}$-GPI, GPE-GPI, and STN-GPI pathways on seizure patterns. Then, using the GCT model, we apply the TPDS on the GPI to potentially investigate the alternative and improved approach if these pathways to the GPI are blocked. The results show that the striatum $D_{1}$, GPE, and STN can indeed jointly and significantly affect seizure patterns. In particular, the TPDS can effectively reproduce the seizure pattern if the $D_{1}$-GPI, GPE-GPI, and STN-GPI pathways are cut off. In addition, the seizure abatement can be obtained by well tuning the TPDS stimulation parameters. This implies that the TPDS can play the surrogate role similar to the modulation of basal ganglia, which hopefully can be helpful for the development of the brain-computer interface in the clinical application of epilepsy.

Key words: epileptic absence seizure, spike and wave discharge (SWD), tri-phase delay stimulation (TPDS), mean field model, seizure control

中图分类号:

Songan HOU, Denggui FAN, Qingyun WANG. Regulating absence seizures by tri-phase delay stimulation applied to globus pallidus internal[J]. Applied Mathematics and Mechanics (English Edition), 2022, 43(9): 1399-1414.

参考文献

[1] PANAYIOTOPOULOS, C. P. Typical absence seizures and their treatment. Archives of Disease in Childhood, 81(4), 351-355(1999)
[2] MOSHÉ, S. L., PERUCCA, E., RYVLIN, P., and TOMSON, T. Epilepsy:new advances. The Lancet, 385(9971), 884-898(2015)
[3] DURÓN, R. M., MEDINA, M. T., MARTÍNEZ-JUÁREZ, I, E., BAILEY, J. N., PEREZGOSIENGFIAO, K. T., RAMOS-RAMÍREZ, R., LÓPEZ-RUIZ, M., ALONSO, M. E., ORTEGA, R. H., PASCUAL-CASTROVIEJO, I., MACHADO-SALAS, J., MIJA, L., and DELGADOESCUETA, A. V. Seizures of idiopathic generalized epilepsies. Epilepsia, 46(s9), 34-47(2005)
[4] VOLMAN, V., PERC, M., and BAZHENOV, M. Gap junctions and epileptic seizures-two sides of the same coin? PLoS One, 6(5), e20572(2011)
[5] JASPER, H. and KERSHMAN, J. Electroencephalographic classification of the epilepsies. Archives of Neurology and Psychiatry, 45(6), 903-943(1941)
[6] LÜTTJOHANN, A. and VAN LUIJTELAAR, G. Thalamic stimulation in absence epilepsy. Epilepsy Research, 106(1), 136-145(2013)
[7] LÜTTJOHANN, A., SCHOFFELEN, J. M., and VAN LUIJTELAAR, G. Termination of ongoing spike-wave discharges investigated by cortico-thalamic network analyses. Neurobiology of Disease, 70, 127-137(2014)
[8] PAZ, J. T., DAVIDSON, T. J., FRECHETTE, E. S., DELORD, B., PARADA, I., PENG, K., DEISSEROTH, K., and HUGUENARD, J. R. Closed-loop optogenetic control of thalamus as a tool for interrupting seizures after cortical injury. Nature Neuroscience, 16(1), 64-70(2013)
[9] MARESCAUX, C. and VERGNES, M. Genetic absence epilepsy in rats from strasbourg (GAERS). Italian Journal of Neurological Sciences, 16(1), 113-118(1995)
[10] COENEN, A. M. L. and VAN LUIJTELAAR, E. L. J. M. Genetic animal models for absence epilepsy:a review of the WAG/Rij strain of rats. Behavior Genetics, 33(6), 635-655(2003)
[11] TIMOFEEV, I. and STERIADE, M. Neocortical seizures:initiation, development and cessation. Neuroscience, 123(2), 299-336(2004)
[12] LYTTON, W. W. Computer modelling of epilepsy. Nature Reviews Neuroscience, 9(8), 626-637(2008)
[13] DESTEXHE, A. Spike-and-wave oscillations based on the properties of GABAb receptors. Journal of Neuroscience the Offcial Journal of the Society for Neuroscience, 18(21), 9099-9111(1998)
[14] DESTEXHE, A. Can GABAa conductances explain the fast oscillation frequency of absence seizures in rodents? European Journal of Neuroscience, 11(6), 2175-2181(1999)
[15] SUFFCZYNSKI, P., KALITZIN, S., and DA SILVA, F. H. Dynamics of non-convulsive epileptic phenomena modeled by a bistable neuronal network. Neuroscience, 126(2), 467-484(2004)
[16] 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. Cerebral Cortex, 16(9), 1296-1313(2006)
[17] DA SILVA, F. L., BLANES, W., KALITZIN, S. N., PARRA, J., SUFFCZYNSKI, P., and VELIS, D. N. Epilepsies as dynamical diseases of brain systems:basic models of the transition between normal and epileptic activity. Epilepsia, 44(s12), 72-83(2003)
[18] CHEN, M. M., GUO, D. Q., WANG, T. B., JING, W., and XIA, Y. Bidirectional control of absence seizures by the basal ganglia:a computational evidence. PLoS Computational Biology, 10(3), e1003495(2014)
[19] CHEN, M. M., GUO, D. Q., LI, M., MA, T., WU, S. D., YAN, J. J., and XIA, Y. Critical roles of the direct gabaergic pallido-cortical pathway in controlling absence seizures. PLoS Computational Biology, 11(10), e1004539(2015)
[20] DERANSART, C., VERCUEIL, L., MARESCAUX, C., and DEPAULIS, A. The role of basal ganglia in the control of generalized absence seizures. Epilepsy Research, 32(1), 213-223(1998)
[21] LUO, C., LI, Q., XIA, Y., LEI, X., XUE, K., YANG, Z., MARTÍNEZ-MONTES, E., LIAO, W., and ZHOU, D. Resting state basal ganglia network in idiopathic generalized epilepsy. Human Brain Mapping, 33(6), 1279-1294(2012)
[22] PAZ, J. T., CHAVEZ, M., SAILLET, S., DENIAU, J. M., and CHARPIER, S. Activity of ventral medial thalamic neurons during absence seizures and modulation of cortical paroxysms by the nigrothalamic pathway. Journal of Neuroscience the Offcial Journal of the Society for Neuroscience, 27(4), 929-941(2007)
[23] MANNING, J. P. A., RICHARDS, D. A., and BOWERY, N. G. Pharmacology of absence epilepsy. Trends in Pharmacological Sciences, 24(10), 542-549(2003)
[24] MASUR, D., SHINNAR, S., CNAAN, A., SHINNAR, R. C., and GLAUSER, T. A. Pretreatment cognitive deficits and treatment effects on attention in childhood absence epilepsy. Neurology, 81(18), 1572-1580(2013)
[25] RUSSO, E., CITRARO, R., SCICCHITANO, F., DE FAZIO, S., PAOLA, E. D. D., CONSTANTI, A., and DE SARRO, G. Comparison of the antiepileptogenic effects of an early long-term treatment with ethosuximide or levetiracetam in a genetic animal model of absence epilepsy. Epilepsia, 51(8), 1560-1569(2010)
[26] KWAN, P., ARZIMANOGLOU, A., BERG, A. T., BRODIE, M. J., HAUSER, A., MATHERN, G., MOSHÉ, S. L., PERUCCA, E., WIEBE, S., and FRENCH, J. Definition of drug resistant epilepsy:consensus proposal by the ad hoc task force of the ilae commission on therapeutic strategies. Epilepsia, 51(6), 1069-1077(2010)
[27] BENABID, A. L., CHABARDES, S., MITROFANIS, J., and POLLAK, P. Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson's disease. The Lancet Neurology, 8(1), 67-81(2009)
[28] KILE, K. B., TIAN, N., and DURAND, D. M. Low frequency stimulation decreases seizure activity in a mutation model of epilepsy. Epilepsia, 51(9), 1745-1753(2010)
[29] BIKSON, M. Suppression of epileptiform activity by high frequency sinusoidal fields in rat hippocampal slices. Journal of Physiology, 531(1), 181-191(2001)
[30] CHIANG, C. C., LIN, C. C. K., JU, M. S., and DURAND, D. M. High frequency stimulation can suppress globally seizures induced by 4-AP in the rat hippocampus:an acute in vivo study. Brain Stimulation, 6(2), 180-189(2013)
[31] FAN, D., ZHENG, Y., YANG, Z., and WANG, Q. Improving control effects of absence seizures using single-pulse alternately resetting stimulation (SARS) of corticothalamic circuit. Applied Mathematics and Mechanics (English Edition), 41(9), 1287-1302(2020) https://doi.org/10.1007/s10483020-2644-8
[32] YU, Y., WANG, X., WANG, Q., and WANG, Q. A review of computational modeling and deep brain stimulation:applications to Parkinson's disease. Applied Mathematics and Mechanics (English Edition), 41(12), 1747-1768(2020) https://doi.org/10.1007/s10483-020-2689-9
[33] HAGHIGHI, H. S. and MARKAZI, A. H. D. Control of epileptic seizures by electrical stimulation:a model-based study. Biomedical Physics and Engineering Express, 7(6), 065009(2021)
[34] BORDEY, A. Treating seizures with low-frequency electrical stimulation. Epilepsy Currents, 21(3), 197-198(2021)
[35] ZHANG, H., ZHAO, Y., SHEN, Z., CHEN, F., CAO, Z., and SHAN, W. Control analysis of optogenetics and deep brain stimulation targeting basal ganglia for Parkinson's disease. Era, 30(6), 2263-2282(2022)
[36] TAKEUCHI, Y., HARANGOZÓ, M., PEDRAZA, L., FLDI, T., KOZÁK, G., LI, Q., and BERÉNYI, A. Closed-loop stimulation of the medial septum terminates epileptic seizures. Brain, 144(3), 885-908(2021)
[37] STIEVE, B. J., RICHNER, T. J., KROOK-MAGNUSON, C., NETOFF, T. I., and KROOKMAGNUSON, E. Optimization of closed-loop electrical stimulation enables robust cerebellardirected seizure control. Brain, awac051(2022)
[38] WYCKHUYS, T., RAEDT, R., VONCK, K., WADMAN, W., and BOON, P. Comparison of hippocampal deep brain stimulation with high (130Hz) and low frequency (5Hz) on afterdischarges in kindled rats. Epilepsy Research, 88(2), 239-246(2010)
[39] BRIEN, T. J., MORRIS, M. J., REID, C. A., JOVANOVSKA, V., BRIEN, P., VAN RAAY, L., GANDRATHI, A. K., and PINAULT, D. Rhythmic neuronal activity in S2 somatosensory and insular cortices contribute to the initiation of absence-related spike-and-wave discharges. Epilepsia, 53(11), 1948-1958(2012)
[40] NAMBU, A., TOKUNO, H., HAMADA, I., KITA, H., and HASEGAWA, N. Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. Journal of Neurophysiology, 84(1), 289-300(2000)
[41] NAMBU, A., TAKADA, M., INASE, M., and TOKUNO, H. Dual somatotopical representations in the primate subthalamic nucleus:evidence for ordered but reversed body-map transformations from the primary motor cortex and the supplementary motor area. Journal of Neuroscience, 16(8), 2671(1996)
[42] EJ MÜLLER, ALBADA, S. V., KIM, J. W., and ROBINSON, P. A. Unified neural field theory of brain dynamics underlying oscillations in Parkinson's disease and generalized epilepsies. Journal of Theoretical Biology, 428, 132-146(2017)
[43] VAN ALBADA, S. J. and ROBINSON, P. A. Mean-field modeling of the basal gangliathalamocortical system, I:firing rates in healthy and parkinsonian states. Journal of Theoretical Biology, 257(4), 642-663(2009)
[44] VAN ALBADA, S. J., GRAY, R. T., DRYSDALE, P. M., and ROBINSON, P. A. Mean-field modeling of the basal ganglia-thalamocortical system, II:dynamics of parkinsonian oscillations. Journal of Theoretical Biology, 257(4), 664-688(2009)
[45] ROBINSON, P. A., RENNIE, C. J., and ROWE, D. L. Dynamics of large-scale brain activity in normal arousal states and epileptic seizures. Physical Review E, 65(4), 041924(2002)
[46] ROBINSON, P. A., RENNIE, C. J., WRIGHT, J. J., and BOURKE, P. D. Steady states and global dynamics of electrical activity in the cerebral cortex. Physical Review E, 58(3), 3557(1998)
[47] ROBINSON, P. A., RENNIE, C. J., and WRIGHT, J. J. Propagation and stability of waves of electrical activity in the cerebral cortex. Physical Review E, 56(1), 826(1997)
[48] FREYER, F., ROBERTS, J. A., BECKER, R., ROBINSON, P. A., RITTER, P., and BREAKSPEAR, M. Biophysical mechanisms of multistability in resting-state cortical rhythms. Journal of Neuroscience, 31(17), 6353-6361(2011)
[49] MARTEN, F., RODRIGUES, S., BENJAMIN, O., RICHARDSON, M. P., and TERRY, J. R. Onset of polyspike complexes in a mean-field model of human electroencephalography and its application to absence epilepsy. Philosophical Transactions of the Royal Society A:Mathematical; Physical and Engineering Sciences, 367(1891), 1145-1161(2009)
[50] ROBINSON, P. A., RENNIE, C. J., ROWE, D. L., and O'CONNOR, S. C. Estimation of multiscale neurophysiologic parameters by electroencephalographic means. Human Brain Mapping, 23(1), 53-72(2004)