Research article

Regulatory role of excitatory interneurons by combining electrical stimulation for absence seizures in the coupled thalamocortical model

  • Received: 26 December 2023 Revised: 01 February 2024 Accepted: 03 February 2024 Published: 19 February 2024
  • The role of excitatory interneurons (EINs) in the cortical has received increasing attention in the discussion of absence seizures. Numerous physiological experiments have confirmed the correlation between EIN and absence seizures. However, the dynamic mechanisms underlying this relationship are not well understood, and there are some challenges in selecting appropriate stimulation strategies for pyramidal clusters. In this study, we incorporated EIN into the previous Taylor model and developed an improved thalamocortical coupled model consisting of ten neuronal populations. Initially, we investigated the excitatory induction effect of EIN to pyramidal clusters and the external input of EIN. Then, four different targeted treatment approaches (deep brain stimulation (DBS), current balanced biphasic pulse (CBBP), 1:0 coordinated resetting stimulation (1:0 CRS), and 3:2 CRS) were applied to the pyramidal clusters. Moreover, we established two quantitative indices to evaluate the stimulation effects. The results showed that modifying the external input of EIN and the coupling strength projected onto the pyramidal clusters can effectively transition the system from an absence seizure state to other normal states. Additionally, inputs from the left compartment were found to reduce the generation of abnormal discharge regions in the right compartment. Furthermore, considering the treatment effects and current consumption, the 3:2 CRS stimulation strategy appeared to be the most suitable treatment approach for the pyramidal clusters. This work introduces a novel coupled model containing EIN, which contributes new theoretical foundations and insights for the future treatment of absence seizures.

    Citation: Quanjun Wu, Zhu Zhang, Ranran Li, Yufan Liu, Yuan Chai. Regulatory role of excitatory interneurons by combining electrical stimulation for absence seizures in the coupled thalamocortical model[J]. Electronic Research Archive, 2024, 32(3): 1533-1550. doi: 10.3934/era.2024070

    Related Papers:

  • The role of excitatory interneurons (EINs) in the cortical has received increasing attention in the discussion of absence seizures. Numerous physiological experiments have confirmed the correlation between EIN and absence seizures. However, the dynamic mechanisms underlying this relationship are not well understood, and there are some challenges in selecting appropriate stimulation strategies for pyramidal clusters. In this study, we incorporated EIN into the previous Taylor model and developed an improved thalamocortical coupled model consisting of ten neuronal populations. Initially, we investigated the excitatory induction effect of EIN to pyramidal clusters and the external input of EIN. Then, four different targeted treatment approaches (deep brain stimulation (DBS), current balanced biphasic pulse (CBBP), 1:0 coordinated resetting stimulation (1:0 CRS), and 3:2 CRS) were applied to the pyramidal clusters. Moreover, we established two quantitative indices to evaluate the stimulation effects. The results showed that modifying the external input of EIN and the coupling strength projected onto the pyramidal clusters can effectively transition the system from an absence seizure state to other normal states. Additionally, inputs from the left compartment were found to reduce the generation of abnormal discharge regions in the right compartment. Furthermore, considering the treatment effects and current consumption, the 3:2 CRS stimulation strategy appeared to be the most suitable treatment approach for the pyramidal clusters. This work introduces a novel coupled model containing EIN, which contributes new theoretical foundations and insights for the future treatment of absence seizures.



    加载中


    [1] Y. Yu, F. Han, Q. Wang, A hippocampal-entorhinal cortex neuronal network for dynamical mechanisms of epileptic seizure, IEEE Trans. Neural Syst. Rehabil. Eng., 31 (2023), 1986–1996. https://doi.org/10.1109/TNSRE.2023.3265581 doi: 10.1109/TNSRE.2023.3265581
    [2] E. Akyuz, A. K. Polat, E. Eroglu, I. Kullu, E. Angelopoulou, Y. N. Paudel, Revisiting the role of neurotransmitters in epilepsy: An updated review, Life Sci., 265 (2021), 118826. https://doi.org/10.1016/j.seizure.2013.01.008 doi: 10.1016/j.seizure.2013.01.008
    [3] R. D. Thijs, R. Surges, T. J. O'Brien, J. W. Sander, Epilepsy in adults, Lancet, 393 (2019), 689–701. https://doi.org/10.1016/S0140-6736(18)32596-0
    [4] S. Gregorčič, J. Hrovat, N. Bizjak, P. Z. Rener, T. Hostnik, B. Stres, et al., Difficult to treat absence seizures in children: A single-center retrospective study, Front. Neurol., 13 (2022), 958369. https://doi.org/10.3389/fneur.2022.958369 doi: 10.3389/fneur.2022.958369
    [5] Z. W. Wong, T. Engel, More than a drug target: Purinergic signalling as a source for diagnostic tools in epilepsy, Neuropharmacology, 222 (2023), 109303. https://doi.org/10.1016/j.neuropharm.2022.109303 doi: 10.1016/j.neuropharm.2022.109303
    [6] R. S. Fisher, C. Acevedo, A. Arzimanoglou, A. Bogacz, J. H. Cross, C. E. Elger, et al., ILAE official report: a practical clinical definition of epilepsy, Epilepsia, 55 (2014), 475–482. https://doi.org/10.1111/epi.12550 doi: 10.1111/epi.12550
    [7] J. Xue, P. Gong, H. Yang, X. Liu, Y. Jiang, Y. Zhang, et al., Genetic (idiopathic) epilepsy with photosensitive seizures includes features of both focal and generalized seizures, Sci. Rep., 8 (2018), 6254. https://doi.org/10.1038/s41598-018-24644-0 doi: 10.1038/s41598-018-24644-0
    [8] Z. Liu, F. Han, Q. Wang, A review of computational models for gamma oscillation dynamics: from spiking neurons to neural masses, Nonlinear Dyn., 108 (2022), 1849–1866. https://doi.org/10.1007/s11071-022-07298-6 doi: 10.1007/s11071-022-07298-6
    [9] D. Pinault, T. J. O'brien, Cellular and network mechanisms of genetically-determined absence seizures, Thalamus Relat. Syst., 3 (2005), 181–203. https://doi.org/10.1017/S1472928807000209 doi: 10.1017/S1472928807000209
    [10] S. Bhattacharya, M. B. L. Cauchois, P. A. Iglesias, Z. S. Chen, The impact of a closed-loop thalamocortical model on the spatiotemporal dynamics of cortical and thalamic traveling waves, Sci. Rep., 11 (2021), 14359. https://doi.org/10.1038/s41598-021-93618-6 doi: 10.1038/s41598-021-93618-6
    [11] P. N. Taylor, Y. Wang, M. Goodfellow, J. Dauwels, F. Moeller, U. Stephani, et al., A computational study of stimulus driven epileptic seizure abatement, PLoS One, 9 (2014), 1–26. https://doi.org/10.1371/journal.pone.0114316 doi: 10.1371/journal.pone.0114316
    [12] S. I. Amari, Characteristics of randomly connected threshold-element networks and network systems, Proc. IEEE, 59 (1971), 35–47. https://doi.org/10.1109/PROC.1971.8087 doi: 10.1109/PROC.1971.8087
    [13] H. R. Wilson, J. D. Cowan, Excitatory and inhibitory interactions in localized populations of model neurons, Biophys. J., 12 (1972), 1–24. https://doi.org/10.1016/S0006-3495(72)86068-5 doi: 10.1016/S0006-3495(72)86068-5
    [14] M. Goodfellow, K. Schindler, G. Baier, Intermittent spike-wave dynamics in a heterogeneous, spatially extended neural mass model, NeuroImage, 55 (2011), 920–932. https://dx.doi.org/10.1016/j.neuroimage.2010.12.074 doi: 10.1016/j.neuroimage.2010.12.074
    [15] P. N. Taylor, J. Thomas, N. Sinha, J. Dauwels, M. Kaiser, T. Thesen, et al., Optimal control based seizure abatement using patient derived connectivity, Front. Neurosci., 9 (2015), 202. https://doi.org/10.3389/fnins.2015.00202 doi: 10.3389/fnins.2015.00202
    [16] S. Liu, Q. Wang, Transition dynamics of generalized multiple epileptic seizures associated with thalamic reticular nucleus excitability: A computational study, Commun. Nonlinear Sci. Numer. Simul., 52 (2017), 203–213. https://doi.org/10.1016/j.cnsns.2017.04.035 doi: 10.1016/j.cnsns.2017.04.035
    [17] Y. Cao, X. He, Y. Hao, Q. Wang, Transition dynamics of epileptic seizures in the coupled thalamocortical network model, Int. J. Bifurcation Chaos, 28 (2018), 1850104. https://doi.org/10.1142/S0218127418501043 doi: 10.1142/S0218127418501043
    [18] L. Yan, H. Zhang, Z. Sun, Z. Shen, Control analysis of electrical stimulation for epilepsy waveforms in a thalamocortical network, J. Theor. Biol., 504 (2020), 110391. https://doi.org/10.1016/j.jtbi.2020.110391 doi: 10.1016/j.jtbi.2020.110391
    [19] Z. Wang, L. Duan, The combined effects of the thalamic feed-forward inhibition and feed-back inhibition in controlling absence seizures, Nonlinear Dyn., 108 (2022), 191–205. https://doi.org/10.1007/s11071-021-07178-5 doi: 10.1007/s11071-021-07178-5
    [20] A. Somarowthu, K. M. Goff, E. M. Goldberg, Two-photon calcium imaging of seizures in awake, head-fixed mice, Cell Calcium, 96 (2021), 102380. https://doi.org/10.1016/j.ceca.2021.102380 doi: 10.1016/j.ceca.2021.102380
    [21] M. Steriade, Interneuronal epileptic discharges related to spike-and-wave cortical seizures in behaving monkeys, Electroencephalogr. Clin. Neurophysiol., 37 (1974), 247–263. https://doi.org/10.1016/0013-4694(74)90028-5 doi: 10.1016/0013-4694(74)90028-5
    [22] S. Tabatabaee, F. Bahrami, M. Janahmadi, The critical modulatory role of spiny stellate cells in seizure onset based on dynamic analysis of a neural mass model, Front. Neurosci., 15 (2021), 743720. https://doi.org/10.3389/fnins.2021.743720 doi: 10.3389/fnins.2021.743720
    [23] L. Yan, H. Zhang, Z. Sun, Z. Cao, Z. Shen, Y. Zhao, Mechanism analysis for excitatory interneurons dominating poly-spike wave and optimization of electrical stimulation, Chaos Interdiscip. J. Nonlinear Sci., 32 (2022). https://doi.org/10.1063/5.0076439
    [24] L. Yan, H. Zhang, Z. Sun, S. Liu, Y. Liu, P. Xiao, Optimization of stimulation waveforms for regulating spike-wave discharges in a thalamocortical model, Chaos, Solitons Fractals, 158 (2022), 112025. https://doi.org/10.1016/j.chaos.2022.112025 doi: 10.1016/j.chaos.2022.112025
    [25] Y. Yu, X. Wang, Q. Wang, Q. Y. Wang, A review of computational modeling and deep brain stimulation: applications to Parkinson's disease, Appl. Math. Mech., 41 (2020), 1747–1768. https://doi.org/10.1007/s10483-020-2689-9 doi: 10.1007/s10483-020-2689-9
    [26] O. V. Popovych, P. A. Tass, Multisite delayed feedback for electrical brain stimulation, Front. Physiol., 9 (2018), 46. https://doi.org/10.3389/fphys.2018.00046 doi: 10.3389/fphys.2018.00046
    [27] Z. Wang, Q. Wang, Stimulation strategies for absence seizures: targeted therapy of the focus in coupled thalamocortical model, Nonlinear Dyn., 96 (2019), 1649–1633. https://doi.org/10.1007/s11071-019-04876-z doi: 10.1007/s11071-019-04876-z
    [28] Y. Yu, Y. Fan, F. Han, G. Luan, Q. Wang, Transcranial direct current stimulation inhibits epileptic activity propagation in a large-scale brain network model, Sci. China Technol. Sci., 66 (2023), 3628–3638. https://doi.org/10.1007/s11431-022-2341-x doi: 10.1007/s11431-022-2341-x
    [29] S. Hou, D. Fan, Q. Wang, Regulating absence seizures by tri-phase delay stimulation applied to globus pallidus internal, Appl. Math. Mech., 43 (2022), 1399–1414. https://doi.org/10.1007/s10483-022-2896-7 doi: 10.1007/s10483-022-2896-7
    [30] P. A. Tass, L. Qin, C. Hauptmann, S. Dovero, E. Bezard, T. Boraud, et al., Coordinated reset has sustained aftereffects in Parkinsonian monkeys, Ann. Neurol., 72 (2012), 816–820. https://doi.org/10.1002/ana.23663 doi: 10.1002/ana.23663
    [31] D. Fan, Q. Wang, Closed-loop control of absence seizures inspired by feedback modulation of basal ganglia to the corticothalamic circuit, IEEE Trans. Neural Syst. Rehabil. Eng., 28 (2020), 581–590. https://doi.org/10.1109/TNSRE.2020.2969426 doi: 10.1109/TNSRE.2020.2969426
    [32] N. Sinha, J. Dauwels, M. Kaiser, S. Cash, W. M. Brandon, Y. Wang, et al., Predicting neurosurgical outcomes in focal epilepsy patients using computational modelling, Brain, 140 (2017), 319–332. https://doi.org/10.1093/brain/aww299 doi: 10.1093/brain/aww299
    [33] D. Fan, Q. Wang, J. Su, H. Xi, Stimulus-induced transitions between spike-wave discharges and spindles with the modulation of thalamic reticular nucleus, J. Comput. Neurosci., 43 (2017), 203–225. https://doi.org/10.1007/s10827-017-0658-4 doi: 10.1007/s10827-017-0658-4
    [34] L. Yin, F. Han, Y. Yu, Q. Wang, A computational network dynamical modeling for abnormal oscillation and deep brain stimulation control of obsessive–compulsive disorder, Cognit. Neurodyn., 17 (2023), 1167–1184. https://doi.org/10.1007/s11571-022-09858-3 doi: 10.1007/s11571-022-09858-3
    [35] X. Wang, Y. Yu, F. H, Q. Wang, Beta-band bursting activity in computational model of heterogeneous external globus pallidus circuits, Commun. Nonlinear Sci. Numer. Simul., 110 (2022), 106388. https://doi.org/10.1016/j.cnsns.2022.106388 { doi: 10.1016/j.cnsns.2022.106388
    [36] Y. Yu, Y. Fan, S. Hou, Q. Wang, Optogenetic stimulation of primary motor cortex regulates beta oscillations in the basal ganglia: A Computational study, Commun. Nonlinear Sci. Numer. Simul., 117 (2023), 106918. https://doi.org/10.1016/j.cnsns.2022.106918 doi: 10.1016/j.cnsns.2022.106918
    [37] K. B. Baker, E. B. Plow, S. Nagel, A. B. Rosenfeldt, R. Gopalakrishnan, C. Clark, et al., Cerebellar deep brain stimulation for chronic post-stroke motor rehabilitation: a phase I trial, Nat. Med., 29 (2023), 2366–2374. https://doi.org/10.1038/s41591-023-02507-0 doi: 10.1038/s41591-023-02507-0
    [38] T. Loddenkemper, A. Pan, S. Neme, K. B. Baker, A. R. Rezai, D. S. Dinner, et al., Deep brain stimulation in epilepsy, J. Clin. Neurophysiol., 18 (2001), 514–532. https://doi.org/10.1097/00004691-200111000-00002 doi: 10.1097/00004691-200111000-00002
    [39] D. Fan, Z. Wang, Q. Wang, Optimal control of directional deep brain stimulation in the parkinsonian neuronal network, Commun. Nonlinear Sci. Numer. Simul., 36 (2016), 219–237. https://doi.org/10.1016/j.cnsns.2015.12.005 doi: 10.1016/j.cnsns.2015.12.005
    [40] J. J. Lippman-Bell, C. Zhou, H. Sun, J. S. Feske, F. E. Jensen, Early-life seizures alter synaptic calcium-permeable AMPA receptor function and plasticity, Mol. Cell. Neurosci., 76 (2016), 11–20. https://doi.org/10.1016/j.mcn.2016.08.002 doi: 10.1016/j.mcn.2016.08.002
    [41] C. H. Tran, M. Vaiana, J. Nakuci, A. Somarowthu, K. M. Goff, N. Goldstein, et al., Interneuron desynchronization precedes seizures in a mouse model of Dravet syndrome, J. Neurosci., 40 (2020), 2764–2755. https://doi.org/10.1523/JNEUROSCI.2370-19.2020 doi: 10.1523/JNEUROSCI.2370-19.2020
    [42] A. Satlin, L. Kramer, A. Laurenza, Development of perampanel in epilepsy, Acta Neurol. Scand., 127 (2013), 3–8. https://doi.org/10.1111/ane.12098 doi: 10.1111/ane.12098
    [43] M. V. Sysoeva, A. Lüttjohann, G. V. Luijtelaar, I. V. Sysoev, Dynamics of directional coupling underlying spike-wave discharges, Neuroscience, 314 (2016), 75–89. https://doi.org/10.1016/j.neuroscience.2015.11.044 doi: 10.1016/j.neuroscience.2015.11.044
    [44] Y. Yu, F. Han, Q. Wang, Q. Y. Wang, Model-based optogenetic stimulation to regulate beta oscillations in Parkinsonian neural networks, Cognit. Neurodyn., 16 (2022), 667–681. https://doi.org/10.1007/s11571-021-09729-3 doi: 10.1007/s11571-021-09729-3
    [45] M. Lv, J. Ma, Multiple modes of electrical activities in a new neuron model under electromagnetic radiation, Neurocomputing, 205 (2016), 375–381. https://doi.org/10.1016/j.neucom.2016.05.004 doi: 10.1016/j.neucom.2016.05.004
  • Reader Comments
  • © 2024 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(370) PDF downloads(57) Cited by(0)

Article outline

Figures and Tables

Figures(8)  /  Tables(1)

Other Articles By Authors

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog