Skip to main content
Log in

Exploring the dynamical transitions on an epileptic hippocampal network model and its modulation strategy based on transcranial magneto-acoustical stimulation

  • Original Paper
  • Published:
Nonlinear Dynamics Aims and scope Submit manuscript

Abstract

The mechanisms of network and transition dynamics of epileptiform activity remain unclear. In general, the transitions of epileptiform discharges comprise slow interictal discharges, ictal discharges and postictal depression. Studies have indicated that network properties and the inherent parameters of neuronal models have great impacts on the transitions. Recently, a novel neuromodulation technique, transcranial magneto-acoustical stimulation (TMAS), has been tested for its efficiency experimentally and computationally. In this paper, we establish a biophysical computational network model of an ictogenic hippocampus area to investigate the underlying transitions mechanisms and reveal neuromodulation mechanisms combined with TMAS. Results demonstrate that long distance connections caused by increased connection probability and the number of nearest-neighbour edges make the network more random and focused. The cooperation of network topological structure and neuronal parameters including ion concentration and inherent external input of neurons could induce epileptic transitions. Moreover, the focused ultrasound transducer has the ability to launch and focus the transcranial ultrasound wave to the hippocampal area in the depth of the three-layer tissue. By coupling with a static magnetic field, the proposed modulated induced TMAS currents can terminate epileptiform activity but consumes more energy by regulating magnetic strength. However, changing modulation frequency was unable to fully suppress seizures. These computational results offer an explanation of the mechanisms of neurodynamics of epileptiform discharges and its neuromodulation by TMAS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Haut, S.R., Nabbout, R.: Recognizing seizure clusters in the community: the path to uniformity and individualization in nomenclature and definition. Epilepsia 63(Suppl. 1), S6–S13 (2022). https://doi.org/10.1111/epi.17346

    Article  Google Scholar 

  2. Sainburg, L.E., Janson, A.P., Johnson, G.W., et al.: Structural disconnection relates to functional changes after temporal lobe epilepsy surgery. Brain (2023). https://doi.org/10.1093/brain/awad117

    Article  Google Scholar 

  3. Bernhardt, B.C., Bonilha, L., Gross, D.W.: Network analysis for a network disorder: the emerging role of graph theory in the study of epilepsy. Epilepsy Behav. Behav. 50, 162–170 (2015). https://doi.org/10.1016/j.yebeh.2015.06.005

    Article  Google Scholar 

  4. Voets, N.L., Beckmann, C.F., Cole, D.M., et al.: Structural substrates for resting network disruption in temporal lobe epilepsy. Brain 135, 2350–2357 (2012). https://doi.org/10.1093/brain/aws137

    Article  Google Scholar 

  5. Watts, D.J., Strogatz, S.H.: Colletive dynamics of ‘small-world’ networks. Nature 393(4), 440–442 (1998). https://doi.org/10.1038/30918

    Article  Google Scholar 

  6. Netoff, T.I., Clewley, R., Arno, S., et al.: Epilepsy in small-world networks. J. Neurosci.Neurosci. 24(37), 8075–8083 (2004). https://doi.org/10.1523/JNEUROSCI.1509-04.2004

    Article  Google Scholar 

  7. Percha, B., Dzakpasu, R., Żochowski, M.: Transition from local to global phase synchrony in small world neural network and its possible implications for epilepsy. Phys. Rev. E 72, 031909 (2005). https://doi.org/10.1103/PhysRevE.72.031909

    Article  Google Scholar 

  8. Scharfman, H.E.: The enigmatic mossy cell of the dentate gyrus. Nat. Rev. Neurosci.Neurosci. 17, 562–575 (2016). https://doi.org/10.1038/nrn.2016.87

    Article  Google Scholar 

  9. Shiri, Z., Manseau, F., Lévesque, M., et al.: Activation of specific neuronal networks leads to different seizure onset types. Ann. Neurol. 79(3), 354–365 (2016). https://doi.org/10.1002/ana.24570

    Article  Google Scholar 

  10. Cordon, T., English, A.W.: Strategies to promote peripheral nerve regeneration: electrical stimulation and/or exercise. Eur. J. Neurosci.Neurosci. 43(3), 336–350 (2016). https://doi.org/10.1111/ejn.13005

    Article  Google Scholar 

  11. Zhang, L., Fan, D., Wang, Q.: Synchronous high-frequency oscillations in inhibitory-dominant network motifs consisting of three dentate gyrus-CA3 systems. Chaos 28, 063101 (2018). https://doi.org/10.1063/1.5017012

    Article  MathSciNet  Google Scholar 

  12. Zhang, L., Ma, Z., Yu, Y., et al.: Examining the low-voltage fast seizure-onset and its response to optogenetic stimulation in a biophysical network model of the hippocampus. Cogn. Neurodyn.. Neurodyn. (2023). https://doi.org/10.1007/s11571-023-09935-1

    Article  Google Scholar 

  13. Yu, Y., Han, F., Wang, Q.: A hippocampal-entorhinal cortex neuronal network for dynamical mechanisms of epileptic seizure. IEEE Trans. Neural Syst. Rehabil. Eng.Rehabil. Eng. 31, 1986–1996 (2022). https://doi.org/10.1109/TNSRE.2023.3265581

    Article  Google Scholar 

  14. Ahn, S., Jun, S.B., Lee, H.W., et al.: Computational modeling of epileptiform activities in medial temporal lobe epilepsy combined with in vitro experiments. J. Comput. Neurosci.Comput. Neurosci. 41, 207–223 (2016). https://doi.org/10.1007/s10827-016-0614-8

    Article  MathSciNet  Google Scholar 

  15. Wendling, F., Benquet, P., Bartolomei, F., et al.: Computational models of epileptiform activity. J. Neurosci. MethodsNeurosci. Methods 260, 233–251 (2016). https://doi.org/10.1016/j.jneumeth.2015.03.027

    Article  Google Scholar 

  16. Curia, G., Longo, D., Biagini, G., et al.: The pilocarpine model of temporal lobe epilepsy. J. Neurosci. MethodsNeurosci. Methods 172, 143–157 (2008). https://doi.org/10.1016/j.jneumeth.2008.04.019

    Article  Google Scholar 

  17. Yu, Y., Hao, Y., Wang, Q.: Model-based optimized phase-deviation deep brain stimulation for Parkinson’s disease. Neural Netw.Netw. 122, 308–319 (2019). https://doi.org/10.1016/j.neunet.2019.11.001

    Article  Google Scholar 

  18. Ben-Menachem, E.: Vagus-nerve stimulation for the treatment of epilepsy. Lancet Neurol. 1, 477–482 (2002). https://doi.org/10.1016/S1474-4422(02)00220-X

    Article  Google Scholar 

  19. Yang, A.-C., Shi, L., Li, L.-M., et al.: Potential protective effects of chronic anterior thalamic nucleus stimulation on hippocampal neurons in epileptic monkeys. Brain Stimul.Stimul. 8, 1049–1057 (2015). https://doi.org/10.1016/j.brs.2015.07.041

    Article  Google Scholar 

  20. Krook-Magnuson, E., Szabo, G.G., Armstrong, C., et al.: Cerebellar directed optogenetic intervention inhibits spontaneous hippocampal seizures in a mouse model of temporal lobe epilepsy. eNeuro 1(1), e.2014 (2014). https://doi.org/10.1523/ENEURO.0005-14.2014

    Article  Google Scholar 

  21. Regner, G.G., Pereira, P., Leffa, D.T., et al.: Preclinical to clinical translation of studies of transcranial direct-current stimulation in the treatment of epilepsy: a systematic review. Front. Neurosci.Neurosci. 12, 189 (2018). https://doi.org/10.3389/fnins.2018.00189

    Article  Google Scholar 

  22. Rabut, C., Yoo, S., Hurt, R.C., et al.: Ultrasound technologies for imaging and modulating neural activity. Neuron 108, 93–110 (2020). https://doi.org/10.1016/j.neuron.2020.09.003

    Article  Google Scholar 

  23. Brinker, S.T., Preiswerk, F., White, P.J., et al.: Focused ultrasound platform for investigating therapeutic neuromodulation across the human hippocampus. Ultrasound Med. Biol. 46(5), 1270–1274 (2020). https://doi.org/10.1016/j.ultrasmedbio.2020.01.007

    Article  Google Scholar 

  24. Zhang, H., Yu, Y., Deng, Z., et al.: Activity pattern analysis of the subthalamopallidal network under ChannelRhodopsin-2 and Halorhodopsin photocurrent control. Chaos Soliton Fract. 138, 109963 (2020). https://doi.org/10.1016/j.chaos.2020.109963

    Article  MathSciNet  Google Scholar 

  25. Zhao, J., Yu, Y., Wang, Q.: Dynamical regulation of epileptiform discharges caused by abnormal astrocyte function with optogenetic stimulation. Chaos Soliton Fract. 164, 112720 (2022). https://doi.org/10.1016/j.chaos.2022.112720

    Article  MathSciNet  Google Scholar 

  26. Norton, S.J.: Can ultrasound be used to stimulate nerve tissue. Biomed. Eng. 2, 6 (2003). https://doi.org/10.1186/1475-925X-2-6

    Article  Google Scholar 

  27. Zhang, Y., Zhang, M., Ling, Z., et al.: The influence of transcranial magnetoacoustic stimulation parameters on the basal ganglia-thalamus neural network in Parkinson’s disease. Front. Neuosci. 15, 761720 (2021). https://doi.org/10.3389/fnins.2021.761720

    Article  Google Scholar 

  28. Yuan, Y., Pang, N., Chen, Y., et al.: A phase-locking analysis of neuronal firing rhythms with transcranial magneto-acoustical stimulation based on the Hodgkin–Huxley neuron model. Front. Comput. Neurosci.Comput. Neurosci. 11, 1 (2017). https://doi.org/10.3389/fncom.2017.00001

    Article  Google Scholar 

  29. Zhou, X., Liu, S., Wang, Y., et al.: High-resolution transcranial electrical stimulation for living mice based on magneto-acoustic effect. Front. Neurosci.Neurosci. 13, 1342 (2019). https://doi.org/10.3389/fnins.2019.01342

    Article  Google Scholar 

  30. McLean, M.J., Engström, S., Zhang, Q., et al.: Effects of a static magnetic filed on audiogenic seizures in black Swiss mice. Epilepsy Res. 80(2–3), 119–131 (2008). https://doi.org/10.1016/j.eplepsyres.2008.03.022

    Article  Google Scholar 

  31. Qiu, Z., Kala, S., Guo, J., et al.: Targeted neurostimulation in mouse brains with non-invasive ultrasound. Cell Rep. 32(7), 108033 (2020). https://doi.org/10.1016/j.celrep.2020.108033

    Article  Google Scholar 

  32. Olufsen, M., Whittington, M., Camperi, M., et al.: New functions for the gamma rhythm: population tuning and preprocessing for the beta rhythm. J. Comput. Neurosci.Comput. Neurosci. 14(1), 33–54 (2003). https://doi.org/10.1023/A:1021124317706

    Article  Google Scholar 

  33. Hodgkin, A.L., Huxley, A.F.: Currents carried by sodium and potassium ions through the membrane of the giant axon of loligo. J. Physiol. 116(4), 449–472 (1952). https://doi.org/10.1113/jphysiol.1952.sp004717

    Article  Google Scholar 

  34. Wang, X., Buzśaki, G.: Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J. Neurosci.Neurosci. 16(20), 6402–6413 (1996). https://doi.org/10.1523/JNEUROSCI.16-20-06402.1996

    Article  Google Scholar 

  35. Kopell, N., Börgers, C., Pervouchine, D., et al.: Gamma and theta rhythms in biophysical models of hippocampal circuits. In: Cutsuridis, V., Graham, B., Cobb, S., et al. (eds.) Hippocampal Microcircuits. Springer Series in Computational Neuroscience, vol. 5, pp. 423–457. Springer, New York (2010)

    Google Scholar 

  36. Bernhardt, B.C., Chen, Z., He, Y., et al.: Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. Cereb. Cortex. Cortex 21, 2147–2157 (2011). https://doi.org/10.1093/cercor/bhq291

    Article  Google Scholar 

  37. Montalibet, A., Jossinet, J., Matias, A., Cathignol, D.: Electric current generated by ultrasonically induced Lorentz force in biological media. Med. Biol. Eng. Comput.Comput. 39, 15–20 (2001). https://doi.org/10.1007/BF02345261

    Article  Google Scholar 

  38. Yuan, Y., Chen, Y., Li, X.: Theoretic analysis of transcranial magneto-acoustical stimulation with Hodgkin–Huxley neuron model. Front. Comput. Neurosci.Comput. Neurosci. 10, 35 (2016). https://doi.org/10.3389/fncom.2016.00035

    Article  Google Scholar 

  39. Hendee, W.R., Ritenour, E.R.: Medical Imaging Physics, 4th edn. Wiley, New York (2002)

    Book  Google Scholar 

  40. Treeby, B.E., Cox, B.T.: k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields. J. Biomed. Opt. 15(2), 021314 (2010). https://doi.org/10.1117/1.3360308

    Article  Google Scholar 

  41. Tufail, Y., Yoshihiro, A., Pati, S., et al.: Ultrasonic neuromodulation by brain stimulation with transcranial ultrasound. Nat. Protoc.Protoc. 6, 1453–1470 (2011). https://doi.org/10.1038/nprot.2011.371

    Article  Google Scholar 

  42. Gnatkovsky, V., Librizzi, L., Trombin, F., et al.: Fast activity at seizure onset is mediated by inhibitory circuits in the entorhinal cortex in vitro. Ann. Neurol. 64, 674–686 (2008). https://doi.org/10.1002/ana.21519

    Article  Google Scholar 

  43. Magloire, V., Savtchenko, L.P., Jensen, T.P., et al.: Volume-transmitted GABA waves pace epileptiform rhythms in the hippocampal network. Curr. Biol. 33, 1–16 (2023). https://doi.org/10.1016/j.cub.2023.02.051

    Article  Google Scholar 

  44. Barrio, R., Ibáñez, S., Pérez, L., et al.: Spike-adding structure in fold/hom bursters. Commun. Nonlinear Sci. Numer. Simul.. Nonlinear Sci. Numer. Simul. 83, 105100 (2020). https://doi.org/10.1016/j.cnsns.2019.105100

    Article  MathSciNet  Google Scholar 

  45. Barreto, E., Cressman, J.R.: Ion concentration dynamics as a mechanism for neuronal bursting. J. Biol. Phys. 37, 361–373 (2010). https://doi.org/10.1007/s10867-010-9212-6

    Article  Google Scholar 

  46. Florence, G., Pereira, T., Kurth, J.: Extracellular potassium dynamics in the hyperexcitable state of the neuronal ictal activity. Commun. Nonlinear Sci. Numer. Simul.. Nonlinear Sci. Numer. Simul. 17, 4700–4706 (2012). https://doi.org/10.1016/j.cnsns.2011.06.023

    Article  MathSciNet  Google Scholar 

  47. Howe, T., Blockeel, A.J., Taylor, H., et al.: NMDA receptors promote hippocampal sharp-wave ripples and the associated coactivity of CA1 pyramidal cells. Hippocampus 30, 1356–1370 (2020). https://doi.org/10.1002/hipo.23276

    Article  Google Scholar 

  48. Wang, Y., Feng, L., Liu, S., et al.: Transcranial magneto-acoustic stimulation improves neuroplasticity in hippocampus Parkinson’s disease model mice. Neurotherapeutics 16(4), 1210–1224 (2019). https://doi.org/10.1007/s13311-019-00732-5

    Article  Google Scholar 

  49. Liu, R., Ma, R., Liu, X., et al.: A noninvasive deep brain stimulation method via temporal-spatial interference magneto-acoustic effects: simulation and experimental validation. IEEE Trans. Ultrason. Ferroelectr. Freq. ControlUltrason. Ferroelectr. Freq. Control 69(8), 2474–2483 (2022). https://doi.org/10.1109/TUFFC.2022.3187748

    Article  Google Scholar 

Download references

Funding

This research was supported by the National Natural Science Foundation of China (Grant Nos. 12102014, 11932003, 32271361 and 12202022) and the National Key Research and Development Program of China (Grant Nos. 2021YFA1000200 and 2021YFA1000202).

Author information

Authors and Affiliations

Authors

Contributions

LZ: Conceptualization, Methodology, Software, Writing original draft, Writing-reviewing and editing. YX: Designed, Performed the research, Analyzed the data, Writing the original draft. GB: Conceptualization, Methodology, Writing-reviewing and editing. YL: Conceptualization, Writing-reviewing. BL: Conceptualization, Methodology, Software, Writing-reviewing and editing.

Corresponding author

Correspondence to Bao Li.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, L., Xu, Y., Baier, G. et al. Exploring the dynamical transitions on an epileptic hippocampal network model and its modulation strategy based on transcranial magneto-acoustical stimulation. Nonlinear Dyn (2024). https://doi.org/10.1007/s11071-024-09476-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11071-024-09476-0

Keywords

Navigation