Skip to content
naulon

No retraction, correction or concern found when last checked on Oct 26, 2026.

Predicting the spatiotemporal diversity of seizure propagation and termination in human focal epilepsy

Timothée Proix, Viktor K. Jirsa, Fabrice Bartolomei and 2 more

Nature Communications · 2018 · CC BY

doi:10.1038/s41467-018-02973-y

Abstract

Recent studies have shown that seizures can spread and terminate across brain areas via a rich diversity of spatiotemporal patterns. In particular, while the location of the seizure onset area is usually invariant across seizures in an individual patient, the source of traveling (2–3 Hz) spike-and-wave discharges during seizures can either move with the slower propagating ictal wavefront or remain stationary at the seizure onset area. Furthermore, although many focal seizures terminate synchronously across brain areas, some evolve into distinct ictal clusters and terminate asynchronously. Here, we introduce a unifying perspective based on a new neural field model of epileptic seizure dynamics. Two main mechanisms, the co-existence of wave propagation in excitable media and coupled-oscillator dynamics, together with the interaction of multiple time scales, account for the reported diversity. We confirm our predictions in seizures and tractography data obtained from patients with pharmacologically resistant epilepsy. Our results contribute toward patient-specific seizure modeling.

Full text

Its licence does not allow us to show the full text. Read it at PubMed Central:

Read at PubMed Central

References 62

  1. 1.

    Hutchings F, et al. Predicting surgery targets in temporal lobe epilepsy through structural connectome based simulations. PLOS Comput. Biol. 2015;11:e1004642.

    Not in our library10.1371/journal.pcbi.1004642

  2. 2.
  3. 3.

    Proix T, Bartolomei F, Guye M, Jirsa VK. Individual brain structure and modelling predict seizure propagation. Brain. 2017;140:641-654.

    Not in our library10.1093/brain/awx004

  4. 4.

    Taylor PN, et al. A computational study of stimulus driven epileptic seizure abatement. PLoS ONE. 2014;9:e114316.

    Not in our library10.1371/journal.pone.0114316

  5. 5.

    Kuhlmann L, Grayden DB, Wendling F, Schiff SJ. Role of multiple-scale modeling of epilepsy in seizure forecasting. J. Clin. Neurophysiol. 2015;32:220-226.

    Not in our library10.1097/wnp.0000000000000149

  6. 6.

    Heck CN, et al. Two-year seizure reduction in adults with medically intractable partial onset epilepsy treated with responsive neurostimulation: final results of the RNS System Pivotal trial. Epilepsia. 2014;55:432-441.

    Not in our library10.1111/epi.12534

  7. 7.

    Aghagolzadeh, M., Hochberg, L. R., Cash, S. S. & Truccolo, W. Predicting seizures from local field potentials recorded via intracortical microelectrode arrays. In IEEE 38th Annual International Conference of the Engineering in Medicine and Biology Society, 6353–6356 (2016).

    Not in our library10.1109/embc.2016.7592181

  8. 8.
  9. 9.

    Kramer MA, et al. Coalescence and fragmentation of cortical networks during focal seizures. J. Neurosci. 2010;30:10076-10085.

    Not in our library10.1523/jneurosci.6309-09.2010

  10. 10.

    Burns SP, et al. Network dynamics of the brain and influence of the epileptic seizure onset zone. Proc. Natl Acad. Sci. 2014;111:E5321-E5330.

    Not in our library10.1073/pnas.1401752111

  11. 11.

    González-Ramírez LR, Ahmed OJ, Cash SS, Wayne CE, Kramer MA. A biologically constrained, mathematical model of cortical wave propagation preceding seizure termination. PLoS Comput. Biol. 2015;11:e1004065.

    Not in our library10.1371/journal.pcbi.1004065

  12. 12.
  13. 13.

    Kramer MA, et al. Human seizures self-terminate across spatial scales via a critical transition. Proc. Natl Acad. Sci. 2012;109:21116-21121.

    Not in our library10.1073/pnas.1210047110

  14. 14.

    Jirsa VK, Stacey WC, Quilichini PP, Ivanov AI, Bernard C. On the nature of seizure dynamics. Brain. 2014;137:2210-2230.

    Not in our library10.1093/brain/awu133

  15. 15.

    Perucca P, Dubeau F, Gotman J. Intracranial electroencephalographic seizure-onset patterns: effect of underlying pathology. Brain. 2013;137:183-196.

    Not in our library10.1093/brain/awt299

  16. 16.

    Truccolo W, et al. Neuronal ensemble synchrony during human focal seizures. J. Neurosci. 2014;34:9927-9944.

    Not in our library10.1523/jneurosci.4567-13.2014

  17. 17.

    Schevon CA, et al. Evidence of an inhibitory restraint of seizure activity in humans. Nat. Commun. 2012;3:1060.

    Not in our library10.1038/ncomms2056

  18. 18.

    Martinet LE, Ahmed OJ, Lepage KQ, Cash SS, Kramer MA. Slow spatial recruitment of neocortex during secondarily generalized seizures and its relation to surgical outcome. J. Neurosci. 2015;35:9477-9490.

    Not in our library10.1523/jneurosci.0049-15.2015

  19. 19.

    Wagner FB, et al. Microscale spatiotemporal dynamics during neocortical propagation of human focal seizures. NeuroImage. 2015;122:114-130.

    Not in our library10.1016/j.neuroimage.2015.08.019

  20. 20.

    Coombes S. Waves, bumps, and patterns in neural field theories. Biol. Cybern. 2005;93:91-108.

    Not in our library10.1007/s00422-005-0574-y

  21. 21.

    Braitenberg V, Schüz A. Anatomy of the Cortex: Statistics and Geometry. 1991.

    Not in our library

  22. 22.

    Nunez PL, Cutillo BA. Neocortical Dynamics and Human EEG Rhythms. 1995.

    Not in our library

  23. 23.

    Ermentrout GB, Kleinfeld D. Traveling electrical waves in cortex: insights from phase dynamics and speculation on a computational role. Neuron. 2001;29:33-44.

    Not in our library10.1016/s0896-6273(01)00178-7

  24. 24.

    Heinemann U, Louvel J. Changes in [Ca2+] o and [K+] o during repetitive electrical stimulation and during pentetrazol induced seizure activity in the sensorimotor cortex of cats. Pflüg. Arch. 1983;398:310-317.

    Not in our library10.1007/bf00657240

  25. 25.

    Kager H, Wadman WJ, Somjen GG. Simulated seizures and spreading depression in a neuron model incorporating interstitial space and ion concentrations. J. Neurophysiol. 2000;84:495-512.

    Not in our library10.1152/jn.2000.84.1.495

  26. 26.

    Frohlich F, Bazhenov M, Iragui-Madoz V, Sejnowski TJ. Potassium dynamics in the epileptic cortex: new insights on an old topic. Neuroscientist. 2007;14:422-433.

    Not in our library10.1177/1073858408317955

  27. 27.

    Ullah G, Cressman JR, Barreto E, Schiff SJ. The influence of sodium and potassium dynamics on excitability, seizures, and the stability of persistent states: II. Network and glial dynamics. J. Comput. Neurosci. 2009;26:171-183.

    Not in our library10.1007/s10827-008-0130-6

  28. 28.

    Ho ECY, Truccolo W. Interaction between synaptic inhibition and glial-potassium dynamics leads to diverse seizure transition modes in biophysical models of human focal seizures. J. Comput. Neurosci. 2016;41:225-244.

    Not in our library10.1007/s10827-016-0615-7

  29. 29.

    Zhao M, et al. Preictal and ictal neurovascular and metabolic coupling surrounding a seizure focus. J. Neurosci. 2011;31:13292-13300.

    Not in our library10.1523/jneurosci.2597-11.2011

  30. 30.

    Wei Y, Ullah G, Schiff SJ. Unification of neuronal spikes, seizures, and spreading depression. J. Neurosci. 2014;34:11733-11743.

    Not in our library10.1523/jneurosci.0516-14.2014

  31. 31.

    Suh M, Ma H, Zhao M, Sharif S, Schwartz TH. Neurovascular coupling and oximetry during epileptic events. Mol. Neurobiol. 2006;33:181-197.

    Not in our library10.1385/mn:33:3:181

  32. 32.

    Wei Y, Ullah G, Ingram J, Schiff SJ. Oxygen and seizure dynamics: II. Computational modeling. J. Neurophysiol. 2014;112:213-223.

    Not in our library10.1152/jn.00541.2013

  33. 33.

    Haken H. Advanced Synergetics: Instabiltiy Hierarchies of Self-Organizing Systems and Devices. 1987.

    Not in our library

  34. 34.

    Avoli M, et al. Specific imbalance of excitatory/inhibitory signaling establishes seizure onset pattern in temporal lobe epilepsy. J. Neurophysiol. 2016;115:3229-3237.

    Not in our library10.1152/jn.01128.2015

  35. 35.

    Trevelyan AJ, Sussillo D, Yuste R. Feedforward inhibition contributes to the control of epileptiform propagation speed. J. Neurosci. 2007;27:3383-3387.

    Not in our library10.1523/jneurosci.0145-07.2007

  36. 36.

    Jirsa VK, Kelso JS. Spatiotemporal pattern formation in neural systems with heterogeneous connection topologies. Phys. Rev. E. 2000;62:8462-8465.

    Not in our library10.1103/physreve.62.8462

  37. 37.

    Jirsa VK. Neural field dynamics with local and global connectivity and time delay. Philos. Trans. R. Soc. A: Math., Phys. Eng. Sci. 2009;367:1131-1143.

    Not in our library10.1098/rsta.2008.0260

  38. 38.

    Saggio, M. L., Spiegler, A., Bernard, C. & Jirsa, V. K. Fast-slow bursters in the unfolding of a high codimension singularity and the ultra-slow transitions of classes. J. Math. Neurosci.7, 7 (2017).

    Not in our library10.1186/s13408-017-0050-8

  39. 39.

    Sanz-Leon P, Knock SA, Spiegler A, Jirsa VK. Mathematical framework for large-scale brain network modeling in the virtual brain. NeuroImage. 2015;111:385-430.

    Not in our library10.1016/j.neuroimage.2015.01.002

  40. 40.

    Spiegler, A., Hansen, E. C. A., Bernard, C., McIntosh, A. R., and Jirsa, V. K. Selective activation of resting-state networks following focal stimulation in a connectome-based network model of the humanBrain. eNeuro3, e0068–16.2016 (2016).

    Not in our library10.1523/eneuro.0068-16.2016

  41. 41.
  42. 42.

    Proix T, Bartolomei F, Chauvel P, Bernard C, Jirsa VK. Permittivity coupling across brain regions determines seizure recruitment in partial epilepsy. J. Neurosci. 2014;34:15009-15021.

    Not in our library10.1523/jneurosci.1570-14.2014

  43. 43.

    Durand DM, Park EH, Jensen AL. Potassium diffusive coupling in neural networks. Philos. Trans. R. Soc. B: Biol. Sci. 2010;365:2347-2362.

    Not in our library10.1098/rstb.2010.0050

  44. 44.

    Amzica F, Massimini M, Manfridi A. Spatial buffering during slow and paroxysmal sleep oscillations in cortical networks of glial cells in vivo. J. Neurosci. 2002;22:1042-1053.

    Not in our library10.1523/jneurosci.22-03-01042.2002

  45. 45.

    Khambhati AN, Davis KA, Lucas TH, Litt B, Bassett DS. Virtual cortical resection reveals push-pull network control preceding seizure evolution. Neuron. 2016;91:1170-1182.

    Not in our library10.1016/j.neuron.2016.07.039

  46. 46.

    Jbabdi S, Johansen-Berg H. Tractography: where do we go from here? Brain Connect. 2011;1:169-183.

    Not in our library10.1089/brain.2011.0033

  47. 47.

    Smith RE, Tournier JD, Calamante F, Connelly A. The effects of SIFT on the reproducibility and biological accuracy of the structural connectome. NeuroImage. 2015;104:253-265.

    Not in our library10.1016/j.neuroimage.2014.10.004

  48. 48.

    Park, Y. S., Hochberg, L. R., Eskandar, E. N., Cash, S. S. & Truccolo, W. Early detection of human focal seizures based on cortical multiunit activity. In 36th Annual International Conference of the IEEE onEngineering in Medicine and Biology Society, 5796–5799 (2014).

    Not in our library10.1109/embc.2014.6944945

  49. 49.
  50. 50.

    Truccolo W, et al. Single-neuron dynamics in human focal epilepsy. Nat. Neurosci. 2011;14:635-641.

    Not in our library10.1038/nn.2782

  51. 51.

    Uva L, et al. A novel focal seizure pattern generated in superficial layers of the olfactory cortex. J. Neurosci. 2017;37:3544-3554.

    Not in our library10.1523/jneurosci.2239-16.2016

  52. 52.

    Jirsa, V., et al. The virtual epileptic patient: individualized whole-brain models of epilepsy spread. NeuroImage145, 377–388 (2017).

    Not in our library10.1016/j.neuroimage.2016.04.049

  53. 53.

    Proix, T., et al. How do parcellation size and short-range connectivity affect dynamics in large-scale brain network models? NeuroImage 142, 135–149 (2016).

    Not in our library10.1016/j.neuroimage.2016.06.016

  54. 54.

    Zalesky A, et al. Whole-brain anatomical networks: does the choice of nodes matter? NeuroImage. 2010;50:970-983.

    Not in our library10.1016/j.neuroimage.2009.12.027

  55. 55.

    El Houssaini, K., Ivanov, A. I., Bernard, C. & Jirsa, V. K. Seizures, refractory status epilepticus, and depolarization block as endogenous brain activities. Phys. Rev. E91, 010701 (2015).

    Not in our library10.1103/physreve.91.010701

  56. 56.

    Coombes S, Lord G, Owen M. Waves and bumps in neuronal networks with axo-dendritic synaptic interactions. Phys. D: Nonlinear Phenom. 2003;178:219-241.

    Not in our library10.1016/s0167-2789(03)00002-2

  57. 57.

    Izhikevich EM. Neural excitability, spiking and bursting. Int. J. Bifurc. Chaos. 2000;10:1171-1266.

    Not in our library10.1142/s0218127400000840

  58. 58.

    Jirsa VK, Jantzen KJ, Fuchs A, Kelso JS. Spatiotemporal forward solution of the eeg and meg using network modeling. IEEE Trans. Med. Imaging. 2002;21:493-504.

    Not in our library10.1109/tmi.2002.1009385

  59. 59.

    Jirsa VK, Ding M. Will a large complex system with time delays be stable? Phys. Rev. Lett. 2004;93:070602.

    Not in our library10.1103/physrevlett.93.070602

  60. 60.

    Feng J, Jirsa VK, Ding M. Synchronization in networks with random interactions: theory and applications. Chaos: Interdiscip. J. Nonlinear Sci. 2006;16:015109.

    Not in our library10.1063/1.2180690

  61. 61.

    Qubbaj MR, Jirsa VK. Neural field dynamics with heterogeneous connection topology. Phys. Rev. Lett. 2007;98:238102.

    Not in our library10.1103/physrevlett.98.238102

  62. 62.

    Petkoski S, et al. Heterogeneity of time delays determines synchronization of coupled oscillators. Phys. Rev. E. 2016;94:012209.

    Not in our library10.1103/physreve.94.012209

Cited by papers we hold 1

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.