Skip to main content
SpringerLink
Log in

Stochastic fluctuations of permittivity coupling regulate seizure dynamics in partial epilepsy

  • Article
  • Published:
Science China Technological Sciences Aims and scope Submit manuscript

Abstract

Partial epilepsy is characterized by recurrent seizures that arise from a localized pathological brain region. During the onset of partial epilepsy, the seizure evolution commonly exhibits typical timescale separation phenomenon. This timescale separation behavior can be mimicked by a paradigmatic model termed as Epileptor, which consists of coupled fast-slow neural populations via a permittivity variable. By incorporating permittivity noise into the Epileptor model, we show here that stochastic fluctuations of permittivity coupling participate in the modulation of seizure dynamics in partial epilepsy. In particular, introducing a certain level of permittivity noise can make the model produce more comparable seizure-like events that capture the temporal variability in realistic partial seizures. Furthermore, we observe that with the help of permittivity noise our stochastic Epileptor model can trigger the seizure dynamics even when it operates in the theoretical nonepileptogenic regime. These findings establish a deep mechanistic understanding on how stochastic fluctuations of permittivity coupling shape the seizure dynamics in partial epilepsy, and provide insightful biological implications.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Talairach J, Bancaud J. Lesion, “irritative” zone and epileptogenic focus. Confin Neurol, 2004, 27: 91–94

    Article  Google Scholar 

  2. Wang Y, Goodfellow M, Taylor P N, et al. Dynamic mechanisms of neocortical focal seizure onset. PLoS Comput Biol, 2014, 10: e1003787

    Article  Google Scholar 

  3. Bartolomei F, Wendling F, Bellanger J J, et al. Dynamic mechanisms of neocortical focal seizure onset. PLoS Comput Biol, 2011, 112: 1746–1760

    Google Scholar 

  4. Laxer K D, Trinka E, Hirsch L J, et al. The consequences of refractory epilepsy and its treatment. Epilepsy Behav, 2014, 37: 59–70

    Article  Google Scholar 

  5. Braakman H M H, Vaessen M J, Jansen J F A, et al. Frontal lobe connectivity and cognitive impairment in pediatric frontal lobe epilepsy. Epilepsia, 2013, 54: 446–454

    Article  Google Scholar 

  6. Dinkelacker V, Xin X, Baulac M, et al. Interictal epileptic discharge correlates with global and frontal cognitive dysfunction in temporal lobe epilepsy. Epilepsy Behav, 2016, 62: 197–203

    Article  Google Scholar 

  7. Liao W, Zhang Z, Pan Z, et al. Default mode network abnormalities in mesial temporal lobe epilepsy: A study combining fMRI and DTI. Hum Brain Mapp, 2011, 32: 883–895

    Article  Google Scholar 

  8. Bartolomei F, Guye M, Wendling F. Abnormal binding and disruption in large scale networks involved in human partial seizures. EPJ Nonlinear Biomed Phys, 2013, 1: 4

    Article  Google Scholar 

  9. Leao A A. Spreading depression of activity in the cerebral cortex. J Neurophysiol, 1944, 7: 359–390

    Google Scholar 

  10. Krishnan G P, Bazhenov M. Ionic dynamics mediate spontaneous termination of seizures and postictal depression state. J Neurosci, 2011, 31: 8870–8882

    Article  Google Scholar 

  11. Wendling F, Bartolomei F, Bellanger J J, et al. Epileptic fast activity can be explained by a model of impaired GABAergic dendritic inhibition. Eur J Neurosci, 2002, 15: 1499–1508

    Article  Google Scholar 

  12. Wang Y J, Goodfellow M, Taylor P N, et al. Phase space approach for modeling of epileptic dynamics. Phys Rev E, 2012, 85: 061918

    Article  Google Scholar 

  13. Jirsa V K, Stacey W C, Quilichini P P, et al. On the nature of seizure dynamics. Brain, 2014, 137: 2210–2230

    Article  Google Scholar 

  14. Proix T, Bartolomei F, Chauvel P, et al. Permittivity coupling across brain regions determines seizure recruitment in partial epilepsy. J Neurosci, 2014, 34: 15009–15021

    Article  Google Scholar 

  15. El Houssaini K, Ivanov A I, Bernard C, et al. Seizures, refractory status epilepticus, and depolarization block as endogenous brain activities. Phys Rev E, 2015, 91: 010701

    Article  Google Scholar 

  16. Destexhe A, Rudolph-Lilith M. Neuronal Noise (in English). New York: Springer Press, 2012

    Book  MATH  Google Scholar 

  17. Gerstner W, Kistler W M. Spiking Neuron Models: Single Neurons, Populations, Plasticity. Cambridge: Cambridge University Press, 2002

    Book  MATH  Google Scholar 

  18. Li C, Chen L, Aihara K. Transient resetting: A novel mechanism for synchrony and its biological examples. PLoS Comput Biol, 2006, 2: e103

    Article  Google Scholar 

  19. Wang Q, Duan Z, Perc M, et al. Synchronization transitions on smallworld neuronal networks: Effects of information transmission delay and rewiring probability. Europhys Lett, 2008, 83: 50008

    Article  Google Scholar 

  20. Wang Q, Perc M, Duan Z, et al. Delay-enhanced coherence of spiral waves in noisy Hodgkin-Huxley neuronal networks. Phys Lett A, 2008, 372: 5681–5687

    Article  MATH  Google Scholar 

  21. Guo D, Wang Q, Perc M. Complex synchronous behavior in interneuronal networks with delayed inhibitory and fast electrical synapses. Phys Rev E, 2012, 85: 061905

    Article  Google Scholar 

  22. Neiman A B, Yakusheva T A, Russell D F. Noise-induced transition to bursting in responses of paddlefish electroreceptor afferents. J Neurophysiol, 2007, 98: 2795–2806

    Article  Google Scholar 

  23. Guo D, Li C. Stochastic and coherence resonance in feed-forwardloop neuronal network motifs. Phys Rev E, 2009, 79: 051921

    Article  Google Scholar 

  24. Guo D, Li C. Signal propagation in feedforward neuronal networks with unreliable synapses. J Comput Neurosci, 2011, 30: 567–587

    Article  MathSciNet  Google Scholar 

  25. Guo D, Li C. Stochastic resonance in Hodgkin-Huxley neuron induced by unreliable synaptic transmission. J Theor Biol, 2012, 308: 105–114

    Article  MathSciNet  Google Scholar 

  26. Ma J, Wu Y, Ying H P, et al. Channel noise-induced phase transition of spiral wave in networks of Hodgkin-Huxley neurons. Chin Sci Bull, 2011, 56: 151–157

    Article  Google Scholar 

  27. Ma J, Tang J, Zhang A H, et al. Robustness and breakup of the spiral wave in a two-dimensional lattice network of neurons. Sci China-Phys Mech Astron, 2010, 53: 672–679

    Article  Google Scholar 

  28. Ma J, Jia Y, Tang J, et al. Breakup of spiral waves in coupled Hindmarsh-Rose neurons. Chin Phys Lett, 2008, 25: 4325–4328

    Article  Google Scholar 

  29. Kramer M A, Truccolo W, Eden U T, et al. Human seizures selfterminate across spatial scales via a critical transition. Proc Natl Acad Sci USA, 2012, 109: 21116–21121

    Article  Google Scholar 

  30. Takeshita D, Sato Y D, Bahar S. Transitions between multistable states as a model of epileptic seizure dynamics. Phys Rev E, 2007, 75: 051925

    Article  Google Scholar 

  31. Prusseit J, Lehnertz K. Stochastic qualifiers of epileptic brain dynamics. Phys Rev Lett, 2007, 98: 138103

    Article  Google Scholar 

  32. Heinemann U, Konnerth A, Pumain R, et al. Extracellular calcium and potassium concentration changes in chronic epileptic brain tissue. Adv Neurol, 1986, 44: 641–661

    Google Scholar 

  33. Suh M, Ma H, Zhao M, et al. Neurovascular coupling and oximetry during epileptic events. Mol Neurobiol, 2006, 33: 181–198

    Article  Google Scholar 

  34. Zhao M, Nguyen J, Ma H, et al. Preictal and ictal neurovascular and metabolic coupling surrounding a seizure focus. J Neurosci, 2011, 31: 13292–13300

    Article  Google Scholar 

  35. de Curtis M, Gnatkovsky V. Reevaluating the mechanisms of focal ictogenesis: The role of low-voltage fast activity. Epilepsia, 2009, 50: 2514–2525

    Article  Google Scholar 

  36. Kramer M A, Cash S S. Epilepsy as a disorder of cortical network organization. Neuroscientist, 2012, 18: 360–372

    Article  Google Scholar 

  37. Miley C E, Forster F M. Activation of partial complex seizures by hyperventilation. Archives Neurology, 1977, 34: 371–373

    Article  Google Scholar 

  38. Şenol V, Soyuer F, Arman F, et al. Influence of fatigue, depression, and demographic, socioeconomic, and clinical variables on quality of life of patients with epilepsy. Epilepsy Behav, 2007, 10: 96–104

    Article  Google Scholar 

  39. de Groot M, Reijneveld J C, Aronica E, et al. Epilepsy in patients with a brain tumour: Focal epilepsy requires focused treatment. Brain, 2012, 135: 1002–1016

    Article  Google Scholar 

  40. Misirli H, Ozge A, Somay G, et al. Seizure development after stroke. Int J Clin Pract, 2006, 60: 1536–1541

    Article  Google Scholar 

  41. Szaflarski J P, Nazzal Y, Dreer L E. Post-traumatic epilepsy: Current and emerging treatment options. Neuropsychiatr Dis Treat, 2014, 10: 1469

    Article  Google Scholar 

  42. Chen M, Guo D, Wang T, et al. Bidirectional control of absence seizures by the basal ganglia: A computational evidence. PLoS Comput Biol, 2014, 10: e1003495

    Article  Google Scholar 

  43. Chen M, Guo D, Li M, et al. Critical roles of the direct GABAergic pallido-cortical pathway in controlling absence seizures. PLoS Comput Biol, 2015, 11: e1004539

    Article  Google Scholar 

  44. Hu B, Guo D, Wang Q. Control of absence seizures induced by the pathways connected to SRN in corticothalamic system. Cogn Neurodyn, 2015, 9: 279–289

    Article  Google Scholar 

  45. Fan D, Wang Q, Perc M. Disinhibition-induced transitions between absence and tonic-clonic epileptic seizures. Sci Rep, 2015, 5: 12618

    Article  Google Scholar 

  46. Hu B, Wang Q. Controlling absence seizures by deep brain stimulus applied on substantia nigra pars reticulata and cortex. Chaos Soliton Fract, 2015, 80: 13–23

    Article  MathSciNet  MATH  Google Scholar 

  47. Hu B, Wang Q Y. The conditions for onset of beta oscillations in an extended subthalamic nucleus-globus pallidus network. Sci China Tech Sci, 2014, 57: 2020–2027

    Article  Google Scholar 

  48. Fan D, Liu S, Wang Q. Stimulus-induced epileptic spike-wave discharges in thalamocortical model with disinhibition. Sci Rep, 2016, 6: 37703

    Article  Google Scholar 

  49. Liu S, Wang Q, Fan D. Disinhibition-induced delayed onset of epileptic spike-wave discharges in a five variable model of cortex and thalamus. Front Comput Neurosci, 2016, 10: 28

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Key Laboratory for NeuroInformation of Ministry of Education, School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu, 610054, China

    DaQing Guo, Chuan Xia, ShengDun Wu, TianJiao Zhang, YangSong Zhang, Yang Xia & DeZhong Yao

  2. Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, 610054, China

    DaQing Guo, YangSong Zhang, Yang Xia & DeZhong Yao

  3. School of Computer Science and Technology, Southwest University of Science and Technology, Mianyang, 621002, China

    YangSong Zhang

Authors
  1. DaQing Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chuan Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. ShengDun Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. TianJiao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. YangSong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yang Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. DeZhong Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to DaQing Guo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, D., Xia, C., Wu, S. et al. Stochastic fluctuations of permittivity coupling regulate seizure dynamics in partial epilepsy. Sci. China Technol. Sci. 60, 995–1002 (2017). https://doi.org/10.1007/s11431-017-9030-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11431-017-9030-4

Keywords

Search

Navigation