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Brain Topography

, Volume 32, Issue 3, pp 394–404 | Cite as

Altered Dynamic Functional Network Connectivity in Frontal Lobe Epilepsy

  • Benjamin Klugah-Brown
  • Cheng LuoEmail author
  • Hui He
  • Sisi Jiang
  • Gabriel Kofi Armah
  • Yu Wu
  • Jianfu Li
  • Wenjie Yin
  • Dezhong Yao
Original Paper

Abstract

Frontal lobe epilepsy has recently been associated with disrupted brain functional connectivity; variations among various resting-state networks (RSNs) across time remains largely unclear. This study applied dynamic functional network connectivity (dFNC) analysis to investigate functional patterns in the temporal and spatial domains of various functional systems in FLE. Resting-state fMRI data were acquired from 19 FLE patients and 18 controls. Independent component analysis was used to decompose RSNs, which were grouped into seven functional systems. Sliding windows and clustering approach were used to identify the dFNC patterns. Then, state-specific connectivity pattern and dynamic functional state interactions (dFSIs) were evaluated. Compared with healthy controls, FLE patients exhibited decreased dFNC in almost all four patterns, changes that were mostly related to the frontoparietal system, suggesting a disturbed communication of the frontoparietal system with other systems in FLE. Additionally, regarding the fundamental connectivity pattern (state 3 in this study), FLE showed decreased time spent in this state. Moreover, the duration positively correlated with seizure onset. Furthermore, significantly reduced dynamic connections in this state were observed in the frontoparietal system linked to the cerebellar and subcortical systems. These findings imply abnormal fundamental dynamic interactions and dysconnectivity associated with the subcortical and cerebellar regulation of dysfunctions in frontoparietal regions in FLE. Finally, based on the developed FSI analysis, temporal dynamic abnormalities among states were observed in FLE. Therefore, this altered dynamic FNC extended our understanding of the abnormalities in the frontoparietal system in FLE. The dynamic FNC provided novel insight into the fundamental pathophysiological mechanisms in FLE.

Keywords

Frontal lobe epilepsy Dynamic functional network connectivity Dynamic functional state interaction Resting-state fMRI Double regression 

Notes

Acknowledgements

This work was supported by grants from the National Nature Science Foundation of China (Grant Nos. 81771822, 81471638 and 81330032); The Project of Science and Technology Department of Sichuan Province (Nos. 2017SZ0004 and 2017HH0001); and the ‘111’ project of China (Grant No. B12027). We thank Dr. Jiang and Dr. Wang for their help in collecting data.

Compliance with Ethical Standards

Conflict of interest

None of the authors had any conflicts of interest to disclose. We confirm that we have read the Journal’s position on the issues involved in ethical publication and affirm that this report is consistent with those guidelines.

Supplementary material

10548_2018_678_MOESM1_ESM.docx (6.9 mb)
Supplementary material 1 (DOCX 7043 KB)

References

  1. Allen EA, Damaraju E, Plis SM, Erhardt EB, Eichele T, Calhoun VD (2011) Tracking whole-brain connectivity dynamics in the resting state. Cereb Cortex 24:663–676CrossRefGoogle Scholar
  2. An D, Dubeau F, Gotman J (2015) BOLD responses related to focal spikes and widespread bilateral synchronous discharges generated in the frontal lobe. Epilepsia 56(3):366–374CrossRefGoogle Scholar
  3. Beckmann CF, Mackay CE, Filippini N, Smith SM (2009) Group comparison of resting-state FMRI data using multi-subject ICA and dual regression. NeuroImage 47:S39–S41.  https://doi.org/10.1016/S1053-8119(09)71511-3 CrossRefGoogle Scholar
  4. Beleza P, Pinho J (2011) Frontal lobe epilepsy. J Clin Neurosci 18(5):593–600CrossRefGoogle Scholar
  5. Braakman H, Vaessen M, Hofman P, Debeij-van Hall M, Backes W, Vles J, Aldenkamp A (2011) Cognitive and behavioral complications of frontal lobe epilepsy in children: a review of the literature. Epilepsia 52:849–856CrossRefGoogle Scholar
  6. Braakman H, Vaessen M, Jansen J, Debeij-van Hall M, de Louw A, Hofman P et al (2013) Frontal lobe connectivity and cognitive impairment in pediatric frontal lobe epilepsy. Epilepsia 54:446–454CrossRefGoogle Scholar
  7. Chang C, Glover G (2010) Time frequency dynamics of resting state brain connectivity measured with fMRI. Neuroimage 50:81–98.  https://doi.org/10.1016/j.neuroimage.2009.12.001 CrossRefGoogle Scholar
  8. Damaraju E, Allen E, Belger A, Ford J, McEwen S, Mathalon D et al (2014) Dynamic functional connectivity analysis reveals transient states of dysconnectivity in schizophrenia. NeuroImage:Clinical 5:298–308CrossRefGoogle Scholar
  9. Deco G, Ponce-Alvarez A, Mantini D, Romani G, Hagmann P, Corbetta M (2013) Resting-state functional connectivity emerges from structural and dynamically shaped slow linear fluctuation. J Neurosci 33:11239–11252CrossRefGoogle Scholar
  10. Direito B, Teixeira CA, Sales F, Castelo-Branco M, Dourado A (2017) A realistic seizure prediction study based on multiclass SVM. Int J Neural Syst 27(3):1750006.  https://doi.org/10.1142/S012906571750006X CrossRefGoogle Scholar
  11. Doelken M, Mennecke A, Huppertz H (2012) Multimodality approach in cryptogenic epilepsy with focus on morphometric 3T MRI. J Neuroradiol 39(2):87–96CrossRefGoogle Scholar
  12. Dong L, Wang P, Peng R, Jiang S, Klugah-Brown B, Luo C, Yao D (2016) Altered basal ganglia-cortical functional connections in frontal lobe epilepsy: a resting-state fMRI study. Epilepsy Res 128:12–20CrossRefGoogle Scholar
  13. Dong L, Luo C, Liu X, Jiang S, Feng H, Li J, Gong D, Yao D (2018) Neuroscience information toolbox: an open source toolbox for EEG-fMRI multimodal fusion analysis. Front Neuroinform 12:56CrossRefGoogle Scholar
  14. Engel J Jr, International League Against Epilepsy (ILAE) (2001) A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia 42(6):796–803CrossRefGoogle Scholar
  15. Exner C, Boucsein K, Lange C, Winter H, Weniger G, Steinhoff B, Irle E (2002) Neuropsychological performance in frontal lobe epilepsy. Seizure 11:20–32CrossRefGoogle Scholar
  16. Fletcher P, Henson R (2001) Henson, frontal lobes and human memory. Brain 124:849–881CrossRefGoogle Scholar
  17. Geier C, Lehnertz K (2017) Which brain regions are important for seizure dynamics in epileptic networks? Influence of link identification and EEG recording montage on node centralities. Int J Neural Syst 27(1):1550035.  https://doi.org/10.1142/S0129065715500355 CrossRefGoogle Scholar
  18. Graña M, Ozaeta L, Chyzhyk D (2017) Resting state effective connectivity allows auditory hallucination discrimination. Int J Neural Syst 27(05):1750019.  https://doi.org/10.1142/S0129065717500198 CrossRefGoogle Scholar
  19. Jafri M, GD P, Stevens M, Calhoun V (2008) A method for functional network connectivity among spatially independent resting-state components in schizophrenia. Neuroimage 39:1666–1681CrossRefGoogle Scholar
  20. Jiang S, Luo C, Gong J, Peng R, Ma S, Tan S et al (2017) Aberrant thalamocortical connectivity in juvenile myoclonic epilepsy. Int J Neural Syst.  https://doi.org/10.1142/S0129065717500344 Google Scholar
  21. Jiang Y, Luo C, Li X, Li Y, Yang H, Li J, Chang X, Li H, Yang H, Wang J, Duan M, Yao D (2018) White-matter functional networks changes in patients with schizophrenia. Neuroimage.  https://doi.org/10.1016/j.neuroimage.2018.1004.1018 Google Scholar
  22. Kellinghaus C, Lüders HO (2004) Frontal lobe epilepsy. Epileptic Disord 6(4):223–239Google Scholar
  23. Kros L, Eelkman RO, De Zeeuw C, Hoebeek F (2015a) Controlling cerebellar output to treat refractory epilepsy. Trends Neurosci 38(12):787–799.  https://doi.org/10.1016/j.tins.2015.10.002 CrossRefGoogle Scholar
  24. Kros L, Eelkman ROH, Spanke JK, Alva P, van Dongen MN, Karapatis A et al (2015b) Cerebellar output controls generalized spike-and-wave discharge occurrence. Ann Neurol.  https://doi.org/10.1002/ana.24399 Google Scholar
  25. Li Q, Cao W, Liao X, Chen Z, Yang T, Gong Q et al (2015) Altered resting state functional network connectivity in children absence epilepsy. J Neurol Sci 354(1–2):79–85CrossRefGoogle Scholar
  26. Li J, Zhou W, Yuan S, Zhang Y, Li C, Wu Q (2016) An Improved sparse representation over learned dictionary method for seizure detection. Int J Neural Syst 26(1):1750006.  https://doi.org/10.1142/S012906571750006X Google Scholar
  27. Li Q, Chen Y, Wei Y, Chen S, Ma L, He Z, Chen Z (2017a) Functional network connectivity patterns between idiopathic generalized epilepsy with myoclonic and absence seizures. Front Comput Neurosci.  https://doi.org/10.3389/fncom.2017.00038. (ecollection)Google Scholar
  28. Li R, Ji GJ, Yu Y, Yu Y, Ding MP, Tang YL, Chen H, Liao W (2017b) Epileptic discharge related functional connectivity within and between networks in benign epilepsy with centrotemporal spikes. Int J Neural Syst 27(7):1750018.  https://doi.org/10.1142/S0129065717500186 CrossRefGoogle Scholar
  29. Luo C, Qiu C, Guo Z, Fang J, Li Q, Lei X et al (2012) Disrupted functional brain connectivity in partial epilepsy: a resting-state fMRI study. PLoS ONE 7:e28196CrossRefGoogle Scholar
  30. Luo C, An D, Yao D, Gotman J (2014) Patient-specific connectivity pattern of epileptic network in frontal lobe epilepsy. Neuroimage Clin 4:668–675CrossRefGoogle Scholar
  31. Luo C, Zhang Y, Cao W, Huang Y, Yang F, Wang J et al (2015) Altered structural and functional feature of striato-cortical circuit in benign epilepsy with centrotemporal spikes. Int J Neural Syst 25(6): 1550027CrossRefGoogle Scholar
  32. Mayo Clinic (2008) Mayoclinic. http://Mayoclinic.com. Accessed Sept 2017
  33. McAvoy M, Larson-Prior L, Nolan T, Vaishnavi S, Raichle M, d’Avossa G (2008) Resting states affect spontaneous BOLD oscillation in sensory and paralimbic cortex. J Neurophysiol 100:922–931CrossRefGoogle Scholar
  34. Norden A, Blumenfeld H (2002) The role of subcortical structures in human epilepsy. Epilepsy Behav 3:219–231CrossRefGoogle Scholar
  35. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154CrossRefGoogle Scholar
  36. Rashid B, Damaraju E, Pearlson GD, Calhoun VD (2014) Dynamic connectivity states estimated from resting fMRI Identify differences among Schizophrenia, bipolar disorder, and healthy control subjects. Front Hum Neurosci 8:897.  https://doi.org/10.3389/fnhum.2014.00897. (eCollection 2014)CrossRefGoogle Scholar
  37. Shen K, Hutchison R, Bezgin G, Everling S, McIntosh A (2015) Network structure shapes spontaneous functional connectivity dynamics. J Neurosci 35:5579–5588CrossRefGoogle Scholar
  38. Tan Y, Tan J, Deng J, Cui W, He H, Yang F et al (2015) Alteration of basal ganglia and right frontoparietal network in early drug-naive Parkinson’s disease during heat pain stimuli and resting state. Front Hum Neurosci 9:467CrossRefGoogle Scholar
  39. Tracy J, Doucet G (2015) Resting-state functional connectivity in epilepsy: growing relevance for clinical decision making. Curr Opin Neurol 28(2):158–165CrossRefGoogle Scholar
  40. Wang L, Liu Q, Shen H, Li H, Hu D (2015) Large-scale functional brain network changes in taxi drivers: evidence from resting state fMRI. Hum Brain Mapp 36:862–871CrossRefGoogle Scholar
  41. Williamson P, Jobst B (2000) Frontal lobe epilepsy. In: Williamson P, Siegel A, Roberts D, Thadani V, Gazzaniga M, (eds) Advances in neurology. Raven Press, Philadelphia pp 215–251Google Scholar
  42. Xiaobo C, Han Z, Yue G, Chong-Yaw W, Gang L, Dinggang S, the Alzheimer’s Disease Neuroimaging Initiative (2016) High-order resting-state functional connectivity network for MCI classification. Hum Brain Mapp 37: 3282–3296CrossRefGoogle Scholar
  43. Zhang H, Chen X, Zhang Y, Shen D (2017) Test-Retest Reliability of “high-order” functional connectivity in young healthy adults. Front Neurosci 11:439.  https://doi.org/10.3389/fnins.2017.00439 CrossRefGoogle Scholar
  44. Zhong C, Liu R, Luo C, Jiang S, Dong L, Peng R, Guo F, Wang P (2018) Altered structural and functional connectivity of juvenile myoclonic epilepsy: an fMRI study. Neural Plast.  https://doi.org/10.1155/2018/7392187 Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Benjamin Klugah-Brown
    • 1
  • Cheng Luo
    • 1
    Email author
  • Hui He
    • 1
  • Sisi Jiang
    • 1
  • Gabriel Kofi Armah
    • 2
  • Yu Wu
    • 3
  • Jianfu Li
    • 1
  • Wenjie Yin
    • 3
  • Dezhong Yao
    • 1
  1. 1.The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, School of life Science and technologyUniversity of Electronic Science and Technology of ChinaChengduPeople’s Republic of China
  2. 2.Navrongo Campus, Computer Science DepartmentUniversity for Development studiesTamaleGhana
  3. 3.Department of RadiologyChengdu First People’s HospitalChengduPeople’s Republic of China

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