Brain Topography

, Volume 30, Issue 5, pp 639–655 | Cite as

Simultaneous Intracranial EEG-fMRI Shows Inter-Modality Correlation in Time-Resolved Connectivity Within Normal Areas but Not Within Epileptic Regions

  • Ben Ridley
  • Jonathan Wirsich
  • Gaelle Bettus
  • Roman Rodionov
  • Teresa Murta
  • Umair Chaudhary
  • David Carmichael
  • Rachel Thornton
  • Serge Vulliemoz
  • Andrew McEvoy
  • Fabrice Wendling
  • Fabrice Bartolomei
  • Jean-Philippe Ranjeva
  • Louis Lemieux
  • Maxime Guye
Original Paper

Abstract

For the first time in research in humans, we used simultaneous icEEG-fMRI to examine the link between connectivity in haemodynamic signals during the resting-state (rs) and connectivity derived from electrophysiological activity in terms of the inter-modal connectivity correlation (IMCC). We quantified IMCC in nine patients with drug-resistant epilepsy (i) within brain networks in ‘healthy’ non-involved cortical zones (NIZ) and (ii) within brain networks involved in generating seizures and interictal spikes (IZ1) or solely spikes (IZ2). Functional connectivity (h2) estimates for 10 min of resting-state data were obtained between each pair of electrodes within each clinical zone for both icEEG and fMRI. A sliding window approach allowed us to quantify the variability over time of h2 (vh2) as an indicator of connectivity dynamics. We observe significant positive IMCC for h2 and vh2, for multiple bands in the NIZ only, with the strongest effect in the lower icEEG frequencies. Similarly, intra-modal h2 and vh2 were found to be differently modified as a function of different epileptic processes: compared to NIZ, \(h_{\text{BOLD}}^{2}\) was higher in IZ1, but lower in IZ2, while \(h_{\text{icEEG}}^{2}\) showed the inverse pattern. This corroborates previous observations of inter-modal connectivity discrepancies in pathological cortices, while providing the first direct invasive and simultaneous comparison in humans. We also studied time-resolved FC variability multimodally for the first time, finding that IZ1 shows both elevated internal \(h_{\text{BOLD}}^{2}\) and less rich dynamical variability, suggesting that its chronic role in epileptogenesis may be linked to greater homogeneity in self-sustaining pathological oscillatory states.

Keywords

Connectivity Multimodal imaging Resting-state Focal epilepsy Dynamic connectivity 

Abbreviations

ECoG

Electrocorticography

FC

Functional connectivity

FLE

Frontal lobe epilepsy

IED

Interictal epileptic discharges

icEEG

Intracranial electroencephalography

ICN

Intrinsic connectivity network

IZ

Irritative zone

NIZ

Non-involved zone

TLE

Temporal lobe epilepsy

SEEG

Stereo-electroencephalography

Notes

Acknowledgements

Data for this was acquired at UCLH/UCL who received a proportion of funding from the Department of Health’s NIHR Biomedical Research Centres funding scheme. We acknowledge the financial support of the UK Medical Research Council (MRC grant G0301067). Processing and analysis were undertaken at CRMBM/CEMEREM. This work was also supported with funds from the Swiss National Science Foundation (141165 and 140332, SPUM Epilepsy).

Compliance with Ethical Standards

Conflict of interest

The authors declare no competing financial interests.

Ethical Approval

The authors obtained written informed consent from all patients, in compliance with the ethical requirements of the Declaration of Helsinki and the Joint Research Ethics Committee of the NHNN (UCLH NHS Foundation Trust) and UCL Institute of Neurology.

Supplementary material

10548_2017_551_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 18 KB)
10548_2017_551_MOESM2_ESM.tif (73 kb)
Supplementary material 2 (TIF 73 KB)

References

  1. Allen PJ, Josephs O, Turner R (2000) A method for removing imaging artifact from continuous EEG recorded during functional MRI. NeuroImage 12:230–239. doi:10.1006/nimg.2000.0599 CrossRefPubMedGoogle Scholar
  2. Bartolomei F, Bettus G, Stam CJ, Guye M (2013a) Interictal network properties in mesial temporal lobe epilepsy: a graph theoretical study from intracerebral recordings. Clin Neurophysiol Off J Int Fed. Clin Neurophysiol. doi:10.1016/j.clinph.2013.06.003 Google Scholar
  3. Bartolomei F, Guye M, Wendling F (2013b) Abnormal binding and disruption in large scale networks involved in human partial seizures. EPJ Nonlinear Biomed Phys 1:1–16. doi:10.1140/epjnbp11 CrossRefGoogle Scholar
  4. Bartolomei F, Trébuchon A, Bonini F et al (2016) What is the concordance between the seizure onset zone and the irritative zone? A SEEG quantified study. Clin Neurophysiol Off J Int Fed Clin Neurophysiol 127:1157–1162. doi:10.1016/j.clinph.2015.10.029 CrossRefGoogle Scholar
  5. Bénar CG, Grova C, Kobayashi E, Bagshaw AP, Aghakhani Y, Dubeau F, Gotman J (2006) EEG-fMRI of epileptic spikes: concordance with EEG source localization and intracranial EEG. Neuroimage 30(4):1161–1170. doi:10.1016/j.neuroimage.2005.11.008 CrossRefPubMedGoogle Scholar
  6. Bettus G, Wendling F, Guye M et al (2008) Enhanced EEG functional connectivity in mesial temporal lobe epilepsy. Epilepsy Res 81:58–68. doi:10.1016/j.eplepsyres.2008.04.020 CrossRefPubMedGoogle Scholar
  7. Bettus G, Guedj E, Joyeux F et al (2009) Decreased basal fMRI functional connectivity in epileptogenic networks and contralateral compensatory mechanisms. Hum Brain Mapp 30:1580–1591. doi:10.1002/hbm.20625 CrossRefPubMedGoogle Scholar
  8. Bettus G, Bartolomei F, Confort-Gouny S et al (2010) Role of resting state functional connectivity MRI in presurgical investigation of mesial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 81:1147–1154. doi:10.1136/jnnp.2009.191460 CrossRefPubMedGoogle Scholar
  9. Bettus G, Ranjeva J-P, Wendling F, et al (2011) Interictal functional connectivity of human epileptic networks assessed by intracerebral EEG and BOLD signal fluctuations. PloS ONE 6:e20071. doi:10.1371/journal.pone.0020071 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bourien J, Bartolomei F, Bellanger JJ et al (2005) A method to identify reproducible subsets of co-activated structures during interictal spikes. Application to intracerebral EEG in temporal lobe epilepsy. Clin Neurophysiol Off J Int Fed. Clin Neurophysiol 116:443–455. doi:10.1016/j.clinph.2004.08.010 CrossRefGoogle Scholar
  11. Braakman HMH, Vaessen MJ, Jansen JFA et al (2013) Frontal lobe connectivity and cognitive impairment in pediatric frontal lobe epilepsy. Epilepsia 54:446–454. doi:10.1111/epi.12044 CrossRefPubMedGoogle Scholar
  12. Bruyns-Haylett M, Harris S, Boorman L et al (2013) The resting-state neurovascular coupling relationship: rapid changes in spontaneous neural activity in the somatosensory cortex are associated with haemodynamic fluctuations that resemble stimulus-evoked haemodynamics. Eur J Neurosci 38:2902–2916. doi:10.1111/ejn.12295 PubMedGoogle Scholar
  13. Cabral J, Kringelbach ML, Deco G (2014) Exploring the network dynamics underlying brain activity during rest. Prog Neurobiol 114:102–131. doi:10.1016/j.pneurobio.2013.12.005 CrossRefPubMedGoogle Scholar
  14. Carmichael DW, Thornton JS, Rodionov R, et al (2010) Feasibility of simultaneous intracranial EEG-fMRI in humans: a safety study. NeuroImage 49:379–390. doi:10.1016/j.neuroimage.2009.07.062 CrossRefPubMedGoogle Scholar
  15. Carmichael DW, Vulliemoz S, Rodionov R, et al (2012) Simultaneous intracranial EEG-fMRI in humans: protocol considerations and data quality. NeuroImage 63:301–309. doi:10.1016/j.neuroimage.2012.05.056 CrossRefPubMedGoogle Scholar
  16. Casdagli MC, Iasemidis LD, Savit RS et al (1997) Non-linearity in invasive EEG recordings from patients with temporal lobe epilepsy. Electroencephalogr Clin Neurophysiol 102:98–105CrossRefPubMedGoogle Scholar
  17. Centeno M, Carmichael DW (2014) Network connectivity in epilepsy: resting state fMRI and EEG–fMRI contributions. Epilepsy 5:93. doi:10.3389/fneur.2014.00093 Google Scholar
  18. Chauvel P (2001) Contributions of Jean Talairach and Jean Bancaud to epilepsy surgery. In: Luders H, Comair YG (eds) Epilepsy Surgery. Lippincott Williams & Wilkins, Philadelphia, pp 35–41Google Scholar
  19. Deco G, Corbetta M (2011) The dynamical balance of the brain at rest. Neurosci Rev J Bringing Neurobiol Neurol Psychiatry 17:107–123. doi:10.1177/1073858409354384 Google Scholar
  20. Deco G, Jirsa VK (2012) Ongoing cortical activity at rest: criticality, multistability, and ghost attractors. J Neurosci Off J. Soc Neurosci 32:3366–3375. doi:10.1523/JNEUROSCI.2523-11.2012 CrossRefGoogle Scholar
  21. Deligianni F, Centeno M, Carmichael DW, Clayden JD (2014) Relating resting-state fMRI and EEG whole-brain connectomes across frequency bands. Front Neurosci 8:258. doi:10.3389/fnins.2014.00258 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Douw L, Leveroni CL, Tanaka N, et al (2015) Loss of resting-state posterior cingulate flexibility is associated with memory disturbance in left temporal lobe epilepsy. PloS ONE 10:e0131209. doi:10.1371/journal.pone.0131209 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Duncan J (2009) The current status of neuroimaging for epilepsy. Curr Opin Neurol 22:179–184. doi:10.1097/WCO.0b013e328328f260 PubMedGoogle Scholar
  24. Duncan JS (2010) Imaging in the surgical treatment of epilepsy. Nat Rev Neurol 6:537–550. doi:10.1038/nrneurol.2010.131 CrossRefPubMedGoogle Scholar
  25. Duncan NW, Northoff G (2013) Overview of potential procedural and participant-related confounds for neuroimaging of the resting state. J Psychiatry Neurosci JPN 38:84–96. doi:10.1503/jpn.120059 CrossRefPubMedGoogle Scholar
  26. Duncan D, Duckrow RB, Pincus SM et al (2013) Intracranial EEG evaluation of relationship within a resting state network. Clin Neurophysiol Off J Int Fed. Clin Neurophysiol 124:1943–1951. doi:10.1016/j.clinph.2013.03.028 CrossRefGoogle Scholar
  27. Englot DJ, Hinkley LB, Kort NS et al (2015) Global and regional functional connectivity maps of neural oscillations in focal epilepsy. Brain J Neurol 138:2249–2262. doi:10.1093/brain/awv130 CrossRefGoogle Scholar
  28. Feige B, Spiegelhalder K, Kiemen A, et al (2016) Distinctive time-lagged resting-state networks revealed by simultaneous EEG-fMRI. NeuroImage doi:10.1016/j.neuroimage.2016.09.027 PubMedGoogle Scholar
  29. Garrett DD, Kovacevic N, McIntosh AR, Grady CL (2010) Blood oxygen level-dependent signal variability is more than just noise. J Neurosci Off J. Soc Neurosci 30:4914–4921. doi:10.1523/JNEUROSCI.5166-09.2010 CrossRefGoogle Scholar
  30. Garrett DD, Kovacevic N, McIntosh AR, Grady CL (2013) The modulation of BOLD variability between cognitive states varies by age and processing speed. Cereb Cortex N Y N 1991 23:684–693. doi:10.1093/cercor/bhs055 Google Scholar
  31. Gotman J, Pittau F (2011) Combining EEG and fMRI in the study of epileptic discharges. Epilepsia 52(Suppl 4):38–42. doi:10.1111/j.1528-1167.2011.03151.x CrossRefPubMedPubMedCentralGoogle Scholar
  32. Guye M, Le Fur Y, Confort-Gouny S et al (2002) Metabolic and electrophysiological alterations in subtypes of temporal lobe epilepsy: a combined proton magnetic resonance spectroscopic imaging and depth electrodes study. Epilepsia 43:1197–1209CrossRefPubMedGoogle Scholar
  33. Guye M, Ranjeva JP, Le Fur Y, et al (2005) 1 H-MRS imaging in intractable frontal lobe epilepsies characterized by depth electrode recording. NeuroImage 26:1174–1183. doi:10.1016/j.neuroimage.2005.03.023 CrossRefPubMedGoogle Scholar
  34. Guye M, Bartolomei F, Ranjeva J-P (2008) Imaging structural and functional connectivity: towards a unified definition of human brain organization? Curr Opin Neurol 21:393–403. doi:10.1097/WCO.0b013e3283065cfb CrossRefPubMedGoogle Scholar
  35. Guye M, Bettus G, Bartolomei F, Cozzone PJ (2010) Graph theoretical analysis of structural and functional connectivity MRI in normal and pathological brain networks. Magma N Y N 23:409–421. doi:10.1007/s10334-010-0205-z CrossRefGoogle Scholar
  36. Harris S, Bruyns-Haylett M, Kennerley A et al (2013) The effects of focal epileptic activity on regional sensory-evoked neurovascular coupling and postictal modulation of bilateral sensory processing. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab 33:1595–1604. doi:10.1038/jcbfm.2013.115 CrossRefGoogle Scholar
  37. He BJ, Snyder AZ, Zempel JM et al (2008) Electrophysiological correlates of the brain’s intrinsic large-scale functional architecture. Proc Natl Acad Sci USA 105:16039–16044. doi:10.1073/pnas.0807010105 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Holmes M, Folley BS, Sonmezturk HH et al (2014) Resting state functional connectivity of the hippocampus associated with neurocognitive function in left temporal lobe epilepsy. Hum Brain Mapp 35:735–744. doi:10.1002/hbm.22210 CrossRefPubMedGoogle Scholar
  39. Kaneoke Y, Donishi T, Iwatani J, et al (2012) Variance and autocorrelation of the spontaneous slow brain activity. PloS ONE 7:e38131. doi:10.1371/journal.pone.0038131 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Keilholz SD (2014) The neural basis of time-varying resting-state functional connectivity. Brain Connect 4:769–779. doi:10.1089/brain.2014.0250 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kobayashi E, Bagshaw AP, Grova C et al (2006) Negative BOLD responses to epileptic spikes. Hum Brain Mapp 27:488–497. doi:10.1002/hbm.20193 CrossRefPubMedGoogle Scholar
  42. Laufs H (2012) Functional imaging of seizures and epilepsy: evolution from zones to networks. Curr Opin Neurol 25:194–200. doi:10.1097/WCO.0b013e3283515db9 CrossRefPubMedGoogle Scholar
  43. Laufs H, Rodionov R, Thornton R, et al (2014) Altered FMRI connectivity dynamics in temporal lobe epilepsy might explain seizure semiology. Front Neurol 5:175. doi:10.3389/fneur.2014.00175 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Liao W, Zhang Z, Pan Z, et al (2010) Altered functional connectivity and small-world in mesial temporal lobe epilepsy. PloS ONE 5:e8525. doi:10.1371/journal.pone.0008525 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Lopes R, Moeller F, Besson P, et al (2014) Study on the relationships between intrinsic functional connectivity of the default mode network and transient epileptic activity. Front Neurol 5:201. doi:10.3389/fneur.2014.00201 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Lu H, Zuo Y, Gu H et al (2007) Synchronized delta oscillations correlate with the resting-state functional MRI signal. Proc Natl Acad Sci USA 104:18265–18269. doi:10.1073/pnas.0705791104 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Lu H, Wang L, Rea WW, et al (2016) Low- but not high-frequency LFP correlates with spontaneous BOLD fluctuations in rat whisker barrel cortex. Cereb Cortex N Y N 1991 26:683–694. doi:10.1093/cercor/bhu248 Google Scholar
  48. Luo Q, Glover GH (2012) Influence of dense-array EEG cap on fMRI signal. Magn Reson Med 68:807–815. doi:10.1002/mrm.23299 CrossRefPubMedGoogle Scholar
  49. Luo C, An D, Yao D, Gotman J (2014) Patient-specific connectivity pattern of epileptic network in frontal lobe epilepsy. NeuroImage Clin 4:668–675. doi:10.1016/j.nicl.2014.04.006 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Magri C, Schridde U, Murayama Y et al (2012) The amplitude and timing of the BOLD signal reflects the relationship between local field potential power at different frequencies. J Neurosci Off J. Soc Neurosci 32:1395–1407. doi:10.1523/JNEUROSCI.3985-11.2012 CrossRefGoogle Scholar
  51. Mankinen K, Long X-Y, Paakki J-J et al (2011) Alterations in regional homogeneity of baseline brain activity in pediatric temporal lobe epilepsy. Brain Res 1373:221–229. doi:10.1016/j.brainres.2010.12.004 CrossRefPubMedGoogle Scholar
  52. Nedic S, Stufflebeam SM, Rondinoni C et al (2015) Using network dynamic fMRI for detection of epileptogenic foci. BMC Neurol 15:262. doi:10.1186/s12883-015-0514-y CrossRefPubMedPubMedCentralGoogle Scholar
  53. Netoff TI, Pecora LM, Schiff SJ (2004) Analytical coupling detection in the presence of noise and nonlinearity. Phys Rev E 69:017201. doi:10.1103/PhysRevE.69.017201 CrossRefGoogle Scholar
  54. Nir Y, Mukamel R, Dinstein I et al (2008) Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat Neurosci 11:1100–1108CrossRefPubMedPubMedCentralGoogle Scholar
  55. Nissen IA, van Klink NEC, Zijlmans M et al (2016) Brain areas with epileptic high frequency oscillations are functionally isolated in MEG virtual electrode networks. Clin Neurophysiol Off J Int Fed. Clin Neurophysiol 127:2581–2591. doi:10.1016/j.clinph.2016.04.013 CrossRefGoogle Scholar
  56. Noachtar S, Rémi J (2009) The role of EEG in epilepsy: a critical review. Epilepsy Behav EB 15:22–33. doi:10.1016/j.yebeh.2009.02.035 CrossRefGoogle Scholar
  57. Oby E, Janigro D (2006) The blood–brain barrier and epilepsy. Epilepsia 47:1761–1774. doi:10.1111/j.1528-1167.2006.00817.x CrossRefPubMedGoogle Scholar
  58. Palmini A (2006) The concept of the epileptogenic zone: a modern look at Penfield and Jasper’s views on the role of interictal spikes. Epileptic Disord Int Epilepsy J Videotape 8 Suppl 2:S10–15.Google Scholar
  59. Pan W-J, Thompson G, Magnuson M, et al (2011) Broadband local field potentials correlate with spontaneous fluctuations in functional magnetic resonance imaging signals in the rat somatosensory cortex under isoflurane anesthesia. Brain Connect 1:119–131. doi:10.1089/brain.2011.0014 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Pan W-J, Thompson GJ, Magnuson ME, et al (2013) Infraslow LFP correlates to resting-state fMRI BOLD signals. NeuroImage 74:288–297. doi:10.1016/j.neuroimage.2013.02.035 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Power JD, Barnes KA, Snyder AZ, et al (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 59:2142–2154. doi:10.1016/j.neuroimage.2011.10.018 CrossRefPubMedGoogle Scholar
  62. Raichle ME (2015) The restless brain: how intrinsic activity organizes brain function. Philos Trans R Soc Lond B Biol Sci. doi:10.1098/rstb.2014.0172 PubMedPubMedCentralGoogle Scholar
  63. Ridley BGY, Rousseau C, Wirsich J, et al (2015) Nodal approach reveals differential impact of lateralized focal epilepsies on hub reorganization. NeuroImage 118:39–48. doi:10.1016/j.neuroimage.2015.05.096 CrossRefPubMedGoogle Scholar
  64. Rosenow F, Lüders H (2001) Presurgical evaluation of epilepsy. Brain J Neurol 124:1683–1700CrossRefGoogle Scholar
  65. Salek-Haddadi A, Diehl B, Hamandi K, Merschhemke M, Liston A, Friston K, Duncan JS, Fish DR, Lemieux L (2006) Hemodynamic correlates of epileptiform discharges: an EEG-fMRI study of 63 patients with focal epilepsy. Brain Res 1088(1):148–166. doi:10.1016/j.brainres.2006.02.098 Google Scholar
  66. Schevon CA, Cappell J, Emerson R, et al (2007) Cortical abnormalities in epilepsy revealed by local EEG synchrony. NeuroImage 35:140–148. doi:10.1016/j.neuroimage.2006.11.009 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Schölvinck ML, Maier A, Ye FQ et al (2010) Neural basis of global resting-state fMRI activity. Proc Natl Acad Sci USA 107:10238–10243. doi:10.1073/pnas.0913110107 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Schölvinck ML, Leopold DA, Brookes MJ, Khader PH (2013) The contribution of electrophysiology to functional connectivity mapping. NeuroImage 80:297–306. doi:10.1016/j.neuroimage.2013.04.010 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Serles W, Li LM, Antel SB et al (2001) Time course of postoperative recovery of N-acetyl-aspartate in temporal lobe epilepsy. Epilepsia 42:190–197PubMedGoogle Scholar
  70. Shmuel A, Leopold DA (2008) Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: implications for functional connectivity at rest. Hum Brain Mapp 29:751–761. doi:10.1002/hbm.20580 CrossRefPubMedGoogle Scholar
  71. Smith SM, Fox PT, Miller KL et al (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci USA 106:13040–13045. doi:10.1073/pnas.0905267106 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Spencer SS (2002) Neural networks in human epilepsy: evidence of and implications for treatment. Epilepsia 43:219–227CrossRefPubMedGoogle Scholar
  73. Sporns O (2014) Contributions and challenges for network models in cognitive neuroscience. Nat Neurosci 17:652–660. doi:10.1038/nn.3690 CrossRefPubMedGoogle Scholar
  74. Stefan H, Lopes da Silva FH (2013) Epileptic neuronal networks: methods of identification and clinical relevance. Front Neurol 4:8. doi:10.3389/fneur.2013.00008 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Stufflebeam SM, Liu H, Sepulcre J et al (2011) Localization of focal epileptic discharges using functional connectivity magnetic resonance imaging. J Neurosurg 114:1693–1697. doi:10.3171/2011.1.JNS10482 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Tagliazucchi E, Laufs H (2015) Multimodal imaging of dynamic functional connectivity. Front Neurol 6:10. doi:10.3389/fneur.2015.00010 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Thompson GJ, Merritt MD, Pan W-J, et al (2013) Neural correlates of time-varying functional connectivity in the rat. NeuroImage 83:826–836. doi:10.1016/j.neuroimage.2013.07.036 CrossRefPubMedGoogle Scholar
  78. Thornton R, Vulliemoz S, Rodionov R, Carmichael DW, Chaudhary UJ, Diehl B, Laufs H, Vollmar C, McEvoy AW, Walker MC, Bartolomei F, Guye M, Chauvel P, Duncan JS, Lemieux L (2011) Epileptic networks in focal cortical dysplasia revealed using electroencephalography-functional magnetic resonance imaging. Ann Neurol 70(5):822–837. doi:10.1002/ana.22535 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Uludağ K, Roebroeck A (2014) General overview on the merits of multimodal neuroimaging data fusion. NeuroImage 102 (1):3–10. doi:10.1016/j.neuroimage.2014.05.018 CrossRefPubMedGoogle Scholar
  80. van Diessen E, Numan T, van Dellen E et al (2015) Opportunities and methodological challenges in EEG and MEG resting state functional brain network research. Clin Neurophysiol Off J Int Fed. Clin Neurophysiol 126:1468–1481. doi:10.1016/j.clinph.2014.11.018 CrossRefGoogle Scholar
  81. van Graan LA, Lemieux L, Chaudhary UJ (2015) Methods and utility of EEG-fMRI in epilepsy. Quant Imaging Med Surg 5:300–312. doi:10.3978/j.issn.2223-4292.2015.02.04 PubMedPubMedCentralGoogle Scholar
  82. Vulliemoz S, Carmichael DW, Rosenkranz K, et al (2011) Simultaneous intracranial EEG and fMRI of interictal epileptic discharges in humans. NeuroImage 54:182–190. doi:10.1016/j.neuroimage.2010.08.004 CrossRefPubMedGoogle Scholar
  83. Warren CP, Hu S, Stead M et al (2010a) Synchrony in normal and focal epileptic brain: the seizure onset zone is functionally disconnected. J Neurophysiol 104:3530–3539. doi:10.1152/jn.00368.2010 CrossRefPubMedPubMedCentralGoogle Scholar
  84. Warren CP, Hu S, Stead M et al (2010b) Synchrony in normal and focal epileptic brain: the seizure onset zone is functionally disconnected. J Neurophysiol 104:3530–3539. doi:10.1152/jn.00368.2010 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Wendling F (2015) Software Amadeus-Visualisation. Inserm-Université de Rennes 1. FR.001.420017.000.S.P.2015.000.31230Google Scholar
  86. Wendling F, Bartolomei F, Bellanger JJ, Chauvel P (2001) Identification of epileptogenic networks from modeling and nonlinear analysis of SEEG signals. Neurophysiol Clin. Clin Neurophysiol 31:139–151CrossRefGoogle Scholar
  87. Wendling F, Chauvel P, Biraben A, Bartolomei F (2010) From intracerebral EEG signals to brain connectivity: identification of epileptogenic networks in partial epilepsy. Front Syst Neurosci 4:154. doi:10.3389/fnsys.2010.00154 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Widjaja E, Zamyadi M, Raybaud C et al (2013) Abnormal functional network connectivity among resting-state networks in children with frontal lobe epilepsy. AJNR Am J Neuroradiol 34:2386–2392. doi:10.3174/ajnr.A3608 CrossRefPubMedGoogle Scholar
  89. Xia M, Wang J, He Y (2013) BrainNet viewer: a network visualization tool for human brain connectomics. PLoS ONE. doi:10.1371/journal.pone.0068910 Google Scholar
  90. Zhang Z, Lu G, Zhong Y et al (2010) fMRI study of mesial temporal lobe epilepsy using amplitude of low-frequency fluctuation analysis. Hum Brain Mapp 31:1851–1861. doi:10.1002/hbm.20982 CrossRefPubMedGoogle Scholar
  91. Zhang Z, Xu Q, Liao W et al (2015) Pathological uncoupling between amplitude and connectivity of brain fluctuations in epilepsy. Hum Brain Mapp 36:2756–2766. doi:10.1002/hbm.22805 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Ben Ridley
    • 1
    • 2
  • Jonathan Wirsich
    • 1
    • 2
    • 3
  • Gaelle Bettus
    • 1
    • 2
    • 3
  • Roman Rodionov
    • 4
    • 5
  • Teresa Murta
    • 4
    • 6
  • Umair Chaudhary
    • 4
    • 5
  • David Carmichael
    • 7
  • Rachel Thornton
    • 4
    • 5
  • Serge Vulliemoz
    • 4
    • 5
    • 8
  • Andrew McEvoy
    • 4
    • 5
    • 9
  • Fabrice Wendling
    • 10
    • 11
  • Fabrice Bartolomei
    • 3
    • 12
  • Jean-Philippe Ranjeva
    • 1
    • 2
  • Louis Lemieux
    • 4
    • 5
  • Maxime Guye
    • 1
    • 2
  1. 1.Aix-Marseille Univ, CNRSCRMBM UMRMarseilleFrance
  2. 2.APHM, Hôpitaux de la TimoneCEMEREMMarseilleFrance
  3. 3.Aix Marseille Univ, Inserm, INS, Institut de Neurosciences des SystèmesMarseilleFrance
  4. 4.Institute of NeurologyUniversity College London (UCL)LondonUK
  5. 5.MRI UnitEpilepsy SocietyBuckinghamshireUK
  6. 6.Institute for Systems and Robotics and Department of Bioengineering, Instituto Superior TécnicoUniversidade de LisboaLisboaPortugal
  7. 7.Institute of Child HealthUCLLondonUK
  8. 8.EEG and Epilepsy Unit, Neurology ClinicUniversity Hospitals and Faculty of Medicine of GenevaGenevaSwitzerland
  9. 9.Department of NeurosurgeryNational Hospital for Neurology and NeurosurgeryLondonUK
  10. 10.INSERM, U1099RennesFrance
  11. 11.Université de Rennes 1, LTSIRennesFrance
  12. 12.Service de Neurophysiologie CliniqueAPHM, Hôpitaux de la TimoneMarseilleFrance

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