Advertisement

Presurgical MEG to Forecast Pediatric Cortical Epilepsies

  • Douglas F. RoseEmail author
  • Hisako Fujiwara
Reference work entry

Abstract

Although multiple modalities (semiology, EEG, MEG, PET, SPECT, fMRI) are useful for presurgical evaluation of patients with medication-resistant epilepsy, only EEG and MEG have the millisecond time resolution to track the onset and spread of interictal discharges and ictal events. For good surgical outcome, both seizure onset zones (SOZ) and regions of immediate spread, the epileptogenic zone (EZ), need to be resected. Although for adults the main preoperative question may be whether seizures arise in left or right mesial temporal lobe, the locations of SOZ can be much more variable in children and adolescents. Recent studies indicate the most common cause of medically intractable epilepsy in pediatrics is cortical dysplasias functioning as epileptogenic regions. A child may have a single circumscribed cortical dysplastic region, multiple regions throughout a lobe, cerebral hemisphere, or even bihemispheric dysplastic regions. Sometimes seizures will start at just one focal cortical dysplastic region and spread throughout the brain. For other patients, multiple cortical dysplastic regions may independently generate seizures, more in the context of a seizure network than a single seizure focus. The difficult task is to anticipate the pattern of locations of cortical dysplasias and functional epileptogenic regions for each pediatric patient. Addressing this task adequately presurgically for each patient allows intracranial electrodes to be placed correctly to verify the locations where seizures start and to observe how the seizures spread in a single patient during different clinical seizure patterns. MEG with mathematical models of the head, brain, and current source regions may be able to contribute significantly to the presurgical identification of the pediatric patient’s seizure networks and to the prediction of source locations that should be assessed with intracranial EEG recording.

Keywords

Beamformer Cortical dysplasia Epilepsy Interictal Ictal Magnetoencephalography Pediatric Seizure Surgery 

References

  1. Alarcon G, Guy CN, Binnie CD, Walker SR, Elwes RD, Polkey CE (1994) Intracerebral propagation of interictal activity in partial epilepsy: implications for source localisation. J Neurol Neurosurg Psychiatry 57(4):435–449PubMedPubMedCentralCrossRefGoogle Scholar
  2. Barth DS, Sutherling W, Engel J Jr, Beatty J (1982) Neuromagnetic localization of epileptiform spike activity in the human brain. Science 218(4575):891–894PubMedCrossRefPubMedCentralGoogle Scholar
  3. Bartolomei F, Wendling F, Chauvel P (2008) The concept of an epileptogenic network in human partial epilepsies. Neurochirurgie 54(3):174–184PubMedCrossRefPubMedCentralGoogle Scholar
  4. Becker AJ, Blumcke I, Urbach H, Hans V, Majores M (2006) Molecular neuropathology of epilepsy-associated glioneuronal malformations. J Neuropathol Exp Neurol 65(2):99–108PubMedCrossRefPubMedCentralGoogle Scholar
  5. Belardinelli P, Ortiz E, Braun C (2012) Source activity correlation effects on LCMV beamformers in a realistic measurement environment. Comput Math Methods Med 2012:190513PubMedPubMedCentralCrossRefGoogle Scholar
  6. Berg AT, Scheffer IE (2011) New concepts in classification of the epilepsies: entering the 21st century. Epilepsia 52(6):1058–1062PubMedCrossRefPubMedCentralGoogle Scholar
  7. Blumcke I, Thom M, Aronica E, Armstrong DD, Vinters HV, Palmini A, Jacques TS, Avanzini G, Barkovich AJ, Battaglia G, Becker A, Cepeda C, Cendes F, Colombo N, Crino P, Cross JH, Delalande O, Dubeau F, Duncan J, Guerrini R, Kahane P, Mathern G, Najm I, Ozkara C, Raybaud C, Represa A, Roper SN, Salamon N, Schulze-Bonhage A, Tassi L, Vezzani A, Spreafico R (2011) The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc task force of the ILAE diagnostic methods commission. Epilepsia 52(1):158–174PubMedCrossRefPubMedCentralGoogle Scholar
  8. Brookes MJ, Stevenson CM, Barnes GR, Hillebrand A, Simpson MI, Francis ST, Morris PG (2007) Beamformer reconstruction of correlated sources using a modified source model. NeuroImage 34(4):1454–1465CrossRefGoogle Scholar
  9. Campi C, Pascarella A, Sorrentino A, Piana M (2011) Highly automated dipole estimation (HADES). Comput Intell Neurosci 2011:982185PubMedPubMedCentralCrossRefGoogle Scholar
  10. Cardinale F, Cossu M, Castana L, Casaceli G, Schiariti MP, Miserocchi A, Fuschillo D, Moscato A, Caborni C, Arnulfo G, Lo Russo G (2013) Stereoelectroencephalography: surgical methodology, safety, and stereotactic application accuracy in 500 procedures. Neurosurgery 72(3):353–366. discussion 366PubMedCrossRefPubMedCentralGoogle Scholar
  11. Chowdhury RA, Lina JM, Kobayashi E, Grova C (2013) MEG source localization of spatially extended generators of epileptic activity: comparing entropic and hierarchical Bayesian approaches. PLoS One 8(2):e55969PubMedPubMedCentralCrossRefGoogle Scholar
  12. de Gooijer-van de Groep KL, Leijten FS, Ferrier CH, Huiskamp GJ (2012) Inverse modeling in magnetic source imaging: comparison of MUSIC, SAM(g2), and sLORETA to interictal intracranial EEG. Hum Brain Mapp 34(9):2032–2044Google Scholar
  13. Diwakar M, Huang MX, Srinivasan R, Harrington DL, Robb A, Angeles A, Muzzatti L, Pakdaman R, Song T, Theilmann RJ, Lee RR (2011) Dual-Core beamformer for obtaining highly correlated neuronal networks in MEG. NeuroImage 54(1):253–263PubMedCrossRefPubMedCentralGoogle Scholar
  14. Elisevich K, Shukla N, Moran JE, Smith B, Schultz L, Mason K, Barkley GL, Tepley N, Gumenyuk V, Bowyer SM (2011) An assessment of MEG coherence imaging in the study of temporal lobe epilepsy. Epilepsia 52(6):1110–1119PubMedPubMedCentralCrossRefGoogle Scholar
  15. Fujiwara H, Greiner HM, Hemasilpin N, Lee KH, Holland-Bouley K, Arthur T, Morita D, Jain SV, Mangano FT, Degrauw T, Rose DF (2012) Ictal MEG onset source localization compared to intracranial EEG and outcome: improved epilepsy presurgical evaluation in pediatrics. Epilepsy Res 99(3):214–224PubMedCrossRefPubMedCentralGoogle Scholar
  16. Gonzalez-Martinez J, Bulacio J, Alexopoulos A, Jehi L, Bingaman W, Najm I (2013) Stereoelectroencephalography in the difficult to localize refractory focal epilepsy: early experience from a north American epilepsy center. Epilepsia 54(2):323–330PubMedCrossRefPubMedCentralGoogle Scholar
  17. Grech R, Cassar T, Muscat J, Camilleri KP, Fabri SG, Zervakis M, Xanthopoulos P, Sakkalis V, Vanrumste B (2008) Review on solving the inverse problem in EEG source analysis. J Neuroengineering Rehabil 5:25CrossRefGoogle Scholar
  18. Hamalainen MS, Ilmoniemi RJ (1994) Interpreting magnetic fields of the brain: minimum norm estimates. Med Biol Eng Compu 32(1):35–42CrossRefGoogle Scholar
  19. Hara K, Lin FH, Camposano S, Foxe DM, Grant PE, Bourgeois BF, Ahlfors SP, Stufflebeam SM (2007) Magnetoencephalographic mapping of interictal spike propagation: a technical and clinical report. Am J Neuroradiol 28(8):1486–1488PubMedCrossRefPubMedCentralGoogle Scholar
  20. Harvey AS, Cross JH, Shinnar S, Mathern BW (2008) Defining the spectrum of international practice in pediatric epilepsy surgery patients. Epilepsia 49(1):146–155PubMedCrossRefPubMedCentralGoogle Scholar
  21. Hong JH, Jun SC (2012) Scanning reduction strategy in MEG/EEG beamformer source imaging. J Appl Math 2012(528469):19.  https://doi.org/10.1155/2012/528469CrossRefGoogle Scholar
  22. Huiskamp G, van Der Meij W, van Huffelen A, van Nieuwenhuizen O (2004) High resolution spatio-temporal EEG-MEG analysis of rolandic spikes. J Clin Neurophysiol Official Publ Am Electroencephalographic Soc 21(2):84–95CrossRefGoogle Scholar
  23. Imai K, Otsubo H, Sell E, Mohamed I, Ochi A, RamachandranNair R, Snead OC 3rd (2007) MEG source estimation from mesio-basal temporal areas in a child with a porencephalic cyst. Acta Neurol Scand 116(4):263–267PubMedCrossRefPubMedCentralGoogle Scholar
  24. Kabat J, Krol P (2012) Focal cortical dysplasia—review. Pol J Radiology Pol Med Soc Radiology 77(2):35–43Google Scholar
  25. Kramer MA, Eden UT, Kolaczyk ED, Zepeda R, Eskandar EN, Cash SS (2010) Coalescence and fragmentation of cortical networks during focal seizures. J Neurosci Official J Soc Neurosci 30(30):10076–10085CrossRefGoogle Scholar
  26. Lantz G, Spinelli L, Seeck M, de Peralta Menendez RG, Sottas CC, Michel CM (2003) Propagation of interictal epileptiform activity can lead to erroneous source localizations: a 128-channel EEG mapping study. J Clin Neurophysiol Official Publ Am Electroencephalographic Soc 20(5):311–319CrossRefGoogle Scholar
  27. Lopes da Silva FH (2008) The impact of EEG/MEG signal processing and modeling in the diagnostic and management of epilepsy. IEEE Rev Biomed Eng 1:143–156PubMedCrossRefGoogle Scholar
  28. Moiseev A, Herdman AT (2013) Multi-core beamformers: derivation, limitations and improvements. NeuroImage 71:135–146PubMedCrossRefGoogle Scholar
  29. Mosher JC, Leahy RM (1999) Source localization using recursively applied and projected (RAP) MUSIC. IEEE Trans Signal Process 47(2):332–340CrossRefGoogle Scholar
  30. Mosher JC, Lewis PS, Leahy RM (1992) Multiple dipole modeling and localization from spatio-temporal MEG data. IEEE Trans Biomed Eng 39(6):541–557PubMedPubMedCentralCrossRefGoogle Scholar
  31. Ossadtchi A, Baillet S, Mosher JC, Thyerlei D, Sutherling W, Leahy RM (2004) Automated interictal spike detection and source localization in magnetoencephalography using independent components analysis and spatio-temporal clustering. Clin Neurophysiol Official J Int Fed Clin Neurophysiol 115(3):508–522CrossRefGoogle Scholar
  32. Ossadtchi A, Mosher JC, Sutherling WW, Greenblatt RE, Leahy RM (2005) Hidden Markov modelling of spike propagation from interictal MEG data. Phys Med Biol 50(14):3447–3469PubMedCrossRefPubMedCentralGoogle Scholar
  33. Otsubo H, Mohamed IS, Cheyne D (2012) Source localization using event related beamformer of magnetoencephalography for interictal spikes in pediatric neocortical epilepsy. In: ICME international conference on complex medical engineering (CME), pp 288–291Google Scholar
  34. Rampp S, Kaltenhauser M, Weigel D, Buchfelder M, Ingmar Blumcke I, Dorfler A, Stefan H (2010) MEG correlates of epileptic high gamma oscillations in invasive EEG. Epilepsia 51(8):1638–1642PubMedCrossRefPubMedCentralGoogle Scholar
  35. Robinson SE, Nagarajan SS, Mantle M, Gibbons V, Kirsch H (2004) Localization of interictal spikes using SAM(g2) and dipole fit. Neurol Clin Neurophysiol 2004:74PubMedPubMedCentralGoogle Scholar
  36. Rose DF, Fujiwara H, Holland-Bouley K, Greiner HM, Arthur T, Mangano FT (2013) Focal peak activities in spread of interictal-ictal discharges in epilepsy with beamformer MEG: evidence for an epileptic network? Front Neurol 4:56PubMedPubMedCentralCrossRefGoogle Scholar
  37. Ryvlin P, Rheims S (2008) Epilepsy surgery: eligibility criteria and presurgical evaluation. Dialogues Clin Neurosci 10(1):91–103PubMedPubMedCentralGoogle Scholar
  38. Sabolek HR, Swiercz WB, Lillis KP, Cash SS, Huberfeld G, Zhao G, Ste Marie L, Clemenceau S, Barsh G, Miles R, Staley KJ (2012) A candidate mechanism underlying the variance of interictal spike propagation. J Neurosci Official J Soc Neurosci 32(9):3009–3021CrossRefGoogle Scholar
  39. Sekihara K, Nagarajan SS, Poeppel D, Marantz A, Miyashita Y (2001) Reconstructing spatio-temporal activities of neural sources using an MEG vector beamformer technique. IEEE Trans Biomed Eng 48(7):760–771PubMedPubMedCentralCrossRefGoogle Scholar
  40. Sekihara K, Nagarajan SS, Poeppel D, Marantz A, Miyashita Y (2002) Application of an MEG eigenspace beamformer to reconstructing spatio-temporal activities of neural sources. Hum Brain Mapp 15(4):199–215PubMedCrossRefPubMedCentralGoogle Scholar
  41. Shiraishi H, Ahlfors SP, Stufflebeam SM, Takano K, Okajima M, Knake S, Hatanaka K, Kohsaka S, Saitoh S, Dale AM, Halgren E (2005a) Application of magnetoencephalography in epilepsy patients with widespread spike or slow-wave activity. Epilepsia 46(8):1264–1272PubMedCrossRefPubMedCentralGoogle Scholar
  42. Shiraishi H, Stufflebeam SM, Knake S, Ahlfors SP, Sudo A, Asahina N, Egawa K, Hatanaka K, Kohsaka S, Saitoh S, Grant PE, Dale AM, Halgren E (2005b) Dynamic statistical parametric mapping for analyzing the magnetoencephalographic epileptiform activity in patients with epilepsy. J Child Neurol 20(4):363–369PubMedCrossRefPubMedCentralGoogle Scholar
  43. Shiraishi H, Ahlfors SP, Stufflebeam SM, Knake S, Larsson PG, Hamalainen MS, Takano K, Okajima M, Hatanaka K, Saitoh S, Dale AM, Halgren E (2011) Comparison of three methods for localizing interictal epileptiform discharges with magnetoencephalography. J Clin Neurophysiol Official Publ Am Electroencephalographic Soc 28(5):431–440Google Scholar
  44. Tanaka N, Cole AJ, von Pechmann D, Wakeman DG, Hamalainen MS, Liu H, Madsen JR, Bourgeois BF, Stufflebeam SM (2009) Dynamic statistical parametric mapping for analyzing ictal magnetoencephalographic spikes in patients with intractable frontal lobe epilepsy. Epilepsy Res 85(2–3):279–286PubMedPubMedCentralCrossRefGoogle Scholar
  45. Tanaka N, Hamalainen MS, Ahlfors SP, Liu H, Madsen JR, Bourgeois BF, Lee JW, Dworetzky BA, Belliveau JW, Stufflebeam SM (2010) Propagation of epileptic spikes reconstructed from spatiotemporal magnetoencephalographic and electroencephalographic source analysis. NeuroImage 50(1):217–222PubMedPubMedCentralCrossRefGoogle Scholar
  46. Tanaka N, Grant PE, Suzuki N, Madsen JR, Bergin AM, Hamalainen MS, Stufflebeam SM (2012) Multimodal imaging of spike propagation: a technical case report. AJNR Am J Neuroradiol 33(6):E82–E84PubMedPubMedCentralCrossRefGoogle Scholar
  47. Terry JR, Benjamin O, Richardson MP (2012) Seizure generation: the role of nodes and networks. Epilepsia 53(9):e166–e169CrossRefGoogle Scholar
  48. Tyvaert L, Hawco C, Kobayashi E, LeVan P, Dubeau F, Gotman J (2008) Different structures involved during ictal and interictal epileptic activity in malformations of cortical development: an EEG-fMRI study. Brain J Neurol 131.(Pt 8:2042–2060CrossRefGoogle Scholar
  49. Ukai S, Kawaguchi S, Ishii R, Yamamoto M, Ogawa A, Mizuno-Matsumoto Y, Robinson SE, Fujita N, Yoshimine T, Shinosaki K, Takeda M (2004) SAM(g2) analysis for detecting spike localization: a comparison with clinical symptoms and ECD analysis in an epileptic patient. Neurol Clin Neurophysiol 2004:57PubMedPubMedCentralGoogle Scholar
  50. Van Essen DC (2005) A population-average, landmark- and surface-based (PALS) atlas of human cerebral cortex. NeuroImage 28(3):635–662PubMedCrossRefGoogle Scholar
  51. Varotto G, Tassi L, Franceschetti S, Spreafico R, Panzica F (2012) Epileptogenic networks of type II focal cortical dysplasia: a stereo-EEG study. NeuroImage 61(3):591–598CrossRefGoogle Scholar
  52. Wang ZI, Jin K, Kakisaka Y, Mosher JC, Bingaman WE, Kotagal P, Burgess RC, Najm IM, Alexopoulos AV (2012) Imag(in)ing seizure propagation: MEG-guided interpretation of epileptic activity from a deep source. Hum Brain Mapp 33(12):2797–2801PubMedCrossRefPubMedCentralGoogle Scholar
  53. Wyler AR, Ojemann GA, Lettich E, Ward AA Jr (1984) Subdural strip electrodes for localizing epileptogenic foci. J Neurosurg 60(6):1195–1200PubMedPubMedCentralCrossRefGoogle Scholar
  54. Xiang J, Liu Y, Wang Y, Kirtman EG, Kotecha R, Chen Y, Huo X, Fujiwara H, Hemasilpin N, Lee K, Mangano FT, Leach J, Jones B, DeGrauw T, Rose D (2009) Frequency and spatial characteristics of high-frequency neuromagnetic signals in childhood epilepsy. Epileptic Disord Int Epilepsy J Videotape 11(2):113–125Google Scholar
  55. Xiang J, Wang Y, Chen Y, Liu Y, Kotecha R, Huo X, Rose DF, Fujiwara H, Hemasilpin N, Lee K, Mangano FT, Jones B, DeGrauw T (2010) Noninvasive localization of epileptogenic zones with ictal high-frequency neuromagnetic signals. J Neurosurg Pediatr 5(1):113–122PubMedCrossRefPubMedCentralGoogle Scholar
  56. Yagyu K, Takeuchi F, Shiraishi H, Nakane S, Sueda K, Asahina N, Kohsaka S, Umeoka S, Usui N, Baba K, Saitoh S (2010) The applications of time-frequency analyses to ictal magnetoencephalography in neocortical epilepsy. Epilepsy Res 90(3):199–206PubMedCrossRefPubMedCentralGoogle Scholar
  57. Yoshinaga H, Ohtsuka Y, Watanabe Y, Inutsuka M, Kitamura Y, Kinugasa K, Oka E (2004) Ictal MEG in two children with partial seizures. Brain and Development 26(6):403–408PubMedCrossRefPubMedCentralGoogle Scholar
  58. Zhang R, Wu T, Wang Y, Liu H, Zou Y, Liu W, Xiang J, Xiao C, Yang L, Fu Z (2011) Interictal magnetoencephalographic findings related with surgical outcomes in lesional and nonlesional neocortical epilepsy. Seizure 20(9):692–700PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Division of Neurology, MEG Center, Cincinnati Children’s Hospital Medical CenterUniversity of CincinnatiCincinnatiUSA

Section editors and affiliations

  • Nobukazu Nakasato
    • 1
  1. 1.Department of EpileptologyTohoku University Graduate School of MedicineSendaiJapan

Personalised recommendations