Journal of Pediatric Epilepsy 2015; 04(04): 139-155
DOI: 10.1055/s-0035-1563726
Review Article
Georg Thieme Verlag KG Stuttgart · New York

Magnetoencephalography for Clinical Pediatrics: Recent Advances in Hardware, Methods, and Clinical Applications

William Gaetz
1   Department of Radiology, The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, United States
,
Ronald S. Gordon
2   Department of Psychology, Behavioral and Cognitive Neuroscience Institute (BCNI), Simon Fraser University, Canada
,
Christos Papadelis
3   Division of Newborn Medicine, Department of Medicine, Fetal-Neonatal Neuroimaging and Developmental Science Center, Boston Children's Hospital, Harvard Medical School, Boston, Massachusetts, United States
,
Hisako Fujiwara
4   Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, United States
,
Douglas F. Rose
4   Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, United States
,
J. Christopher Edgar
1   Department of Radiology, The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, United States
,
Erin S. Schwartz
1   Department of Radiology, The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, United States
,
Timothy P. L. Roberts
1   Department of Radiology, The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, United States
› Author Affiliations
Further Information

Publication History

30 July 2014

04 December 2014

Publication Date:
23 September 2015 (online)

Abstract

Advancements in magnetoencephalography (MEG) present new opportunities for clinical pediatric centers faced with the challenge of offering a sensitive diagnostic evaluation for epilepsy in infants and young children. A noninvasive brain imaging method, which measures the magnetic fields generated by the electrical activity of the human brain, MEG provides significant advantages that make it particularly suitable for pediatric use. First, patient preparation is quick and easy and, unlike functional magnetic resonance imaging/magnetic resonance imaging, operates silently. As such, brain activity can be measured in a much more child-friendly environment. Second, although similar to electroencephalography in providing millisecond temporal resolution of neural activity, MEG offers advantages over electroencephalography in superior spatial resolution given the sensitivity of MEG to intracellular neural currents and the relative “transparency” of magnetic fields to biological tissues. Finally, when combined with magnetic resonance imaging, MEG data contribute unique information to the evaluation and localization of foci beyond that obtained with other neuroimaging technologies. As an example, the utility of MEG has been shown in determining irritative onset zones associated with epileptiform activity and for the functional mapping of nearby eloquent areas. This article reviews MEG theory along with new methods and technological advances, which result in improvements in pediatric epilepsy care. After a brief introduction to MEG technology, recent hardware developments (optimized for pediatrics), improved signal processing methods, and technological developments are reviewed. Next, two clinical case studies are presented to provide examples of MEG source localization methods applied to identify epileptogenic foci in pediatrics and compare established and recently developed analysis methods. We conclude that MEG is a unique and powerful imaging method for epilepsy treatment and patient care, increasingly a focal point in medical settings aiming to excel in the treatment of epilepsy both for diagnostics and surgical outcomes with near-future pediatric MEG system also providing optimal clinical assessments in infants and young children.

 
  • References

  • 1 Hämäläinen MS, Ilmoniemi RJ. Interpreting magnetic fields of the brain: minimum norm estimates. Med Biol Eng Comput 1994; 32 (1) 35-42
  • 2 Okada Y. Neurogenesis of evoked magnetic fields. In: Williamson RJ, Romani GL, Kaurman L, eds. Biomagnetism, An Interdisciplinary Approach. New York: Plenum Press; 1983: 399-408
  • 3 Cohen D. Magnetoencephalography: evidence of magnetic fields produced by alpha-rhythm currents. Science 1968; 161 (3843) 784-786
  • 4 Barth DS, Sutherling W, Engel Jr J, Beatty J. Neuromagnetic localization of epileptiform spike activity in the human brain. Science 1982; 218 (4575) 891-894
  • 5 Barth DS, Sutherling W, Beatty J. Fast and slow magnetic phenomena in focal epileptic seizures. Science 1984; 226 (4676) 855-857
  • 6 Grondin R, Chuang S, Otsubo H , et al. The role of magnetoencephalography in pediatric epilepsy surgery. Childs Nerv Syst 2006; 22 (8) 779-785
  • 7 Chuang SH, Otsubo H, Hwang P, Orrison Jr WW, Lewine JD. Pediatric magnetic source imaging. Neuroimaging Clin N Am 1995; 5 (2) 289-303
  • 8 Huotilainen M. Magnetoencephalography in studies of infants and children. Int Rev Neurobiol 2005; 68: 25-50
  • 9 Kim H, Chung CK, Hwang H. Magnetoencephalography in pediatric epilepsy. Korean J Pediatr 2013; 56 (10) 431-438
  • 10 Obeid M, Wyllie E, Rahi AC, Mikati MA. Approach to pediatric epilepsy surgery: state of the art, Part I: General principles and presurgical workup. Eur J Paediatr Neurol 2009; 13 (2) 102-114
  • 11 Rastogi S, Lee C, Salamon N. Neuroimaging in pediatric epilepsy: a multimodality approach. Radiographics 2008; 28 (4) 1079-1095
  • 12 Schwartz ES, Dlugos DJ, Storm PB , et al. Magnetoencephalography for pediatric epilepsy: how we do it. AJNR Am J Neuroradiol 2008; 29 (5) 832-837
  • 13 Van Poppel M, Wheless JW, Clarke DF , et al. Passive language mapping with magnetoencephalography in pediatric patients with epilepsy. J Neurosurg Pediatr 2012; 10 (2) 96-102
  • 14 Verrotti A, Pizzella V, Trotta D, Madonna L, Chiarelli F, Romani GL. Magnetoencephalography in pediatric neurology and in epileptic syndromes. Pediatr Neurol 2003; 28 (4) 253-261
  • 15 Papadelis C, Harini C, Ahtam B, Doshi C, Grant E, Okada Y. Current and emerging potential for magnetoencephalography in pediatric epilepsy. J Pediatr Epilepsy 2013; 2 (1) 73-85
  • 16 Stefan H, Hummel C, Hopfengärtner R , et al. Magnetoencephalography in extratemporal epilepsy. J Clin Neurophysiol 2000; 17 (2) 190-200
  • 17 Stefan H, Scheler G, Hummel C , et al. Magnetoencephalography (MEG) predicts focal epileptogenicity in cavernomas. J Neurol Neurosurg Psychiatry 2004; 75 (9) 1309-1313
  • 18 Gaetz W, Cheyne D, Rutka JT , et al. Presurgical localization of primary motor cortex in pediatric patients with brain lesions by the use of spatially filtered magnetoencephalography. Neurosurgery 2009; 64 (3, Suppl): ons177-ons185 , discussion ons186
  • 19 Castillo EM, Simos PG, Wheless JW , et al. Integrating sensory and motor mapping in a comprehensive MEG protocol: clinical validity and replicability. Neuroimage 2004; 21 (3) 973-983
  • 20 Papanicolaou AC, Simos PG, Breier JI , et al. Magnetoencephalographic mapping of the language-specific cortex. J Neurosurg 1999; 90 (1) 85-93
  • 21 Bowyer SM, Moran JE, Weiland BJ , et al. Language laterality determined by MEG mapping with MR-FOCUSS. Epilepsy Behav 2005; 6 (2) 235-241
  • 22 Scantlebury N, Gaetz W, Widjaja E , et al. Functional reorganization of the corticospinal tract in a pediatric patient with an arteriovenous malformation. Neuroreport 2014; 25 (1) 55-59
  • 23 Gaetz W, Scantlebury N, Widjaja E , et al. Mapping of the cortical spinal tracts using magnetoencephalography and diffusion tensor tractography in pediatric brain tumor patients. Childs Nerv Syst 2010; 26 (11) 1639-1645
  • 24 Kamada K, Todo T, Masutani Y , et al. Visualization of the frontotemporal language fibers by tractography combined with functional magnetic resonance imaging and magnetoencephalography. J Neurosurg 2007; 106 (1) 90-98
  • 25 Hunold A, Haueisen J, Ahtam B , et al. Localization of the epileptogenic foci in tuberous sclerosis complex: a pediatric case report. Front Hum Neurosci 2014; 8: 175
  • 26 Malmivuo J. Comparison of the properties of EEG and MEG in detecting the electric activity of the brain. Brain Topogr 2012; 25 (1) 1-19
  • 27 Schoffelen JM, Gross J. Source connectivity analysis with MEG and EEG. Hum Brain Mapp 2009; 30 (6) 1857-1865
  • 28 Tian X, Huber DE. Measures of spatial similarity and response magnitude in MEG and scalp EEG. Brain Topogr 2008; 20 (3) 131-141
  • 29 Ioannides AA. Magnetoencephalography as a research tool in neuroscience: state of the art. Neuroscientist 2006; 12 (6) 524-544
  • 30 Kaufman L, Lu ZL. Basics of neuromagnetism and magnetic source imaging,. In: Lu ZL, Kaufman L, eds. Magnetic Source Imaging of the Human Brain. Mahwah, NJ: Lawrence Erlbaum Associates, Inc.; 2003: 1-42
  • 31 Leahy RM, Mosher JC, Spencer ME, Huang MX, Lewine JD. A study of dipole localization accuracy for MEG and EEG using a human skull phantom. Electroencephalogr Clin Neurophysiol 1998; 107 (2) 159-173
  • 32 Cohen D, Cuffin BN. EEG versus MEG localization accuracy: theory and experiment. Brain Topogr 1991; 4 (2) 95-103
  • 33 Kwon H, Lee YH, Kim JM, Park YK, Kuriki S. Localization accuracy of single current dipoles from tangential components of auditory evoked fields. Phys Med Biol 2002; 47 (23) 4145-4154
  • 34 Hillebrand A, Barnes GR. A quantitative assessment of the sensitivity of whole-head MEG to activity in the adult human cortex. Neuroimage 2002; 16 (3, Pt 1) 638-650
  • 35 Papadelis C, Poghosyan V, Fenwick PB, Ioannides AA. MEG's ability to localise accurately weak transient neural sources. Clin Neurophysiol 2009; 120 (11) 1958-1970
  • 36 Barkley GL. Controversies in neurophysiology. MEG is superior to EEG in localization of interictal epileptiform activity: Pro. Clin Neurophysiol 2004; 115 (5) 1001-1009
  • 37 Baumgartner C. Controversies in clinical neurophysiology. MEG is superior to EEG in the localization of interictal epileptiform activity: Con. Clin Neurophysiol 2004; 115 (5) 1010-1020
  • 38 Yamamoto T, Williamson SJ, Kaufman L, Nicholson C, Llinás R. Magnetic localization of neuronal activity in the human brain. Proc Natl Acad Sci U S A 1988; 85 (22) 8732-8736
  • 39 Troebinger L, López JD, Lutti A, Bestmann S, Barnes G. Discrimination of cortical laminae using MEG. Neuroimage 2014; 102 (Pt 2) 885-893
  • 40 Papadelis C, Eickhoff SB, Zilles K, Ioannides AA. BA3b and BA1 activate in a serial fashion after median nerve stimulation: direct evidence from combining source analysis of evoked fields and cytoarchitectonic probabilistic maps. Neuroimage 2011; 54 (1) 60-73
  • 41 Timmermann L, Gross J, Dirks M, Volkmann J, Freund HJ, Schnitzler A. The cerebral oscillatory network of parkinsonian resting tremor. Brain 2003; 126 (Pt 1) 199-212
  • 42 Tenney JR, Fujiwara H, Horn PS, Jacobson SE, Glauser TA, Rose DF. Focal corticothalamic sources during generalized absence seizures: a MEG study. Epilepsy Res 2013; 106 (1–2) 113-122
  • 43 Papadelis C, Leonardelli E, Staudt M, Braun C. Can magnetoencephalography track the afferent information flow along white matter thalamo-cortical fibers?. Neuroimage 2012; 60 (2) 1092-1105
  • 44 Cornwell BR, Carver FW, Coppola R, Johnson L, Alvarez R, Grillon C. Evoked amygdala responses to negative faces revealed by adaptive MEG beamformers. Brain Res 2008; 1244: 103-112
  • 45 Styliadis C, Ioannides AA, Bamidis PD, Papadelis C. Amygdala responses to Valence and its interaction by arousal revealed by MEG. Int J Psychophysiol 2014; 93 (1) 121-133
  • 46 Riggs L, Moses SN, Bardouille T, Herdman AT, Ross B, Ryan JD. A complementary analytic approach to examining medial temporal lobe sources using magnetoencephalography. Neuroimage 2009; 45 (2) 627-642
  • 47 Martin T, Houck JM, Bish JP , et al. MEG reveals different contributions of somatomotor cortex and cerebellum to simple reaction time after temporally structured cues. Hum Brain Mapp 2006; 27 (7) 552-561
  • 48 Ioannides AA, Fenwick PB, Liu L. Widely distributed magnetoencephalography spikes related to the planning and execution of human saccades. J Neurosci 2005; 25 (35) 7950-7967
  • 49 Fuchs M, Wagner M, Wischmann HA , et al. Improving source reconstructions by combining bioelectric and biomagnetic data. Electroencephalogr Clin Neurophysiol 1998; 107 (2) 93-111
  • 50 Styliadis C, Ioannides AA, Bamidis PD, Papadelis C. Distinct cerebellar lobules process arousal, valence and their interaction in parallel following a temporal hierarchy. Neuroimage 2015; 110: 149-161
  • 51 Ebersole JS, Ebersole SM. Combining MEG and EEG source modeling in epilepsy evaluations. J Clin Neurophysiol 2010; 27 (6) 360-371
  • 52 Hari R, Salmelin R. Magnetoencephalography: from SQUIDs to neuroscience. Neuroimage 20th anniversary special edition. Neuroimage 2012; 61 (2) 386-396
  • 53 Anninos PA, Anogianakis G, Lehnertz K, Pantev C, Hoke M. Biomagnetic measurements using squids. Int J Neurosci 1987; 37 (3–4) 149-168
  • 54 Vrba J. Multichannel SQUID biomagnetic systems. In: Weinstock H, ed. NATO Applications of Superconductivity Series. The Netherlands: Springer; 2000: 61-138
  • 55 Gaetz W, Otsubo H, Pang EW. Magnetoencephalography for clinical pediatrics: the effect of head positioning on measurement of somatosensory-evoked fields. Clin Neurophysiol 2008; 119 (8) 1923-1933
  • 56 Pihko E, Nevalainen P, Stephen J, Okada Y, Lauronen L. Maturation of somatosensory cortical processing from birth to adulthood revealed by magnetoencephalography. Clin Neurophysiol 2009; 120 (8) 1552-1561
  • 57 Gaillard WD, Grandin CB, Xu B. Developmental aspects of pediatric fMRI: considerations for image acquisition, analysis, and interpretation. Neuroimage 2001; 13 (2) 239-249
  • 58 Irimia A, Erhart MJ, Brown TT. Variability of magnetoencephalographic sensor sensitivity measures as a function of age, brain volume and cortical area. Clin Neurophysiol 2014; 125 (10) 1973-1984
  • 59 Vrba J, The benefit of reduced distance in Pediatric MEG design. In: Gaetz W. ed. Philadelphia, PA; 2014
  • 60 Johnson BW, Crain S, Thornton R, Tesan G, Reid M. Measurement of brain function in pre-school children using a custom sized whole-head MEG sensor array. Clin Neurophysiol 2010; 121 (3) 340-349
  • 61 Kikuchi M, Yoshimura Y, Shitamichi K , et al. A custom magnetoencephalography device reveals brain connectivity and high reading/decoding ability in children with autism. Sci Rep 2013; 3: 1139
  • 62 Okada Y, Pratt K, Atwood C , et al. BabySQUID: a mobile, high-resolution multichannel magnetoencephalography system for neonatal brain assessment. Rev Sci Instrum 2006; 77: 24301
  • 63 Roberts TP, Paulson DN, Hirschkoff E , et al. Artemis 123: development of a whole-head infant and young child MEG system. Front Hum Neurosci 2014; 8: 99
  • 64 He W, Brock J, Johnson BW. Face-sensitive brain responses measured from a four-year-old child with a custom-sized child MEG system. J Neurosci Methods 2014; 222: 213-217
  • 65 Dammers J, Chocholacs H, Eich E , et al. Source localization of brain activity using helium-free interferometer. Appl Phys Lett 2014; 104 (21) 213705
  • 66 Pang EW. Practical aspects of running developmental studies in the MEG. Brain Topogr 2011; 24 (3–4) 253-260
  • 67 Tesan G, Johnson BW, Reid M, Thornton R, Crain S. Measurement of neuromagnetic brain function in pre-school children with custom sized MEG. J Vis Exp 2010; 36 (36) 1693
  • 68 Mima T, Sadato N, Yazawa S , et al. Brain structures related to active and passive finger movements in man. Brain 1999; 122 (Pt 10) 1989-1997
  • 69 Guzzetta A, Staudt M, Petacchi E , et al. Brain representation of active and passive hand movements in children. Pediatr Res 2007; 61 (4) 485-490
  • 70 Holliday IE, Barnes GR, Hillebrand A, Singh KD. Accuracy and applications of group MEG studies using cortical source locations estimated from participants' scalp surfaces. Hum Brain Mapp 2003; 20 (3) 142-147
  • 71 Tadel F, Baillet S, Mosher JC, Pantazis D, Leahy RM. Brainstorm: a user-friendly application for MEG/EEG analysis. Comput Intell Neurosci 2011; 2011 (11) 879716 . Doi: 10.1155/2011/879716
  • 72 Stolk A, Todorovic A, Schoffelen JM, Oostenveld R. Online and offline tools for head movement compensation in MEG. Neuroimage 2013; 68: 39-48
  • 73 Uutela K, Taulu S, Hämäläinen M. Detecting and correcting for head movements in neuromagnetic measurements. Neuroimage 2001; 14 (6) 1424-1431
  • 74 Medvedovsky M, Taulu S, Bikmullina R, Paetau R. Artifact and head movement compensation in MEG. Neurol Neurophysiol Neurosci 2007; 29: 4
  • 75 Wehner DT, Hämäläinen MS, Mody M, Ahlfors SP. Head movements of children in MEG: quantification, effects on source estimation, and compensation. Neuroimage 2008; 40 (2) 541-550
  • 76 de Munck JC, Verbunt JP, Van't Ent D, Van Dijk BW. The use of an MEG device as 3D digitizer and motion monitoring system. Phys Med Biol 2001; 46 (8) 2041-2052
  • 77 Taulu S, Kajola M, Simola J. Suppression of interference and artifacts by the Signal Space Separation Method. Brain Topogr 2004; 16 (4) 269-275
  • 78 Zhdanov A, Wilenius J, Paetau R, Ahonen A, Mäkelä JP. Quantifying the contribution of video in combined video-magnetoencephalographic ictal recordings of epilepsy patients. Epilepsy Res 2013; 105 (3) 405-409
  • 79 Medvedovsky M, Taulu S, Gaily E , et al. Sensitivity and specificity of seizure-onset zone estimation by ictal magnetoencephalography. Epilepsia 2012; 53 (9) 1649-1657
  • 80 Fujiwara H, Greiner HM, Lee KH , et al. Resection of ictal high-frequency oscillations leads to favorable surgical outcome in pediatric epilepsy. Epilepsia 2012; 53 (9) 1607-1617
  • 81 Fujiwara H, Greiner HM, Hemasilpin N , et al. Ictal MEG onset source localization compared to intracranial EEG and outcome: improved epilepsy presurgical evaluation in pediatrics. Epilepsy Res 2012; 99 (3) 214-224
  • 82 Bagić AI, Knowlton RC, Rose DF, Ebersole JS ; ACMEGS Clinical Practice Guideline (CPG) Committee. American Clinical Magnetoencephalography Society Clinical Practice Guideline 1: recording and analysis of spontaneous cerebral activity. J Clin Neurophysiol 2011; 28 (4) 348-354
  • 83 Andrade-Valenca LP, Dubeau F, Mari F, Zelmann R, Gotman J. Interictal scalp fast oscillations as a marker of the seizure onset zone. Neurology 2011; 77 (6) 524-531
  • 84 Worrell G. High-frequency oscillations recorded on scalp EEG. Epilepsy Curr 2012; 12 (2) 57-58
  • 85 He P, Wilson G, Russell C. Removal of ocular artifacts from electro-encephalogram by adaptive filtering. Med Biol Eng Comput 2004; 42 (3) 407-412
  • 86 Jung TP, Makeig S, Humphries C , et al. Removing electroencephalographic artifacts by blind source separation. Psychophysiology 2000; 37 (2) 163-178
  • 87 Castellanos NP, Makarov VA. Recovering EEG brain signals: artifact suppression with wavelet enhanced independent component analysis. J Neurosci Methods 2006; 158 (2) 300-312
  • 88 Klados M, Papadelis C, Braun C, Bamidis P. REG-ICA: A hybrid methodology combining Blind Source Separation and regression techniques for the rejection of ocular artifacts. Biomed Signal Process Control 2011; 6 (3) 291-300
  • 89 Edgar JC, Stewart J, Miller GA. Digital filters in ERP research. In: Handy TC, ed. Event-Related Potentials: A Methods Handbook. Cambridge, MA: MIT Press; 2005: 85-113
  • 90 Bardouille T, Krishnamurthy SV, Hajra SG, D'Arcy RC. Improved localization accuracy in magnetic source imaging using a 3-D laser scanner. IEEE Trans Biomed Eng 2012; 59 (12) 3491-3497
  • 91 Kim H, Kankirawatana P, Killen J , et al. Magnetic source imaging (MSI) in children with neocortical epilepsy: surgical outcome association with 3D post-resection analysis. Epilepsy Res 2013; 106 (1–2) 164-172
  • 92 Roberts TP, Poeppel D, Rowley HA. Magnetoencephalography and magnetic source imaging. Neuropsychiatry Neuropsychol Behav Neurol 1998; 11 (2) 49-64
  • 93 Romani GL, Pizzella V. Localization of brain activity with magnetoencephalography. Adv Neurol 1990; 54: 67-77
  • 94 Rowley HA, Roberts TP. Functional localization by magnetoencephalography. Neuroimaging Clin N Am 1995; 5 (4) 695-710
  • 95 Sato S, Balish M, Muratore R. Principles of magnetoencephalography. J Clin Neurophysiol 1991; 8 (2) 144-156
  • 96 Stefan H, Nakasato N, Papanicolaou AC. Magnetoencephalography. Handb Clin Neurol 2012; 107: 347-358
  • 97 Wheless JW, Castillo E, Maggio V , et al. Magnetoencephalography (MEG) and magnetic source imaging (MSI). Neurologist 2004; 10 (3) 138-153
  • 98 Gallen CC, Schwartz BJ, Bucholz RD , et al. Presurgical localization of functional cortex using magnetic source imaging. J Neurosurg 1995; 82 (6) 988-994
  • 99 Gallen CC, Sobel DF, Schwartz B, Copeland B, Waltz T, Aung M. Magnetic source imaging. Present and future. Invest Radiol 1993; 28 (Suppl. 03) S153-S157
  • 100 Lewine JD, Orrison Jr WW. Magnetic source imaging: basic principles and applications in neuroradiology. Acad Radiol 1995; 2 (5) 436-440
  • 101 Simos PG, Papanicolaou AC, Castillo EM , et al. [Insights into brain function though magnetic source imaging: A review of research and clinical applications]. Rev Neurol 2002; 34 (9) 871-876
  • 102 Funke M, Constantino T, Van Orman C, Rodin E. Magnetoencephalography and magnetic source imaging in epilepsy. Clin EEG Neurosci 2009; 40 (4) 271-280
  • 103 Knowlton RC, Elgavish R, Howell J , et al. Magnetic source imaging versus intracranial electroencephalogram in epilepsy surgery: a prospective study. Ann Neurol 2006; 59 (5) 835-842
  • 104 Knowlton RC, Razdan SN, Limdi N , et al. Effect of epilepsy magnetic source imaging on intracranial electrode placement. Ann Neurol 2009; 65 (6) 716-723
  • 105 Bagic A, Funke ME, Ebersole J ; ACMEGS Position Statement Committee. American Clinical MEG Society (ACMEGS) position statement: the value of magnetoencephalography (MEG)/magnetic source imaging (MSI) in noninvasive presurgical evaluation of patients with medically intractable localization-related epilepsy. J Clin Neurophysiol 2009; 26 (4) 290-293
  • 106 Ebersole JS. Magnetoencephalography/magnetic source imaging in the assessment of patients with epilepsy. Epilepsia 1997; 38 (Suppl. 04) S1-S5
  • 107 Ebersole JS, Squires KC, Eliashiv SD, Smith JR. Applications of magnetic source imaging in evaluation of candidates for epilepsy surgery. Neuroimaging Clin N Am 1995; 5 (2) 267-288
  • 108 Grynszpan F, Geselowitz DB. Model studies of the magnetocardiogram. Biophys J 1973; 13 (9) 911-925
  • 109 Bast T, Oezkan O, Rona S , et al. EEG and MEG source analysis of single and averaged interictal spikes reveals intrinsic epileptogenicity in focal cortical dysplasia. Epilepsia 2004; 45 (6) 621-631
  • 110 Wennberg R, Cheyne D. Reliability of MEG source imaging of anterior temporal spikes: analysis of an intracranially characterized spike focus. Clin Neurophysiol 2014; 125 (5) 903-918
  • 111 Mosher JC, Baillet S, Leahy RM. EEG source localization and imaging using multiple signal classification approaches. J Clin Neurophysiol 1999; 16 (3) 225-238
  • 112 Tanaka N, Hämäläinen MS, Ahlfors SP , et al. Propagation of epileptic spikes reconstructed from spatiotemporal magnetoencephalographic and electroencephalographic source analysis. Neuroimage 2010; 50 (1) 217-222
  • 113 Pascual-Marqui RD. Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 2002; 24 (Suppl D): 5-12
  • 114 Robinson SE, Nagarajan SS, Mantle M, Gibbons V, Kirsch H. Localization of interictal spikes using SAM(g2) and dipole fit. Neurol Clin Neurophysiol 2004; 2004 (4) 74
  • 115 Robinson SE, Vrba J. Functional neuroimaging by synthetic aperture magnetometry (SAM). In: Yoshimoto T, Kotani M, Kuriki S, Karibe H, Nakasato N, eds. Recent Advances in Biomagnetism. Tohoku, Japan: Tohoku University Press; 1999: 302-305
  • 116 Van Veen BD, van Drongelen W, Yuchtman M, Suzuki A. Localization of brain electrical activity via linearly constrained minimum variance spatial filtering. IEEE Trans Biomed Eng 1997; 44 (9) 867-880
  • 117 Kirsch HE, Robinson SE, Mantle M, Nagarajan S. Automated localization of magnetoencephalographic interictal spikes by adaptive spatial filtering. Clin Neurophysiol 2006; 117 (10) 2264-2271
  • 118 Sugiyama I, Imai K, Yamaguchi Y , et al. Localization of epileptic foci in children with intractable epilepsy secondary to multiple cortical tubers by using synthetic aperture magnetometry kurtosis. J Neurosurg Pediatr 2009; 4 (6) 515-522
  • 119 de Gooijer-van de Groep KL, Leijten FS, Ferrier CH, Huiskamp GJ. Inverse modeling in magnetic source imaging: Comparison of MUSIC, SAM(g2), and sLORETA to interictal intracranial EEG. Hum Brain Mapp 2013; 34 (9) 2032-2044
  • 120 Rose DF, Fujiwara H, Holland-Bouley K, Greiner HM, Arthur T, Mangano FT. Focal peak activities in spread of interictal-ictal discharges in epilepsy with beamformer MEG: Evidence for an epileptic network?. Front Neurol 2013; 4: 56
  • 121 Oostenveld R, Fries P, Maris E, Schoffelen JM. FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011; 2011 (11) 156869 . Article ID 156869
  • 122 Gramfort A, Luessi M, Larson E , et al. MNE software for processing MEG and EEG data. Neuroimage 2014; 86: 446-460
  • 123 Otsubo H, Snead III OC. Magnetoencephalography and magnetic source imaging in children. J Child Neurol 2001; 16 (4) 227-235
  • 124 Kim H, Lim BC, Jeong W , et al. Magnetoencephalography in pediatric lesional epilepsy surgery. J Korean Med Sci 2012; 27 (6) 668-673
  • 125 Seo JH, Holland K, Rose D , et al. Multimodality imaging in the surgical treatment of children with nonlesional epilepsy. Neurology 2011; 76 (1) 41-48
  • 126 Sudre G, Parkkonen L, Bock E, Baillet S, Wang W, Weber DJ. rtMEG: a real-time software interface for magnetoencephalography. Comput Intell Neurosci 2011; 2011 (11) . Article ID 327953
  • 127 Ora H, Takano K, Kawase T, Iwaki S, Parkkonen L, Kansaku K. Implementation of a beam forming technique in real-time magnetoencephalography. J Integr Neurosci 2013; 12 (3) 331-341
  • 128 Kominis IK, Kornack TW, Allred JC, Romalis MV. A subfemtotesla multichannel atomic magnetometer. Nature 2003; 422 (6932) 596-599
  • 129 Dang HB, Maloof AC, Romalis MV. Ultrahigh sensitivity magnetic field and magnetization measurements with an atomic magnetometer. Appl Phys Lett 2010; 97
  • 130 Johnson CN, Schwindt PD, Weisend M. Multi-sensor magnetoencephalography with atomic magnetometers. Phys Med Biol 2013; 58 (17) 6065-6077