Source analysis of interictal spikes in polymicrogyria: Loss of relevant cortical fissures requires simultaneous EEG to avoid MEG misinterpretation

PURPOSE Multiple source analysis of interictal EEG and MEG spikes was used to identify irritative zones in polymicrogyria (PMG). Spike onset times and source localization were compared between both modalities. PMG is characterized by a marked loss of deep cortical fissures. Hence, differences between EEG and MEG were expected since MEG signals are predominantly generated from tangentially orientated neurons in fissures. PATIENTS We studied 7 children and young adults (age 7.5 to 19 years) with localization-related epilepsy and unilateral polymicrogyria (PMG) as defined from anatomical MRI. METHODS 122-channel whole-head MEG and 32-channel EEG were recorded simultaneously for 25 to 40 min. Using the BESA program, interictal spikes were identified visually and used as templates to search for similar spatio-temporal spike patterns throughout the recording. Detected similar spikes (r > 0.85) were averaged, high-pass filtered (5 Hz) to enhance spike onset, and subjected to multiple spatio-temporal source analysis. Source localization was visualized by superposition on T1-weighted MRI and compared to the lesion. RESULTS Nine spike types were identified in seven patients (2 types in 2 patients). Eight out of nine EEG sources and seven MEG sources modeling spike onset were localized within the visible lesion. EEG spike onset preceded MEG significantly in two spike types by 19 and 25 ms. This was related to radial onset activity in EEG while MEG localized propagated activity. In one case, the earliest MEG spike activity was localized to the normal hemisphere while the preceding radial EEG onset activity was localized within the lesion. Distances between EEG and MEG onset sources varied markedly between 9 and 51 mm in the eight spike types with concordant lateralization. CONCLUSION Interictal irritative zones were localized within the lesion in PMG comparable to other malformations, e.g., FCD. Discrepancies in MEG and EEG were related to the lack of deep fissures in PMG. In two cases, MEG was blind to the onset of radial interictal spike activity and localized propagated spike activity. In two other cases, MEG localized to the more peripheral parts of the irritative zone. Simultaneous EEG recordings with MEG and multiple source analysis are required to avoid problems of MEG interpretation.

[1]  Hideaki Ishibashi,et al.  Localization of ictal and interictal bursting epileptogenic activity in focal cortical dysplasia: Agreement of magnetoencephalography and electrocorticography , 2002, Neurological research.

[2]  T. Morioka,et al.  Intrinsic epileptogenicity of focal cortical dysplasia as revealed by magnetoencephalography and electrocorticography , 1999, Epilepsy Research.

[3]  Tomoyuki Nakahori,et al.  Benefit of Simultaneous Recording of EEG and MEG in Dipole Localization , 2002, Epilepsia.

[4]  P Berg,et al.  New concepts of brain source imaging and localization. , 1996, Electroencephalography and clinical neurophysiology. Supplement.

[5]  E Wyllie,et al.  Surgical treatment of epilepsy in children. , 1998, Pediatric neurology.

[6]  Friedrich G Woermann,et al.  Functional organization of the brain with malformations of cortical development , 2003, Annals of neurology.

[7]  H. Stefan,et al.  Ictal onset localization of epileptic seizures by magnetoencephalography , 2002, Acta neurologica Scandinavica.

[8]  M. Avoli,et al.  Seizure‐like discharges recorded in human dysplastic neocortex maintained in vitro , 1995, Neurology.

[9]  R. Guerrini Dysplasias of cerebral cortex and epilepsy , 1996 .

[10]  Patrick Berg,et al.  Advanced Tools for Digital EEG Review:: Virtual Source Montages, Whole-head Mapping, Correlation, and Phase Analysis , 2002, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[11]  F Andermann,et al.  Human Epileptogenesis and Hypothalamic Hamartomas: New Lessons from an Experiment of Nature , 1997, Epilepsia.

[12]  J. Engel,et al.  Ictal magnetic source imaging as a localizing tool in partial epilepsy , 2002, Neurology.

[13]  Rainer Goebel,et al.  An Efficient Algorithm for Topologically Correct Segmentation of the Cortical Sheet in Anatomical MR Volumes , 2001, NeuroImage.

[14]  M. Brodie,et al.  Epilepsy Guidelines in the Real World: The Sound of Music? , 2004, Epilepsia.

[15]  P. Berg,et al.  Brain source montages improve the non-invasive diagnosis in epilepsy , 2004 .

[16]  J S Ebersole,et al.  Magnetoencephalography/Magnetic Source Imaging in the Assessment of Patients with Epilepsy , 1997, Epilepsia.

[17]  G. Hagemann,et al.  Intact functional inhibition in the surround of experimentally induced focal cortical dysplasias in rats. , 2000, Journal of neurophysiology.

[18]  G. Klem,et al.  Epileptogenicity of Focal Malformations Due to Abnormal Cortical Development: Direct Electrocorticographic–Histopathologic Correlations , 2003, Epilepsia.

[19]  N Nakasato,et al.  Comparisons of MEG, EEG, and ECoG source localization in neocortical partial epilepsy in humans. , 1994, Electroencephalography and clinical neurophysiology.

[20]  A. James Barkovich,et al.  Malformations of cortical development and epilepsy , 2001, Brain and Development.

[21]  S. Sisodiya Surgery for malformations of cortical development causing epilepsy. , 2000, Brain : a journal of neurology.

[22]  P Berg,et al.  Multiple source analysis of interictal spikes: goals, requirements, and clinical value. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[23]  H. Otsubo,et al.  MEG Predicts Epileptic Zone in Lesional Extrahippocampal Epilepsy: 12 Pediatric Surgery Cases , 2001, Epilepsia.

[24]  K M Jacobs,et al.  Focal epileptogenesis in a rat model of polymicrogyria. , 1999, Journal of neurophysiology.

[25]  H. Lüders,et al.  Focal cortical dysplasia and intractable epilepsy in adults: clinical, EEG, imaging, and surgical features , 2003, Epilepsy Research.

[26]  H. Matsuda,et al.  Cerebral cortical dysplasia: assessment by MRI and SPECT. , 2000, Pediatric neurology.

[27]  M Kajola,et al.  Magnetoencephalographic Evaluation of Children and Adolescents with Intractable Epilepsy , 1994, Epilepsia.

[28]  F Mauguière,et al.  Apparent asynchrony between interictal electric and magnetic spikes , 1997, Neuroreport.

[29]  M. Scherg,et al.  EEG and MEG Source Analysis of Single and Averaged Interictal Spikes Reveals Intrinsic Epileptogenicity in Focal Cortical Dysplasia , 2004, Epilepsia.

[30]  Tomoyuki Nakahori,et al.  Multimodal estimation of epileptic foci with dipole localization method and other technique , 2005, Brain Topography.

[31]  Jerry J Shih,et al.  Multidipole Analysis of Simulated Epileptic Spikes With Real Background Activity , 2003, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[32]  H. Otsubo,et al.  Magnetoencephalographic localization in pediatric epilepsy surgery: Comparison with invasive intracranial electroencephalography , 1999, Annals of neurology.

[33]  P R Swank,et al.  Does magnetoencephalography add to scalp video-EEG as a diagnostic tool in epilepsy surgery? , 2004, Neurology.

[34]  O Salonen,et al.  Electromagnetic function of polymicrogyric cortex in congenital bilateral perisylvian syndrome , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[35]  F Andermann,et al.  Cortical dysplasias and epilepsy: a review of the architectonic, clinical, and seizure patterns. , 2000, Advances in neurology.

[36]  Frederick Andermann,et al.  Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results , 1995, Annals of neurology.

[37]  Lino Nobili,et al.  Intra-lesional stereo-EEG activity in Taylor 's focal cortical dysplasia. , 2003, Epileptic disorders : international epilepsy journal with videotape.

[38]  Y. Inoue,et al.  Electroclinical and Magnetoencephalographic Analysis of Epilepsy in Patients With Congenital Bilateral Perisylvian Syndrome , 2000, Epilepsia.