Combined EEG and MEG analysis of early somatosensory evoked activity in children and adolescents with focal epilepsies

OBJECTIVE The study aimed to evaluate differences between EEG and MEG analysis of early somatosensory evoked activity in patients with focal epilepsies in localizing eloquent areas of the somatosensory cortex. METHODS Twenty-five patients (12 male, 13 female; age 4-25 years, mean 11.7 years) were included. Syndromes were classified as symptomatic in 17, idiopathic in 2 and cryptogenic in 6 cases. 10 patients presented with malformations of cortical development (MCD). 122 channel MEG and simultaneous 33-channel EEG were recorded during tactile stimulation of the thumb (sampling rate 769 Hz, band-pass 0.3-260 Hz). Forty-four hemispheres were analyzed. Hemispheres were classified as type I: normal (15), II: central structural lesion (16), III: no lesion, but central epileptic discharges (ED, 8), IV: lesion or ED outside the central region (5). Analysis of both sides including one normal and one type II or III hemisphere was possible in 15 patients. Recordings were repeated in 18 hemispheres overall. Averaged data segments were filtered (10-250 Hz) and analyzed off-line with BESA. Latencies and amplitudes of N20 and P30 were analyzed. A regional source was fitted for localizing S1 by MRI co-registration. Orientation of EEG N20 was calculated from a single dipole model. RESULTS EEG and MEG lead to comparable good results in all normal hemispheres. Only EEG detected N20/P30 in 3 hemispheres of types II/III while MEG showed no signal. N20 dipoles had a more radial orientation in these cases. MEG added information in one hemisphere, when EEG source analysis of a clear N20 was not possible because of a low signal-to-noise ratio. Overall N20 dipoles had a more radial orientation in type II when compared to type I hemispheres (p=0.01). Further N20/P30 parameters (amplitudes, latencies, localization related to central sulcus) showed no significant differences between affected and normal hemispheres. Early somatosensory evoked activity was preserved within the visible lesion in 5 of the 10 patients with MCD. CONCLUSIONS MEG should be combined with EEG when analyzing tactile evoked activities in hemispheres with a central structural lesion or ED focus. SIGNIFICANCE At time, MEG analysis is frequently applied without simultaneous EEG. Our results clearly show that EEG may be superior under specific circumstances and combination is necessary when analyzing activity from anatomically altered cortex.

[1]  R. Hari,et al.  Functional Organization of the Human First and Second Somatosensory Cortices: a Neuromagnetic Study , 1993, The European journal of neuroscience.

[2]  L. T. Ho,et al.  MEG localization of rolandic spikes with respect to SI and SII cortices in benign rolandic epilepsy , 2003, NeuroImage.

[3]  A. Papanicolaou,et al.  Brain Plasticity for Sensory and Linguistic Functions: A Functional Imaging Study Using Magnetoencephalography With Children and Young Adults , 2001, Journal of child neurology.

[4]  K Sekihara,et al.  Dynamic activation of distinct cytoarchitectonic areas of the human SI cortex after median nerve stimulation , 2001, Neuroreport.

[5]  T. Yoshimoto,et al.  Abnormal primary somatosensory function in unilateral polymicrogyria: an MEG study , 2005, Brain and Development.

[6]  C Tomberg,et al.  Mapping somatosensory evoked potentials to finger stimulation at intervals of 450 to 4000 msec and the issue of habituation when assessing early cognitive components. , 1989, Electroencephalography and clinical neurophysiology.

[7]  Christoph Stippich,et al.  Interaction of Tactile Input in the Human Primary and Secondary Somatosensory Cortex—A Magnetoencephalographic Study , 2001, NeuroImage.

[8]  Rolf-Detlef Treede,et al.  Spatial resolution of fMRI in the human parasylvian cortex: Comparison of somatosensory and auditory activation , 2005, NeuroImage.

[9]  Christoph Stippich,et al.  Source analysis of interictal spikes in polymicrogyria: Loss of relevant cortical fissures requires simultaneous EEG to avoid MEG misinterpretation , 2005, NeuroImage.

[10]  F E Bloom,et al.  Intrasubject reliability and validity of somatosensory source localization using a large array biomagnetometer. , 1994, Electroencephalography and clinical neurophysiology.

[11]  H Hämäläinen,et al.  Human somatosensory evoked potentials to mechanical pulses and vibration: contributions of SI and SII somatosensory cortices to P50 and P100 components. , 1990, Electroencephalography and clinical neurophysiology.

[12]  S. Peng,et al.  Agyria-pachygyria: clinical, neuroimaging, and neurophysiologic correlations. , 2002, Pediatric neurology.

[13]  M. E. Spencer,et al.  A Study of Dipole Localization Accuracy for MEG and EEG using a Human Skull Phantom , 1998, NeuroImage.

[14]  M. Scherg,et al.  MEG Versus EEG: Influence of Background Activity on Interictal Spike Detection , 2006, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[15]  C Miniussi,et al.  Influence of somatosensory input on paroxysmal activity in benign rolandic epilepsy with 'extreme somatosensory evoked potentials'. , 1998, Brain : a journal of neurology.

[16]  Shozo Tobimatsu,et al.  Reorganization of the primary somatosensory area in epilepsy associated with focal cortical dysplasia. , 2001 .

[17]  A. Maravita,et al.  Spike topography and functional magnetic resonance imaging (fMRI) in benign rolandic epilepsy with spikes evoked by tapping stimulation. , 1998, Electroencephalography and clinical neurophysiology.

[18]  M Scherg,et al.  Somatotopy of human hand somatosensory cortex revealed by dipole source analysis of early somatosensory evoked potentials and 3D-NMR tomography. , 1995, Electroencephalography and clinical neurophysiology.

[19]  J E Desmedt,et al.  Bit-mapped color imaging of human evoked potentials with reference to the N20, P22, P27 and N30 somatosensory responses. , 1987, Electroencephalography and clinical neurophysiology.

[20]  E Ducla-Soares,et al.  Comparison of electroencephalography and magnetoencephalography. , 1990, Advances in neurology.

[21]  A. Papanicolaou,et al.  A magnetoencephalography study of cortical plasticity , 1999 .

[22]  Joshua I. Breier,et al.  Magnetoencephalography (MEG) and Magnetic Source Imaging (MSI) , 2004, The neurologist.

[23]  T. Morioka,et al.  Comparison of magnetoencephalography, functional MRI, and motor evoked potentials in the localization of the sensory-motor cortex. , 1995, Neurological research.

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

[25]  H. Alkadhi,et al.  Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. , 1997, Brain : a journal of neurology.

[26]  M. Taylor,et al.  Subcortical somatosensory evoked potentials after median nerve stimulation in children. , 1998, European journal of paediatric neurology : EJPN : official journal of the European Paediatric Neurology Society.

[27]  H. Freund,et al.  Cerebral Cortical Localization: Application and Validation of the Proportional Grid System in MR Imaging , 1989, Journal of computer assisted tomography.

[28]  Xavier Tricoche,et al.  Influence of tissue conductivity anisotropy on EEG/MEG field and return current computation in a realistic head model: A simulation and visualization study using high-resolution finite element modeling , 2006, NeuroImage.

[29]  P H Crandall,et al.  The magnetic and electric fields agree with intracranial localizations of somatosensory cortex , 1988, Neurology.

[30]  S. Tobimatsu,et al.  Functional mapping of the sensorimotor cortex: combined use of magnetoencephalography, functional MRI, and motor evoked potentials , 1995, Neuroradiology.

[31]  M Scherg,et al.  Preoperative localization of the central sulcus by dipole source analysis of early somatosensory evoked potentials and three-dimensional magnetic resonance imaging. , 1994, Journal of neurosurgery.

[32]  Rainer Boor,et al.  Maturation of near-field and far-field somatosensory evoked potentials after median nerve stimulation in children under 4 years of age , 2000, Clinical Neurophysiology.

[33]  R. Kuzniecky,et al.  Cortical reorganization in malformations of cortical development , 2004, Neurology.

[34]  L. Cohen,et al.  Cortical excitability during prolonged antiepileptic drug treatment and drug withdrawal , 2005, Clinical Neurophysiology.

[35]  R Steinmeier,et al.  Functional neuronavigation with magnetoencephalography: outcome in 50 patients with lesions around the motor cortex. , 1999, Neurosurgical focus.

[36]  R. Johansson,et al.  Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. , 1979, The Journal of physiology.

[37]  David F. Sobel,et al.  Noninvasive presurgical neuromagnetic mapping of somatosensory cortex. , 1993, Neurosurgery.

[38]  C C Wood,et al.  Human cortical potentials evoked by stimulation of the median nerve. II. Cytoarchitectonic areas generating long-latency activity. , 1989, Journal of neurophysiology.

[39]  M. Scherg,et al.  Noninvasive Source Localization of Interictal EEG Spikes: Effects of Signal-to-Noise Ratio and Averaging , 2006, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[40]  Walter Magerl,et al.  Asymmetry in the human primary somatosensory cortex and handedness , 2003, NeuroImage.

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

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

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

[44]  K Scheffler,et al.  Motor, somatosensory and auditory cortex localization by fMRI and MEG , 1998, Neuroreport.

[45]  Ingeborg Krägeloh-Mann,et al.  Coherent corticomuscular oscillations originate from primary motor cortex: Evidence from patients with early brain lesions , 2006, Human brain mapping.

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

[47]  D. Barth,et al.  MEG and ECoG localization accuracy test. , 1995, Electroencephalography and clinical neurophysiology.

[48]  H. Doose,et al.  Benign partial epilepsy and related conditions: Multifactorial pathogenesis with hereditary impairment of brain maturation , 1989, European Journal of Pediatrics.

[49]  J. Sarvas Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. , 1987, Physics in medicine and biology.

[50]  P Berg,et al.  Magnetic source imaging of tactile input shows task‐independent attention effects in SII , 2000, Neuroreport.

[51]  C C Wood,et al.  Electrical sources in human somatosensory cortex: identification by combined magnetic and potential recordings. , 1985, Science.

[52]  H. Lüders,et al.  Detection of Epileptiform Activity by Human Interpreters: Blinded Comparison between Electroencephalography and Magnetoencephalography , 2005, Epilepsia.

[53]  R. Ilmoniemi,et al.  EEG minimum-norm estimation compared with MEG dipole fitting in the localization of somatosensory sources at S1 , 2004, Clinical Neurophysiology.