- Email: [email protected]
On the opposition of EEG and MEG
Clinical Neurophysiology 118 (2007) 1658–1659 www.elsevier.com/locate/clinph
Editorial
On the opposition of EEG and MEG See Article, pages 1721–1735
EEG and MEG are complementary – a conclusion frequently encountered in the closing remarks of literature comparing the two electromagnetic modalities. The statement is undoubtedly correct, although there is quite frequently an intentionally calming connotation to it, to mend damage which might have been caused by findings of the respective study. The question whether either EEG or MEG is superior over the other has the potential to turn complementarity to opposition. There are numerous arguments for either modality: scalp EEG is cheaper, easily available, mobile, less of an obstacle for seizure recordings and does not need a magnetically shielded room. MEG on the other hand is contactless and practically insensitive to tissue conductivity differences, resulting in simpler calculations, which might in turn increase localization accuracy of spontaneous or evoked activity. Numerous studies have demonstrated that magnetic and electric fields provide different views on the same generators, although MEG is looking at their intracellular and EEG at their extracellular components. Park et al. (2004) show that scalp EEG might overlook spikes due to background noise, which is also seen by Ramantani et al. (2006). In contrast, Bast et al. (2005) demonstrate insensitivity of MEG for onset of interictal activity in some cases of polymicrogyria. Knake et al. (2006) compared high resolution EEG and multichannel MEG sensitivity for epileptic spikes and found spikes in both modalities in 55.7%, MEG only 12.9% and EEG 2.9%. Iwasaki et al. (2005) found only a small percentage (median 25.7%) of spikes visible simultaneously in both modalities, while the larger amount was detectable only in either EEG or MEG. Differences between these studies can probably be explained by the lower electrode number compared to Knake et al. Nevertheless, both studies show that there is information available only by using both modalities. The difference in perspective is not limited to the localization of epileptic activity. It also includes clinical questions regarding functional areas. Various studies demonstrate that MEG is a suitable answer (Druschky
et al., 2000; Ganslandt et al., 1999; Ishitobi et al., 2005; Korvenoja et al., 2006; Schiffbauer et al., 2003), because of favourable characteristics like the insensitivity to conductivity differences. However, the value of EEG in this field seems underestimated. There is only sparse literature on EEG use in presurgical functional mapping, mostly in conjunction with MEG recordings (Komssi et al., 2004), although there are various studies investigating the method with healthy individuals (Michel et al., 2004; Schaefer et al., 2002). The reason for this deficit of the otherwise frequent use of EEG technology remains unclear. Bast et al. (2007) contribute to fill this gap. They compare EEG with MEG localizations of activity evoked by tactile stimulation under clinical circumstances. It is the latter that sets the work apart, as the environment of patient care is constrained by severe and specific logistical issues. Any clinical method has to be reliable and provide valuable information, especially under suboptimal conditions. They demonstrate that in several cases predominantly with cortical malformations or epileptic discharge foci, EEG and MEG can yield overlapping results in localizing the somatosensory cortex. In these, the combination of both modalities offers a considerable benefit. Neuronal populations are the generators of magnetic and electric fields. Both modalities have their own perspective on these, overlapping in information content but which are neither identical nor completely orthogonal. Investigation of synchronously recorded EEG and MEG separately yields improved diagnostic information, for which a study of Ramachandran et al. (RamachandranNair et al., 2007) provides an example. They found that seizure freedom after epilepsy surgery in children with normal or subtle and nonfocal MRI findings was most likely to occur when there was concordance between EEG and MEG localization and least likely to occur when these results were divergent. Bast et al. (2007) also show that in some cases either modality can add information when the other is not able to do so, e.g. because of an unfavourable signal-to-noise ratio. Reintegration of both complementary, in some ways opposing modalities, however, is another step further.
1388-2457/$32.00 Ó 2007 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2007.04.021
Editorial / Clinical Neurophysiology 118 (2007) 1658–1659
There are promising works combining EEG and MEG information for optimized source localization (Babiloni et al., 2001, 2004; Fuchs et al., 1998). This utilizes sensitivities of both methods and enables superior spatial localization accuracy which is not only due to the increased number of sensors. A large body of publications describes the use of both EEG and MEG, although – and naturally – not free of subjective weighting. There is no doubt that either modality has advantages and disadvantages. However to improve methodology, the amalgamation of electric and magnetic methods into integrated electromagnetic analysis promises a considerable benefit, leading to further amplification of electrophysiology in combination with imaging methods. Sophisticated and intensive training for recording and analysis is necessary to fully develop the inherent potential because use of EEG and MEG combined with imaging needs special and complex instrumentation. In the next step of further development, national and regional research and clinical neurophysiology MEG–EEG centers should be established. References Babiloni F, Carducci F, Cincotti F, Del Gratta C, Pizzella V, Romani GL, Rossini PM, Tecchio F, Babiloni C. Linear inverse source estimate of combined EEG and MEG data related to voluntary movements. Hum Brain Mapp 2001;14(4):197–209. Babiloni F, Mattia D, Babiloni C, Astolfi L, Salinari S, Basilisco A, Rossini PM, Marciani MG, Cincotti F. Multimodal integration of EEG, MEG and fMRI data for the solution of the neuroimage puzzle. Magn Reson Imaging 2004;22(10):1471–6. Bast T, Ramantani G, Boppel T, Metzke T, Ozkan O, Stippich C, Seitz A, Rupp A, Rating D, Scherg M. Source analysis of interictal spikes in polymicrogyria: loss of relevant cortical fissures requires simultaneous EEG to avoid MEG misinterpretation. Neuroimage 2005;25(4):1232–41. Bast T, Wright T, Boor R, Harting I, Feneberg R, Rupp A, Hoechstetter K, Rating D, Baumga¨rtner U. Combined EEG and MEG analysis of early somatosensory evoked activity in children and adolescents with focal epilepsies. Clin Neurophysiol 2007;118:1721–35. Druschky K, Lang E, Hummel C, Kaltenhauser M, Kohlloffel LU, Neundorfer B, Stefan H. Pain-related somatosensory evoked magnetic fields induced by controlled ballistic mechanical impacts. J Clin Neurophysiol 2000;17(6):613–22. Fuchs M, Wagner M, Wischmann HA, Kohler T, Theissen A, Drenckhahn R, Buchner H. Improving source reconstructions by combining bioelectric and biomagnetic data. Electroencephalogr Clin Neurophysiol 1998;107(2):93–111. Ganslandt O, Fahlbusch R, Nimsky C, Kober H, Moller M, Steinmeier R, Romstock J, Vieth J. Functional neuronavigation with magnetoen-
1659
cephalography: outcome in 50 patients with lesions around the motor cortex. J Neurosurg 1999;91(1):73–9. Ishitobi M, Nakasato N, Yoshimoto T, Iinuma K. Abnormal primary somatosensory function in unilateral polymicrogyria: an MEG study. Brain Dev 2005;27(1):22–9. Iwasaki M, Pestana E, Burgess RC, Luders HO, Shamoto H, Nakasato N. Detection of epileptiform activity by human interpreters: blinded comparison between electroencephalography and magnetoencephalography. Epilepsia 2005;46(1):59–68. Knake S, Halgren E, Shiraishi H, Hara K, Hamer HM, Grant PE, Carr VA, Foxe D, Camposano S, Busa E, Witzel T, Hamalainen MS, Ahlfors SP, Bromfield EB, Black PM, Bourgeois BF, Cole AJ, Cosgrove GR, Dworetzky BA, Madsen JR, Larsson PG, Schomer DL, Thiele EA, Dale AM, Rosen BR, Stufflebeam SM. The value of multichannel MEG and EEG in the presurgical evaluation of 70 epilepsy patients. Epilepsy Res 2006;69(1):80–6. Komssi S, Huttunen J, Aronen HJ, Ilmoniemi RJ. EEG minimumnorm estimation compared with MEG dipole fitting in the localization of somatosensory sources at S1. Clin Neurophysiol 2004;115(3):534–42. Korvenoja A, Kirveskari E, Aronen HJ, Avikainen S, Brander A, Huttunen J, Ilmoniemi RJ, Jaaskelainen JE, Kovala T, Makela JP, Salli E, Seppa M. Sensorimotor cortex localization: comparison of magnetoencephalography, functional MR imaging, and intraoperative cortical mapping. Radiology 2006;241(1):213–22. Michel CM, Murray MM, Lantz G, Gonzalez S, Spinelli L, Grave de Peralta R. EEG source imaging. Clin Neurophysiol 2004;115(10): 2195–222. Park HM, Nakasato N, Iwasaki M, Shamoto H, Tominaga T, Yoshimoto T. Comparison of magnetoencephalographic spikes with and without concurrent electroencephalographic spikes in extratemporal epilepsy. Tohoku J Exp Med 2004;203(3):165–74. RamachandranNair R, Otsubo H, Shroff MM, Ochi A, Weiss SK, Rutka JT, Snead OC 3rd. MEG predicts outcome following surgery for intractable epilepsy in children with normal or nonfocal MRI findings. Epilepsia 2007;48(1):149–57. Ramantani G, Boor R, Paetau R, Ille N, Feneberg R, Rupp A, Boppel T, Scherg M, Rating D, Bast T. MEG versus EEG: influence of background activity on interictal spike detection. J Clin Neurophysiol 2006;23(6):498–508. Schaefer M, Muhlnickel W, Grusser SM, Flor H. Reliability and validity of neuroelectric source imaging in primary somatosensory cortex of human upper limb amputees. Brain Topogr 2002;15(2):95–106. Schiffbauer H, Berger MS, Ferrari P, Freudenstein D, Rowley HA, Roberts TP. Preoperative magnetic source imaging for brain tumor surgery: a quantitative comparison with intraoperative sensory and motor mapping. Neurosurg Focus 2003;15(1):E7.
Stefan Rampp Hermann Stefan Epilepsy Center (ZEE) – Department of Neurology, University Hospital, Schwabachanlage 6, 91054 Erlangen, Germany E-mail address: [email protected] (S. Rampp)
Editorial
On the opposition of EEG and MEG See Article, pages 1721–1735
EEG and MEG are complementary – a conclusion frequently encountered in the closing remarks of literature comparing the two electromagnetic modalities. The statement is undoubtedly correct, although there is quite frequently an intentionally calming connotation to it, to mend damage which might have been caused by findings of the respective study. The question whether either EEG or MEG is superior over the other has the potential to turn complementarity to opposition. There are numerous arguments for either modality: scalp EEG is cheaper, easily available, mobile, less of an obstacle for seizure recordings and does not need a magnetically shielded room. MEG on the other hand is contactless and practically insensitive to tissue conductivity differences, resulting in simpler calculations, which might in turn increase localization accuracy of spontaneous or evoked activity. Numerous studies have demonstrated that magnetic and electric fields provide different views on the same generators, although MEG is looking at their intracellular and EEG at their extracellular components. Park et al. (2004) show that scalp EEG might overlook spikes due to background noise, which is also seen by Ramantani et al. (2006). In contrast, Bast et al. (2005) demonstrate insensitivity of MEG for onset of interictal activity in some cases of polymicrogyria. Knake et al. (2006) compared high resolution EEG and multichannel MEG sensitivity for epileptic spikes and found spikes in both modalities in 55.7%, MEG only 12.9% and EEG 2.9%. Iwasaki et al. (2005) found only a small percentage (median 25.7%) of spikes visible simultaneously in both modalities, while the larger amount was detectable only in either EEG or MEG. Differences between these studies can probably be explained by the lower electrode number compared to Knake et al. Nevertheless, both studies show that there is information available only by using both modalities. The difference in perspective is not limited to the localization of epileptic activity. It also includes clinical questions regarding functional areas. Various studies demonstrate that MEG is a suitable answer (Druschky
et al., 2000; Ganslandt et al., 1999; Ishitobi et al., 2005; Korvenoja et al., 2006; Schiffbauer et al., 2003), because of favourable characteristics like the insensitivity to conductivity differences. However, the value of EEG in this field seems underestimated. There is only sparse literature on EEG use in presurgical functional mapping, mostly in conjunction with MEG recordings (Komssi et al., 2004), although there are various studies investigating the method with healthy individuals (Michel et al., 2004; Schaefer et al., 2002). The reason for this deficit of the otherwise frequent use of EEG technology remains unclear. Bast et al. (2007) contribute to fill this gap. They compare EEG with MEG localizations of activity evoked by tactile stimulation under clinical circumstances. It is the latter that sets the work apart, as the environment of patient care is constrained by severe and specific logistical issues. Any clinical method has to be reliable and provide valuable information, especially under suboptimal conditions. They demonstrate that in several cases predominantly with cortical malformations or epileptic discharge foci, EEG and MEG can yield overlapping results in localizing the somatosensory cortex. In these, the combination of both modalities offers a considerable benefit. Neuronal populations are the generators of magnetic and electric fields. Both modalities have their own perspective on these, overlapping in information content but which are neither identical nor completely orthogonal. Investigation of synchronously recorded EEG and MEG separately yields improved diagnostic information, for which a study of Ramachandran et al. (RamachandranNair et al., 2007) provides an example. They found that seizure freedom after epilepsy surgery in children with normal or subtle and nonfocal MRI findings was most likely to occur when there was concordance between EEG and MEG localization and least likely to occur when these results were divergent. Bast et al. (2007) also show that in some cases either modality can add information when the other is not able to do so, e.g. because of an unfavourable signal-to-noise ratio. Reintegration of both complementary, in some ways opposing modalities, however, is another step further.
1388-2457/$32.00 Ó 2007 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2007.04.021
Editorial / Clinical Neurophysiology 118 (2007) 1658–1659
There are promising works combining EEG and MEG information for optimized source localization (Babiloni et al., 2001, 2004; Fuchs et al., 1998). This utilizes sensitivities of both methods and enables superior spatial localization accuracy which is not only due to the increased number of sensors. A large body of publications describes the use of both EEG and MEG, although – and naturally – not free of subjective weighting. There is no doubt that either modality has advantages and disadvantages. However to improve methodology, the amalgamation of electric and magnetic methods into integrated electromagnetic analysis promises a considerable benefit, leading to further amplification of electrophysiology in combination with imaging methods. Sophisticated and intensive training for recording and analysis is necessary to fully develop the inherent potential because use of EEG and MEG combined with imaging needs special and complex instrumentation. In the next step of further development, national and regional research and clinical neurophysiology MEG–EEG centers should be established. References Babiloni F, Carducci F, Cincotti F, Del Gratta C, Pizzella V, Romani GL, Rossini PM, Tecchio F, Babiloni C. Linear inverse source estimate of combined EEG and MEG data related to voluntary movements. Hum Brain Mapp 2001;14(4):197–209. Babiloni F, Mattia D, Babiloni C, Astolfi L, Salinari S, Basilisco A, Rossini PM, Marciani MG, Cincotti F. Multimodal integration of EEG, MEG and fMRI data for the solution of the neuroimage puzzle. Magn Reson Imaging 2004;22(10):1471–6. Bast T, Ramantani G, Boppel T, Metzke T, Ozkan O, Stippich C, Seitz A, Rupp A, Rating D, Scherg M. Source analysis of interictal spikes in polymicrogyria: loss of relevant cortical fissures requires simultaneous EEG to avoid MEG misinterpretation. Neuroimage 2005;25(4):1232–41. Bast T, Wright T, Boor R, Harting I, Feneberg R, Rupp A, Hoechstetter K, Rating D, Baumga¨rtner U. Combined EEG and MEG analysis of early somatosensory evoked activity in children and adolescents with focal epilepsies. Clin Neurophysiol 2007;118:1721–35. Druschky K, Lang E, Hummel C, Kaltenhauser M, Kohlloffel LU, Neundorfer B, Stefan H. Pain-related somatosensory evoked magnetic fields induced by controlled ballistic mechanical impacts. J Clin Neurophysiol 2000;17(6):613–22. Fuchs M, Wagner M, Wischmann HA, Kohler T, Theissen A, Drenckhahn R, Buchner H. Improving source reconstructions by combining bioelectric and biomagnetic data. Electroencephalogr Clin Neurophysiol 1998;107(2):93–111. Ganslandt O, Fahlbusch R, Nimsky C, Kober H, Moller M, Steinmeier R, Romstock J, Vieth J. Functional neuronavigation with magnetoen-
1659
cephalography: outcome in 50 patients with lesions around the motor cortex. J Neurosurg 1999;91(1):73–9. Ishitobi M, Nakasato N, Yoshimoto T, Iinuma K. Abnormal primary somatosensory function in unilateral polymicrogyria: an MEG study. Brain Dev 2005;27(1):22–9. Iwasaki M, Pestana E, Burgess RC, Luders HO, Shamoto H, Nakasato N. Detection of epileptiform activity by human interpreters: blinded comparison between electroencephalography and magnetoencephalography. Epilepsia 2005;46(1):59–68. Knake S, Halgren E, Shiraishi H, Hara K, Hamer HM, Grant PE, Carr VA, Foxe D, Camposano S, Busa E, Witzel T, Hamalainen MS, Ahlfors SP, Bromfield EB, Black PM, Bourgeois BF, Cole AJ, Cosgrove GR, Dworetzky BA, Madsen JR, Larsson PG, Schomer DL, Thiele EA, Dale AM, Rosen BR, Stufflebeam SM. The value of multichannel MEG and EEG in the presurgical evaluation of 70 epilepsy patients. Epilepsy Res 2006;69(1):80–6. Komssi S, Huttunen J, Aronen HJ, Ilmoniemi RJ. EEG minimumnorm estimation compared with MEG dipole fitting in the localization of somatosensory sources at S1. Clin Neurophysiol 2004;115(3):534–42. Korvenoja A, Kirveskari E, Aronen HJ, Avikainen S, Brander A, Huttunen J, Ilmoniemi RJ, Jaaskelainen JE, Kovala T, Makela JP, Salli E, Seppa M. Sensorimotor cortex localization: comparison of magnetoencephalography, functional MR imaging, and intraoperative cortical mapping. Radiology 2006;241(1):213–22. Michel CM, Murray MM, Lantz G, Gonzalez S, Spinelli L, Grave de Peralta R. EEG source imaging. Clin Neurophysiol 2004;115(10): 2195–222. Park HM, Nakasato N, Iwasaki M, Shamoto H, Tominaga T, Yoshimoto T. Comparison of magnetoencephalographic spikes with and without concurrent electroencephalographic spikes in extratemporal epilepsy. Tohoku J Exp Med 2004;203(3):165–74. RamachandranNair R, Otsubo H, Shroff MM, Ochi A, Weiss SK, Rutka JT, Snead OC 3rd. MEG predicts outcome following surgery for intractable epilepsy in children with normal or nonfocal MRI findings. Epilepsia 2007;48(1):149–57. Ramantani G, Boor R, Paetau R, Ille N, Feneberg R, Rupp A, Boppel T, Scherg M, Rating D, Bast T. MEG versus EEG: influence of background activity on interictal spike detection. J Clin Neurophysiol 2006;23(6):498–508. Schaefer M, Muhlnickel W, Grusser SM, Flor H. Reliability and validity of neuroelectric source imaging in primary somatosensory cortex of human upper limb amputees. Brain Topogr 2002;15(2):95–106. Schiffbauer H, Berger MS, Ferrari P, Freudenstein D, Rowley HA, Roberts TP. Preoperative magnetic source imaging for brain tumor surgery: a quantitative comparison with intraoperative sensory and motor mapping. Neurosurg Focus 2003;15(1):E7.
Stefan Rampp Hermann Stefan Epilepsy Center (ZEE) – Department of Neurology, University Hospital, Schwabachanlage 6, 91054 Erlangen, Germany E-mail address: [email protected] (S. Rampp)