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Synthetic aperture magnetometry analysis of epileptic fast oscillation of MEG
International Congress Series 1232 (2002) 587 – 591
Synthetic aperture magnetometry analysis of epileptic fast oscillation of MEG Hirotomo Ninomiya a,*, Amami Kato a, Masayuki Hirata a, Masaaki Taniguchi a, Haruhiko Kijima a, Junji Yamada a, Shunichiro Hirano a, Katsumi Imai b, Toshiki Yoshimine a a
Department of Neurosurgery, Osaka University Graduate School of Medicine, E6, 2-2 Yamadaoka, Suita, Osaka, Japan b Department of Pediatrics, Osaka University Graduate School of Medicine, E6, 2-2 Yamadaoka, Suita, Osaka, Japan
Abstract The interictal MEG was investigated retrospectively to explore the epileptic fast oscillation. The source of the oscillation was analyzed by the SAM-VS method. The localization of the ECD analysis and the source of the oscillation by the SAM-VS method were compared with the MRI findings and the surgical area. MEG data in 5 of the 38 epilepsy patients (13%) included the epileptic fast oscillation. All five cases had the lesion in the MRI. ECD analysis indicated the unilateral lesion in the cases of two TLE, but the distribution of dipoles was scattered in another two TLE and one FLE. SAM-VS analysis of the epileptic fast oscillation succeeded in disclosing the source of the oscillation in all of the five cases. The epileptic region which SAM-VS analysis indicated was closely localized in the lesion of the MRI, which was confirmed as the epileptogenic lesion by the surgery. D 2002 Published by Elsevier Science B.V. Keywords: Epilepsy; Magnetoencephalography; Synthetic aperture magnetometry
1. Introduction Epileptic fast oscillation of MEG was an on-line monitored on rare occasions during the data acquisition. This fast oscillation was not suitable for the ECD analysis on acAbbreviations: MEG, magnetoencephalography; SAM-VS, synthetic aperture magnetometry virtual sensor; ECD, equivalent current dipole; TLE, PLE and FLE, temporal, parietal and frontal lobe epilepsy. * Corresponding author. Tel.: +81-6-6879-3652; fax: +81-6-6879-3659. E-mail address: [email protected] (H. Ninomiya). 0531-5131/02 D 2002 Published by Elsevier Science B.V. PII: S 0 5 3 1 - 5 1 3 1 ( 0 1 ) 0 0 7 8 8 - 9
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Fig. 1. The SAM virtual sensors of case 3. Virtual sensors were synthesized in the lattice of 1.5-cm width within the brain. Underlined sensors showed epileptic activity on the SAM current odensitogram (see Fig. 3).
count of low dipolarity. However, the SAM-VS analysis we reported enables the serial analysis of the MEG of epilepsy patients as if a virtual ECoG study was performed, even though the MEG is out of phase [1]. This time, we paid attention to the epileptic
Fig. 2. Epileptic oscillation of interictal MEG. MEG of the right channels was in the right column. Epileptic fast oscillation was observed on the right channels and spread to the left in case 3.
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oscillation of MEG retrospectively and aimed to disclose the source by the SAM-VS analysis.
2. Subjects and methods 2.1. Meg data A helmet-shaped 64-channel SQUID system (Model 100, CTF Systems) was used for the MEG data acquisition. MEG data was collected by the sampling rate of 625 or 1250 Hz. MEG raw data of 38 epilepsy patients collected from October 1997 to October 2000 were reviewed retrospectively. Then, MEG data including fast oscillation were used for the following SAM-VS analysis, and the residual MEG data of same patient was performed by ECD analysis. 2.2. Dipole analysis A single ECD modeling was used for the estimation of the source of interictal spikes on MEG. The ECD was superimposed on the MRI scanned with the same fiducial markers that were coordinated with the calibrating points during MEG recording.
Fig. 3. SAM current densitogram. Fast epileptic activity started from the right temporal lobe, and parietal lobe and propagated.
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H. Ninomiya et al. / International Congress Series 1232 (2002) 587–591
2.3. SAM-VS SAM is a high-resolution spatial filtering based on the algorithm of Frost’s adaptive beamformer [2]. SAM works to improve the signals to noise ratio of MEG signals by combining the signals from an array of sensors using a set of weighting factors, and it enables to measure current odensitogram of the small portion of the brain with an enhanced sensitivity. Then, the regional electrical activity of the brain could be measured as if subdural or depth electrodes were inserted (SAM-VS method). SAM virtual sensors were synthesized in the lattice of 1.0- to 1.5-cm width within the brain (Fig. 1). The current odensitogram of SAM-VS was inspected every millisecond to determine the origin of epileptic discharge and its sequence of spreading (Figs. 2 and 3). The virtual sensors, which showed the primary change of current density, were considered as the epileptic sensors and the location of the sensors was classified according to the anatomical aspects and compared with the results of MEG-ECD analysis and the surgical results.
3. Results Fast oscillation of MEG was collected from 5 of 38 epilepsy patients (Table 1). Five patients were consisted of two MTLE, two TLE and one FLE. All patients had the lesion on the MRI. Convergent distribution of dipoles was observed in the case of the unilateral hippocampal sclerosis and the astrocytoma of the medial temporal region, and ECD analysis succeeded in indicating the epileptic lesion in these two cases. In another three cases, ECD analysis failed on the account of the scattered distribution of dipoles. The source of the fast oscillation disclosed by the SAM was the lesion of the MRI in all the five cases. In the two cases of MTLE, the sensors of medial temporal region indicated the primary change of the frequency of the SAM current densitogram. In the case of the TLE associated with the astrocytoma, abnormal oscillation came up not from the lateral temporal lobe but from behind the brain tumor. In the case of TLE with PLE, the sensors of lateral temporal lobe and parietal lobe demonstrated the abnormal discharge. In the case of FLE, abnormal sensors were located in the frontobasal region. Four of five cases were operated and confirmed the epileptogenic region. The sensors, which showed the abnormal oscillation, indicated the operated region.
Table 1 Diagnosis
Age/Sex
MRI findings
ECD
SAM
MTLE MTLE TLE and OLE TLE FLE
25 43 39 27 23
R.HS Bil.HS R.Occ.AVM R.Med.glioma traumatic scar
R.Med.TL Bil.Med.TL scattered R.Med.TL scattered
R.Med.TL R.Med.TL R.TL and PL R.Med.TL R.FL
F M F F M
R, right; Bil, bilateral; Occ, occipital; Med, medial; HS, hippocampal sclerosis; AVM, arteriovenous malformation; TL, temporal lobe; PL, parietal; FL, frontal lobe.
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4. Discussion Epileptic train on the ECoG was closely related to the epileptic focus [3]. However, interictal epileptic oscillation was observed on the EEG in few chances, compared with the ECoG study. However, we confirmed in this study, epileptic oscillation was detected from 13% of epilepsy patients even during the interictal MEG examination for the ECD analysis. Though the routine analysis is stressed on the collection of the epileptic spikes, we think that the exploration of the oscillation is required in the era of a whole-head multichannel magnetometer. There were some reports that the ECD analysis of interictal MEG resulted in the epileptogenic lesion [4,5]. However, SAM-VS method could discriminate complex epileptic spread in the brain with superior spatial and time resolution as if virtual electrodes were inserted in the brain. In the operated cases, the recruited sensors of the oscillation were indicated in the surgical region. SAM-VS method would be quite suitable to delineate the area of epileptic discharge derived from the large area in the brain or the dual pathology.
5. Conclusion Epileptic oscillation of MEG was observed in 5 out of the 38 epilepsy patients. In two of five cases, ECD analysis failed. The SAM-VS analysis succeeded in disclosing the source of the oscillation in all cases. The epileptic region which SAM-VS analysis indicated was closely localized in the epileptogenic lesion confirmed by the surgery.
Acknowledgements This study was supported in part by a Grant-in-Aid for Scientific Research (11470290) from the Japanese Ministry of Education, Science and Culture and Grants from Osaka Medical Foundation for Incurable Diseases, Shimadzu Science Foundation, Japan Epilepsy Research Foundation and National Cardiovascular Center.
References [1] H. Ninomiya, T. Yoshimine, Y. Nii, et al., MEG study of temporal epilepsy—dipole analysis and synthetic aperture magnetometry, in: T. Yoshimoto, M. Kotani, S. Kuriki, H. Karibe, N. Nakasato (Eds.), Recent Advances in Biomagnetism, Tohoku University Press, Sendai, 1999, pp. 786 – 789. [2] M. Taniguchi, A. Kato, N. Fujita, et al., Movement-related desynchronization of the cerebral cortex studied with spatially filtered magnetoencephalography, NeuroImage 12 (2000) 298 – 306. [3] A. Palmini, A. Gambardella, F. Andermann, et al., Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results, Ann. Neurol. 37 (4) (1995) 476 – 487. [4] M. Taniguchi, T. Yoshimine, A. Kato, et al., Dysembryoplastic neuroepithelial tumor in the insular cortex. Three-dimensional magnetoencephalographic localization of epileptic discharges, Neurol. Res. 20 (5) (1998) 433 – 438. [5] T. Yoshimine, A. Kato, M. Taniguchi, et al., Translucence stereoscopy of interictal magnetoencephalographic epileptiform discharge, Neurol. Res. 20 (7) (1998) 572 – 576.
Synthetic aperture magnetometry analysis of epileptic fast oscillation of MEG Hirotomo Ninomiya a,*, Amami Kato a, Masayuki Hirata a, Masaaki Taniguchi a, Haruhiko Kijima a, Junji Yamada a, Shunichiro Hirano a, Katsumi Imai b, Toshiki Yoshimine a a
Department of Neurosurgery, Osaka University Graduate School of Medicine, E6, 2-2 Yamadaoka, Suita, Osaka, Japan b Department of Pediatrics, Osaka University Graduate School of Medicine, E6, 2-2 Yamadaoka, Suita, Osaka, Japan
Abstract The interictal MEG was investigated retrospectively to explore the epileptic fast oscillation. The source of the oscillation was analyzed by the SAM-VS method. The localization of the ECD analysis and the source of the oscillation by the SAM-VS method were compared with the MRI findings and the surgical area. MEG data in 5 of the 38 epilepsy patients (13%) included the epileptic fast oscillation. All five cases had the lesion in the MRI. ECD analysis indicated the unilateral lesion in the cases of two TLE, but the distribution of dipoles was scattered in another two TLE and one FLE. SAM-VS analysis of the epileptic fast oscillation succeeded in disclosing the source of the oscillation in all of the five cases. The epileptic region which SAM-VS analysis indicated was closely localized in the lesion of the MRI, which was confirmed as the epileptogenic lesion by the surgery. D 2002 Published by Elsevier Science B.V. Keywords: Epilepsy; Magnetoencephalography; Synthetic aperture magnetometry
1. Introduction Epileptic fast oscillation of MEG was an on-line monitored on rare occasions during the data acquisition. This fast oscillation was not suitable for the ECD analysis on acAbbreviations: MEG, magnetoencephalography; SAM-VS, synthetic aperture magnetometry virtual sensor; ECD, equivalent current dipole; TLE, PLE and FLE, temporal, parietal and frontal lobe epilepsy. * Corresponding author. Tel.: +81-6-6879-3652; fax: +81-6-6879-3659. E-mail address: [email protected] (H. Ninomiya). 0531-5131/02 D 2002 Published by Elsevier Science B.V. PII: S 0 5 3 1 - 5 1 3 1 ( 0 1 ) 0 0 7 8 8 - 9
588
H. Ninomiya et al. / International Congress Series 1232 (2002) 587–591
Fig. 1. The SAM virtual sensors of case 3. Virtual sensors were synthesized in the lattice of 1.5-cm width within the brain. Underlined sensors showed epileptic activity on the SAM current odensitogram (see Fig. 3).
count of low dipolarity. However, the SAM-VS analysis we reported enables the serial analysis of the MEG of epilepsy patients as if a virtual ECoG study was performed, even though the MEG is out of phase [1]. This time, we paid attention to the epileptic
Fig. 2. Epileptic oscillation of interictal MEG. MEG of the right channels was in the right column. Epileptic fast oscillation was observed on the right channels and spread to the left in case 3.
H. Ninomiya et al. / International Congress Series 1232 (2002) 587–591
589
oscillation of MEG retrospectively and aimed to disclose the source by the SAM-VS analysis.
2. Subjects and methods 2.1. Meg data A helmet-shaped 64-channel SQUID system (Model 100, CTF Systems) was used for the MEG data acquisition. MEG data was collected by the sampling rate of 625 or 1250 Hz. MEG raw data of 38 epilepsy patients collected from October 1997 to October 2000 were reviewed retrospectively. Then, MEG data including fast oscillation were used for the following SAM-VS analysis, and the residual MEG data of same patient was performed by ECD analysis. 2.2. Dipole analysis A single ECD modeling was used for the estimation of the source of interictal spikes on MEG. The ECD was superimposed on the MRI scanned with the same fiducial markers that were coordinated with the calibrating points during MEG recording.
Fig. 3. SAM current densitogram. Fast epileptic activity started from the right temporal lobe, and parietal lobe and propagated.
590
H. Ninomiya et al. / International Congress Series 1232 (2002) 587–591
2.3. SAM-VS SAM is a high-resolution spatial filtering based on the algorithm of Frost’s adaptive beamformer [2]. SAM works to improve the signals to noise ratio of MEG signals by combining the signals from an array of sensors using a set of weighting factors, and it enables to measure current odensitogram of the small portion of the brain with an enhanced sensitivity. Then, the regional electrical activity of the brain could be measured as if subdural or depth electrodes were inserted (SAM-VS method). SAM virtual sensors were synthesized in the lattice of 1.0- to 1.5-cm width within the brain (Fig. 1). The current odensitogram of SAM-VS was inspected every millisecond to determine the origin of epileptic discharge and its sequence of spreading (Figs. 2 and 3). The virtual sensors, which showed the primary change of current density, were considered as the epileptic sensors and the location of the sensors was classified according to the anatomical aspects and compared with the results of MEG-ECD analysis and the surgical results.
3. Results Fast oscillation of MEG was collected from 5 of 38 epilepsy patients (Table 1). Five patients were consisted of two MTLE, two TLE and one FLE. All patients had the lesion on the MRI. Convergent distribution of dipoles was observed in the case of the unilateral hippocampal sclerosis and the astrocytoma of the medial temporal region, and ECD analysis succeeded in indicating the epileptic lesion in these two cases. In another three cases, ECD analysis failed on the account of the scattered distribution of dipoles. The source of the fast oscillation disclosed by the SAM was the lesion of the MRI in all the five cases. In the two cases of MTLE, the sensors of medial temporal region indicated the primary change of the frequency of the SAM current densitogram. In the case of the TLE associated with the astrocytoma, abnormal oscillation came up not from the lateral temporal lobe but from behind the brain tumor. In the case of TLE with PLE, the sensors of lateral temporal lobe and parietal lobe demonstrated the abnormal discharge. In the case of FLE, abnormal sensors were located in the frontobasal region. Four of five cases were operated and confirmed the epileptogenic region. The sensors, which showed the abnormal oscillation, indicated the operated region.
Table 1 Diagnosis
Age/Sex
MRI findings
ECD
SAM
MTLE MTLE TLE and OLE TLE FLE
25 43 39 27 23
R.HS Bil.HS R.Occ.AVM R.Med.glioma traumatic scar
R.Med.TL Bil.Med.TL scattered R.Med.TL scattered
R.Med.TL R.Med.TL R.TL and PL R.Med.TL R.FL
F M F F M
R, right; Bil, bilateral; Occ, occipital; Med, medial; HS, hippocampal sclerosis; AVM, arteriovenous malformation; TL, temporal lobe; PL, parietal; FL, frontal lobe.
H. Ninomiya et al. / International Congress Series 1232 (2002) 587–591
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4. Discussion Epileptic train on the ECoG was closely related to the epileptic focus [3]. However, interictal epileptic oscillation was observed on the EEG in few chances, compared with the ECoG study. However, we confirmed in this study, epileptic oscillation was detected from 13% of epilepsy patients even during the interictal MEG examination for the ECD analysis. Though the routine analysis is stressed on the collection of the epileptic spikes, we think that the exploration of the oscillation is required in the era of a whole-head multichannel magnetometer. There were some reports that the ECD analysis of interictal MEG resulted in the epileptogenic lesion [4,5]. However, SAM-VS method could discriminate complex epileptic spread in the brain with superior spatial and time resolution as if virtual electrodes were inserted in the brain. In the operated cases, the recruited sensors of the oscillation were indicated in the surgical region. SAM-VS method would be quite suitable to delineate the area of epileptic discharge derived from the large area in the brain or the dual pathology.
5. Conclusion Epileptic oscillation of MEG was observed in 5 out of the 38 epilepsy patients. In two of five cases, ECD analysis failed. The SAM-VS analysis succeeded in disclosing the source of the oscillation in all cases. The epileptic region which SAM-VS analysis indicated was closely localized in the epileptogenic lesion confirmed by the surgery.
Acknowledgements This study was supported in part by a Grant-in-Aid for Scientific Research (11470290) from the Japanese Ministry of Education, Science and Culture and Grants from Osaka Medical Foundation for Incurable Diseases, Shimadzu Science Foundation, Japan Epilepsy Research Foundation and National Cardiovascular Center.
References [1] H. Ninomiya, T. Yoshimine, Y. Nii, et al., MEG study of temporal epilepsy—dipole analysis and synthetic aperture magnetometry, in: T. Yoshimoto, M. Kotani, S. Kuriki, H. Karibe, N. Nakasato (Eds.), Recent Advances in Biomagnetism, Tohoku University Press, Sendai, 1999, pp. 786 – 789. [2] M. Taniguchi, A. Kato, N. Fujita, et al., Movement-related desynchronization of the cerebral cortex studied with spatially filtered magnetoencephalography, NeuroImage 12 (2000) 298 – 306. [3] A. Palmini, A. Gambardella, F. Andermann, et al., Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results, Ann. Neurol. 37 (4) (1995) 476 – 487. [4] M. Taniguchi, T. Yoshimine, A. Kato, et al., Dysembryoplastic neuroepithelial tumor in the insular cortex. Three-dimensional magnetoencephalographic localization of epileptic discharges, Neurol. Res. 20 (5) (1998) 433 – 438. [5] T. Yoshimine, A. Kato, M. Taniguchi, et al., Translucence stereoscopy of interictal magnetoencephalographic epileptiform discharge, Neurol. Res. 20 (7) (1998) 572 – 576.