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Chapter 40 Source localization of interictal epileptiform spike potentials estimated with a dipole tracing method using surface and subdural EEG recordings
Clinical Neurophysiologyat tbe Beginning a/the 21st Century (Supplements to Clinical Neurophysiology Vol. 53) Editors: Z. Ambler. S. Nevsimalova. Z. Kadailka. P.M. Rossini Cl2000 ElsevierScience B.V. All rights reserved.
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Chapter 40
Source localization of interictal epileptiform spike potentials estimated with a dipole tracing method using surface and subdural EEG recordings R. Flink a .*, S. Homma", A. Kanamaru", K. Miyamoto" and Y. Okamoto" 'Department of Clinical Neurophysiology, University Hospital, S-75i85 Uppsala (Sweden) bChiba University, Chiba (Japan) "Department of Physiology, Showa University School of Medicine, Tokyo (Japan) dChuo Electronics Co., Tokyo (Japan) 'Department of Electric Engineering, Chiba institute of Technology, Chiba (Japan)
Introduction The paroxysmal depolarization shift of epileptogenic neurons resulting in synchronous discharges in circumscribed neuronal populations can usually be recorded with surface EEG electrodes. The analysis of interictal and ictal EEG activity is, together with seizure semiology and structural and functional neuroradiology, the method of choice in order to locate the epileptic focus in patients with partial epileptic seizures. This is of particular importance in patients with intractable seizures undergoing preoperative evaluation for epilepsy surgery. With the dipole tracing (DT) method (Okamoto et al. 1983; Cuffin 1985; Smith et al. 1985; Meijs et al. 1989),current sources in the brain can be located from EEG recordings using surface electrodes. There are different algorithms to estimate the location of the electric source generator in a 3-dimen-
* Correspondence to: Dr. Roland Flink, Department of Clinical Neurophysiology, University Hospital, S-75l85 Uppsala (Sweden). E-mail: [email protected]
sional spherical model of the head (Cohen et al. 1990; Scherg 1990; Cuffin et al. 1991). We have previously used a realistic 3 shell head model taking into account standard conductivities (Cuffin 1985; Sidman et al. 1989) of the 3 layers, scalp, skull and brain, the SSBIOT method (Homma et al. 1994; 1995). In the present study, the SSBIOT method was used to estimate the location of interictal epileptiform spike activity in two patients undergoing preoperative evaluation for epilepsy surgery. Instead of using the same, standard conductivity values for scalp and skull on both patients, the individual conductivities for each subject were calculated by electrical stimulation of the surface EEG electrodes (Okamoto et al. 1997) and the SSB head model was used with these individually calculated conductivities. Furthermore, the same spike potentials recorded with surface EEG electrodes were simultaneously recorded with intracranial subdural strip electrodes. In the case of the intracranial recordings, the dipole location was estimated with the BlOT method using a single layer head model with the realistic shape of the brain excluding the
276
scalp and the skull. The realistic brain model was constructed from the inner skull bone surface of consecutive CT scans. Since this BlOT method does not have to take into account the conductivities of surrounding tissue, it is plausible to suggest that the estimated location of an electric source generator with the BlOT method would be the most accurate. We compare in the present study the locations of the interictal epileptiform spike activity estimated with the SSBIOT and BlOT methods in two patients.
Material and methods Two patients (KC and IK) with intractable partial complex seizures, who underwent intracranial seizure monitoring with subdural strip electrodes, were investigated. Both patients had epileptic seizures for several years, with typical temporal seizure semiology. There were no structural findings on the MRI scans but the PET scan with fluorodeoxy glucose showed lateralization of hypometabolism to one of the temporal lobes. Surface EEG recordings including sphenoidal electrodes showed interictal spiking from both temporal lobes with a preponderance for the side with hypometabolism. The simultaneous recordings with surface and intracranial electrodes and the electrical surface stimulation were performed one afternoon during the monitoring period where there had been no clinical seizures the previous morning. The patients were informed of the procedure of the dipole tracing method and gave their informed consent. The interictal spike activity was recorded simultaneously from the intracranial subdural strip electrodes and from 21 surface EEG electrodes placed on the scalp according to a modified 10/20 system. The shape of the scalp was measured with a semispherical helmet with 64 probes and 21 of the probes were marked for electrode location. A 3dimensional shape of the scalp could be created from this measurement using the plane through the orbita and the external meatus acusticus as the zero plane and the midpoint between the two external meatus acusticus as the zero point for the
xyz coordinate system. In order to create the 3 shell
realistic head model, CT scans with a thickness of 3 mm were made in the horizontal plane using the same angle as for the helmet. The skull and brain shells were reconstructed with an image scanner from the consecutive CT-scans using the outer skull bone surface as the skull shell and the inner skull bone surface as the brain shell. The brain shell was used as a brain model for the BlOT calculations. In previous studies with the SSBIOT method, the standard conductivities for the 3 shells, scalp, skull and brain of 0.33: 0.0041: 0.33 Slm, respectively, have been used. In the present study the individual conductivities for the outer two layers for each subject were calculated by electrical stimulation. A current square wave pulse (0.1 rnA and 5 ms duration) was applied through a pair of EEG electrodes, 4 different pairs were usually selected. The voltage change during the stimulation was recorded with the remaining surface electrodes and the conductivity of the scalp and skull could be calculated from the recorded signals (Okamoto et al. 1997). The method was tested in our laboratory by stimulating extracranial electrodes and recording with intracranial electrodes. A fixed value of 0.33 Sim was chosen for the conductivity of the brain and the relative conductivities of scalp:skull:brain were decided. The algorithm for calculating the dipole location follows an iterative procedure both for the SSBIOT as well as the BlOT method. A location of an equivalent dipole source is chosen at random and the surface potentials evoked from this source are calculated for the 21 electrodes. The square differences of the recorded and the calculated potentials are calculated and then the dipole is repeatedly moved in order to minimize the sum of the square differences (Homma et al. 1994). When that is obtained, the location of the dipole source is decided. The residual difference between the measured and calculated potentials (the error) is expressed in percent and referred to as the dipolarity. If there is a perfect match, the dipolarity will be 100% and there is no error. We decided from a previous study with intracranial stimulations (Musha and Homma 1990) to use a dipolarity of
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98% as a criterion for significant dipole location. A dipole location with dipolarity below 98% was considered as not significant.
Results The stimulation procedure was used to calculate the conductivities of the two outer layers (scalp and skull) of the 3 shell head model. The conductivity of the scalp was 0.072 and 0.0047 Sim for the skull of subject KC, 0.60 for scalp and 0.011 Sim for skull for subject IK. The standard value of 0.33 SI m was used for the brain conductivity in both cases. The SSB-DT method was used to calculate location of the current sources of interictal epileptiform spikes recorded with the surface electrodes in both subjects. The individual conductivities, calculated from the stimulation procedure, were used. We averaged several spikes in order to reduce the noise of the background EEG activity (Fig. I). Both subjects showed bilateral temporal spike activity. The same spike potentials recorded with surface electrodes were simultaneously recorded with intracranial subdural strip electrodes. Since these were subdurally implanted thus recording directly from the brain surface, the impedance from scalp and skull could be disregarded. Interictal spike potentials recorded with the intracranial subdural electrodes were averaged (Fig. 3) and the dipole method was used in the single layer model (BI DT) to calculate the source location. A comparison was made between source location calculated from the surface electrode recording and the intracranial recording for the same spikes (Fig. 7). Source generators of subject KC estimated from surface recordings
temporal lobe (Fig. 2) corresponding to the cortical area of the inferior gyrus on the MRI scan. The current dipole of the negative peak preceding the positive peak was also calculated to have the same location but with an opposite vector moment direction. It was concluded that the negative and the positive peaks are generated from the same source in the right temporal lobe. Six interictal spikes of the L type were averaged from the surface EEG (Fig. I) and the estimated dipole location of the negative peak of the spike was found to be in the left temporal lobe corresponding to the cortex of the inferior temporal gyrus (Fig. 2). The dipolarity was found to be 99.9%. Eight interictal spikes of the H type were averaged and the location of the negative peak was estimated at the midline. Since that location would be unlikely we continued the calculations using the two-dipole algorithm (Homma et al. 1994). We postulated that the calculated dipole would be the summation of two simultaneous generators. With the two-dipole estimation, two simultaneous generator sources were found bilaterally in the temporal lobes in the right and left hippocampus as shown in Fig. 2 with a dipolarity of 99.9%. Source generators of subject KC estimated from subdural recordings
The location of the current sources of the interictal spikes recorded with subdural electrodes were estimated with the B/DT method. The location of the intracranial subdural strip electrodes is illustrated in the lower frame of Fig. 2. The influence of the impedance of the scalp and skull could be excluded and the brain could be regarded as an uniform conductor using the conductivity of 0.33 S/m.
Three different types of interictal epileptiform spikes could visually be detected from the surface EEG recordings, the R, Land H type (Fig. 1). Three interictal spikes of the R type were averaged in order to reduce the background noise. The dipole location of the upward positive peak was estimated with the SSB/DT method. The dipolarity was 99.8% and the location found to be in the right
The R and the L type spikes could be identified from the subdural recording, but not the H type spikes (Fig. 1). Nine interictal spikes of the R type were averaged (Fig. 3) and the dipole estimation with the B/DT method gave a dipolarity of 98.8% and a location in the right temporal lobe in the inferior gyrus overlapping the location calculated from the R type spike of the scalp EEG
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1s Fig, I. Interictal epileptiform spikes recorded from subject KC with 21 surface electrodes. Three different interictal spikes, type R, L and H were identified visually from the surface recording, The positive peaks of 3 R spikes, and the negative peaks of 6 L spikes and 8 H spikes were averaged, The averaged spikes (Ave) are shown in the right columns of the respecti ve spike types. The dipole locations of the negative peaks of the averaged spikes were estimated with the SSBIDT method.
recording (Figs. 2 and 7). Ten interictal spikes of the L type were averaged in the same way (Fig. 3) and the dipole location was estimated to the left
temporal lobe in the inferior gyrus with a dipolarity of 98.6%. The location corresponded to the location calculated from the L type spikes of the scalp EEG
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Fig. 2. The dipole locations of the source generators of subject KC. The upper figures show the dipole locations of R, Land H spikes (filled circles), estimated with the SSBIDT method from surface EEG recordings. Notice that the source for the H type spike is found bilaterally. The lower figures show the dipole locations of the R and L spikes (unfilled circles), estimated with the BIDT method from EEG recordings with subdural electrodes. The location of the surface EEG electrodes is indicated with crosses in the upper figures and the location of the subdural electrodes in the lower figures (subdural electrodes left side (A-C); right side (D-F». R, right; L, left.
(Figs. 2 and Fig. 7). On the other hand, the H type spikes of the scalp EEG were not recorded with subdural electrodes in the case of subject KC (see Discussion). Thus, as seen in Fig. 7, the discrepancy between the dipole locations calculated with the SSBIDT and the BIDT methods was less than 5 mm both for the R and the L type spikes. Source generators of subject IK estimated from surface recordings
In the case of IK, 3 different interictal spikes, type R, H and L, could be detected from the surface EEG recording (Fig. 4). Five spikes of the R type, 4
spikes of the H type and 5 spikes of the L type were averaged and the dipole locations of the different spikes were estimated with the SSBIDT method. The respective dipolarities were 98.6, 98.5 and 97.6%. The dipolarity of the L type did not fully meet the significant dipolarity value of 98%, but was so close that we accepted the SSBIDT estimation. The locations of the different spikes are shown in the upper frame of Fig. 5. The source generator of the R type spikes was located in the right temporal lobe corresponding to the superior temporal gyrus, that of the H type in the left hippocampus and that of the L type in the left temporal lobe corresponding to the superior temporal gyrus.
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Fig. 3. Interictal epileptiform spike potentials of subject KC recorded with 27 subdural electrodes. The Rand L type spikes were identified from the subdural recording. Nine spikes of the R type and 10 spikes of the L type were averaged. The averaged spikes (Ave) are shown in the right columns of the respective spike types.
We did not use the two-dipole algorithm in this case since there were no midline location of dipoles.
Source generators of subject IK estimated from subdural recordings
The same 3 types of interictal spikes, R, Hand L could also be detected from the intracranial recording with subdural strip electrodes. Eleven spikes of the R type, 4 spikes of the H type and 6 spikes of the L type were collected to be averaged (Fig. 6). The dipole locations for the different types of spikes were estimated with the BIDT method. The different dipolarities were calculated as 98.4, 98.9 and 99.3%, respectively, for R, Hand L type spikes. The location and vector moments are shown in Fig. 5. The source generators were located in the superior temporal gyrus of the right temporal lobe, the hippocampus and the superior temporal gyrus of the left temporal lobe and completely overlapped the locations calculated from the surface EEG recordings with the SSBIDT method (Figs. 5 and 7). The discrepancy between the locations calculated with SSBIDT and BIDT methods were in all cases less than 5 mm. The results from the two subjects (KC and IK) are summarized in Fig. 7. There is almost a complete overlap between dipole location estimated from surface EEG recordings using the SSBIDT method in combination with individual measurement of the conductivity of the scalp and skull and the dipole location estimated from the subdural intracranial EEG recordings using the B/ DT method. The discrepancy between the two methods in dipole location is less than 5 mm. Also the vector moments obtained by the SSBIDT and the B/DT methods are orientated in the same direction. If the intracranial recording is accepted as the golden standard for locating interictal and ictal spike activity, we conclude that the SSBIDT method in combination with individual measurement of the conductivity of the scalp and skull can determine the current dipole location with the same precision as the intracranial recording. On the other hand, the intracranial electrodes, as in the case of subject KC, may not record potentials of source generators far from the electrodes as can be recorded with surface EEG electrodes (see Discussion). The SSBIDT method, however, can estimate dipole location from surface EEG-recordings with
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1s Fig. 4, Interictal epileptiform spikes recorded from subject IK with 21 surface electrodes. Three different interictal spikes, type R, L and H, were identified visually from the surface recording. Five spikes each of the R and the L type and 4 spikes of the H type were averaged and are shown in the right columns of the respective spike types (Ave).
the same precision as the BlOT method using intracranial recordings, thus making the SSBIOT method a most useful tool to calculate the dipole location of source generators in the human brain.
Discussion The difference in conductivities for scalp and skull between the two subjects can be explained
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Fig. 5. Source generators of the averaged spike types, R, Land H, of subject IK, estimated from surface EEG recordings (filled circles, upper row) and from subdural recordings (unfilled circles, lower row). The location of the surface EEG electrodes is indicated with crosses in the upper row and the location of the subdural electrodes in the lower row. R, right; L, left.
by the scalp conditions, body temperature, sweating as well as the difference in skull bone thickness. The thickness of the skull bone in IK was thinner than that of KC serving as one explanation for the larger conductivity in IK. Differences in the conductivities for scalp and skull will affect the estimation of the calculated dipole location. This underlines the importance of taking the conductivities into consideration when making the dipole analysis. In a previous study (Homma et al. 1994) using the SSBIOT method with fixed relative conductivities for scalp, skull and brain (l: 1/ 80:1), the averaged dislocation was found to be 8.5 mm when comparing calculated dipole location with location of stimulated, intracranially located subdural electrodes. In this study the dislocation between dipole location calculated from intracranial subdural strip electrodes and extracranial surface EEG electrodes was less than 5 mm.
Although the vector moments for the different sources showed the same orientation when calculated from surface and intracranial recordings there is still not a complete overlap with respect to location. There may be several reasons to explain that residual error. At present we have concluded that the dipole location determined by the BlOT method represents the real foci of the source generator. However, the subdural electrodes attached to the cortical surface will only record potentials from source generators close to the electrode (Blom et al. 1989), since the lead field for the source generator is localized to only a small area. In the case of subject KC, the H type spikes recorded from the scalp EEG, were not recorded from the subdural electrodes probably because the subdural strips were not inserted deeply enough. In the case of subject IK, the tip of the subdural strips were more medially inserted, thus recording potentials
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1s Fig. 6, Interictal epileptiform spikes of subject IK recorded with 16 subdural electrodes, The R, L and H type spikes were identified from the subdural recording. Eleven spikes of the R type, 4 spikes of the H type and 6 spikes of the L type were averaged, respectively. The averaged spike potentials are shown in the respective right columns.
of deep generator sources as in the hippocampus (compare location of subdural strip electrodes seen in the lower frame of Figs, 2 and 5). In other
words, the subdural electrodes might on some occasions be to selective. Even though we have tried to calculate the individual conductivities of the 3
284
KC
Fig. 7. Source generators of subjects KC and IK estimated with the SSB/DT method from EEG recordings with surface electrodes and with the BlOT method from EEG recordings with subdural electrodes, respectively. The dipole locations calculated from surface recordings are shown with filled circles (the direction of the vector moment of the current is also indicated) and the dipole locations from subdural recordings are shown with unfilled circles. The two methods showed very similar results and the discrepancy between the dipole locations when comparing the same type of spikes calculated with SSBIOT method and BlOT method was less than 5 mm. R, right; L, left.
shells in the realistic head model, the inhomogeneity of the skull bone must be considered, especially since these calculations were performed in patients with intracranial subdural electrodes which are introduced through burr holes in the skull bone. There are topographical differences in the skull bone conductivity such as various bone openings in the skull base and the air-containing mastoid cells in the temporal bone, which will affect the dipole location and it remains to be seen whether these differences can be taken into account in the calculations. Several authors have pointed out the clinical use of dipole analysis from surface EEG in patients
with focal epilepsy (Homma et aI. 1990; Ebersole 1991; Sutherling et aI. 1991; Stefan et aI. 1993; Flink et aI. 1996; Lantz et al., 1997). In epilepsy groups working with preoperative evaluation of patients with intractable epilepsy, there have been studies comparing intracranial EEG recordings with dipole analysis with surface EEG electrodes as well as comparisons between dipole location and structural (MRI) and functional (PET, SPECT) neuroimaging (Lantz et al. 1994; 1996; Flink et al. 1996) showing a good correlation between dipole results and the other localizing methods. Both of the patients investigated in this study
285
appeared to have bilateral interictal spiking which could be concluded from the dipole analysis showing source generators in both temporal lobes. The bilateral foci were obvious in the subdural recordings but at least in one case (KC) not obvious when visually analyzing the surface EEG recordings. The bilateral temporal epileptogenicity was furthermore confirmed by intracranial seizure monitoring. Since the bilateral temporal dysfunction increases the risk of postoperative memory problems, none of the two patients have been operated on even though the PET scans showed lateralizing signs of hypometabolism. Further studies will show whether the SSB/DT method with individual conductivities will be useful also for extra-temporal epileptic foci. However, by introducing individual conductivities into the calculations, the dislocation of the estimated dipole location has decreased, thus increasing the value of the method for clinical use.
Acknowledgements The authors acknowledge the help from professors K.-E. Hagbarth and I. Homma. We also would like to thank Chuo Electronic Company for providing the equipment used in the study. The study was supported by grants from the Swedish Medical Research Council, project no. K98-14X09482-08C, and the Margaretha Hemmet Foundation.
EEG localization accuracy using implanted sources in the human brain. Ann. Neurol., 1991,29: 132-138. Ebersole, 1.S. EEG dipole modeling in complex partial epilepsy. Brain Topogr., 1991,4: 113-123. Flink, R., Blom, S. and Hagbarth, K.-E. The electric dipole method in the preoperative evaluation of epilepsy surgery patients. In: 1. Kimura and H. Shibasaki (Eds.), Recent Advances in Clinical Neurophysiology. Elsevier, Amsterdam, 1996: 983-989. Homma, S., Nakajima, Y., Musha, T., Okamoto, Y., Hagbarth, K.E., Blorn, S. and Flink, R. Generator mechanisms of epileptic potentials analyzed by dipole tracing method. Neurosci. Lett..
1990, 113: 181-186. Homma, S., Musha, T., Nakajima, Y., Okamoto, Y., Blom, S., Flink, R., Hagbarth, K.-E. and Mostrom, U. Location of electric current sources in the human brain estimated by dipole tracing method of the scalp-skull-brain (SSB) head model. Electroenceph. din. Neurophysiol., 1994. 91: 374-382. Hornrna, S., Musha, T., Nakajima, Y.. Okamoto, Y., Blorn, S., Flink, R. and Hagbarth, K.-E. Conductivity ratios of the scalpskull-brain head model in estimating equivalent dipole sources in human brain. Neurosci. Res., 1995,22: 51-55. Lantz, G., Ryding, E. and Rosen, I. Three-dimensional localization of interictal epileptiform activity with dipole analysis: comparison with intracranial recordings and SPECT findings. J. Epilepsy, 1994,7: 117-129. Lantz, G., Holub, M., Ryding, E. and Rosen, I. Simultaneous intracranial and extracranial recording of interictal epileptiform activity in patients with drug resistant partial epilepsy: patterns of conduction and results from dipole reconstructions. Electroenceph. dill. Neurophysiol., 1996,99: 69-78. Lantz, G.. Ryding, E. and Rosen, I. Dipole reconstruction as a method for identifying patients with meso limbic epilepsy. Seizure, 1997,6: 303-310. Meijs, 1.W.H., Weier, O.W., Peters. MJ. and van Oosteram, A. On the numerical accuracy of the boundary element method. IEEE Trans. Biomed. Eng.. 1989,36: 1038-1049. Musha, T. and Homma, S. Do optimal dipoles obtained by the dipole tracing method always suggest true source locations? Brain Topogr.• 1990: 3: 143-150. Okamoto, Y., Teramachi, Y.. Musha, T., Tsunakawa, H. and Harumi, K. Limitations of the inverse problem in body surface potential mapping. IEEE Trans. Biomed. Eng., 1983.30: 749-
754.
References Blorn, S., Flink, R., Hetta, 1., Hilton-Brown, P., Hoffstedt, c, Osterman, P.O. and Spannare, B. Interictal and ictal activity recorded with subdural electrodes during preoperative evaluation for surgical treatment of epilepsy. J. Epilepsy, 1989, 2: 9-
20. Cohen, D., Cuffin, B.N., Yunokuchi, K., Maniewski, R., Purcell, C., Cosgrove, G.R., Ives, J., Kennedy, 1.G. and Schomer, D.L. MEG versus EEG localization test using implanted sources in the human brain. Ann. Neurol., 1990,28: 811-817. Cuffin, B.N. A comparison of moving dipole inverse solutions using EEGs and MEGs. IEEE. Trans. Biomed. Eng.. 1985.32: 905-
910. Cuffin, B.N .• Cohen, D., Yunokuchi, K., Maniewski, R., Purcell, C; Cosgrove, G.R., Ives, 1., Kennedy, 1. and Schomer, D. Tests of
Okamoto, Y., Hornma, S. and Miyamoto, K. Estimation of tissue conductivities in a head by means of weak current injection from scalp surface. Jpn. J. Med. Electron. Bioi. Eng.• 1997,
35: 279-287. Scherg, M. Fundamentals of dipole source potential analysis. In: F. Grandori, M. Hoke and G.L. Romani (Eds.), Auditory Evoked Magnetic Fields and Electric Potentials. Advances in Audiology, Vol. 6. Karger, Basel, 1990:40-96. Sidman. R.D .• Baker, Kearfott R., Major, DJ .• Denson, c., Ford, M.R., Smith, D.B., Lee, I. and Kramer. R. Development and application of mathematical techniques for the non-invasive localization of the sources of scalp-recorded electric potentials. In: 1. Eisenfeld, D.S. Levine and M. Willen (Eds.). Biomedical Modeling and Simulation. Elsevier, Amsterdam. 1989: 133-
157. Smith, D.B, Sidman, R.D., Flanigin, H.• Henke, J. and Labiner, D. A reliable method for localizing deep intracranial sources of the EEG. Neurology, 1985,35: 1702-1707.
286 Stefan. H.• Schneider. S.• Feistel, H.• Pawlik. G.. Schuler, P.• Abraham-Fuchs. K.• Schlegel. T.• Neubauer. U. and Huk, W,J. Ictal and interictal activity in partial epilepsy recorded with multichannel magnetoencephalography: correlation of electroencephalography/electrocorticography. magnetic resonance imaging. single photon emission computed tomography and
positron emission tomography findings. Epilepsia, 1993. 33: 874-887. Sutherling, W.W.• Levesque, M.F., Crandall. P.H. and Barth, D.S. Localization of partial epilepsy using magnetic and electric measurements. Epilepsia, 1991, 32(Suppl. 5): 29-40.
275
Chapter 40
Source localization of interictal epileptiform spike potentials estimated with a dipole tracing method using surface and subdural EEG recordings R. Flink a .*, S. Homma", A. Kanamaru", K. Miyamoto" and Y. Okamoto" 'Department of Clinical Neurophysiology, University Hospital, S-75i85 Uppsala (Sweden) bChiba University, Chiba (Japan) "Department of Physiology, Showa University School of Medicine, Tokyo (Japan) dChuo Electronics Co., Tokyo (Japan) 'Department of Electric Engineering, Chiba institute of Technology, Chiba (Japan)
Introduction The paroxysmal depolarization shift of epileptogenic neurons resulting in synchronous discharges in circumscribed neuronal populations can usually be recorded with surface EEG electrodes. The analysis of interictal and ictal EEG activity is, together with seizure semiology and structural and functional neuroradiology, the method of choice in order to locate the epileptic focus in patients with partial epileptic seizures. This is of particular importance in patients with intractable seizures undergoing preoperative evaluation for epilepsy surgery. With the dipole tracing (DT) method (Okamoto et al. 1983; Cuffin 1985; Smith et al. 1985; Meijs et al. 1989),current sources in the brain can be located from EEG recordings using surface electrodes. There are different algorithms to estimate the location of the electric source generator in a 3-dimen-
* Correspondence to: Dr. Roland Flink, Department of Clinical Neurophysiology, University Hospital, S-75l85 Uppsala (Sweden). E-mail: [email protected]
sional spherical model of the head (Cohen et al. 1990; Scherg 1990; Cuffin et al. 1991). We have previously used a realistic 3 shell head model taking into account standard conductivities (Cuffin 1985; Sidman et al. 1989) of the 3 layers, scalp, skull and brain, the SSBIOT method (Homma et al. 1994; 1995). In the present study, the SSBIOT method was used to estimate the location of interictal epileptiform spike activity in two patients undergoing preoperative evaluation for epilepsy surgery. Instead of using the same, standard conductivity values for scalp and skull on both patients, the individual conductivities for each subject were calculated by electrical stimulation of the surface EEG electrodes (Okamoto et al. 1997) and the SSB head model was used with these individually calculated conductivities. Furthermore, the same spike potentials recorded with surface EEG electrodes were simultaneously recorded with intracranial subdural strip electrodes. In the case of the intracranial recordings, the dipole location was estimated with the BlOT method using a single layer head model with the realistic shape of the brain excluding the
276
scalp and the skull. The realistic brain model was constructed from the inner skull bone surface of consecutive CT scans. Since this BlOT method does not have to take into account the conductivities of surrounding tissue, it is plausible to suggest that the estimated location of an electric source generator with the BlOT method would be the most accurate. We compare in the present study the locations of the interictal epileptiform spike activity estimated with the SSBIOT and BlOT methods in two patients.
Material and methods Two patients (KC and IK) with intractable partial complex seizures, who underwent intracranial seizure monitoring with subdural strip electrodes, were investigated. Both patients had epileptic seizures for several years, with typical temporal seizure semiology. There were no structural findings on the MRI scans but the PET scan with fluorodeoxy glucose showed lateralization of hypometabolism to one of the temporal lobes. Surface EEG recordings including sphenoidal electrodes showed interictal spiking from both temporal lobes with a preponderance for the side with hypometabolism. The simultaneous recordings with surface and intracranial electrodes and the electrical surface stimulation were performed one afternoon during the monitoring period where there had been no clinical seizures the previous morning. The patients were informed of the procedure of the dipole tracing method and gave their informed consent. The interictal spike activity was recorded simultaneously from the intracranial subdural strip electrodes and from 21 surface EEG electrodes placed on the scalp according to a modified 10/20 system. The shape of the scalp was measured with a semispherical helmet with 64 probes and 21 of the probes were marked for electrode location. A 3dimensional shape of the scalp could be created from this measurement using the plane through the orbita and the external meatus acusticus as the zero plane and the midpoint between the two external meatus acusticus as the zero point for the
xyz coordinate system. In order to create the 3 shell
realistic head model, CT scans with a thickness of 3 mm were made in the horizontal plane using the same angle as for the helmet. The skull and brain shells were reconstructed with an image scanner from the consecutive CT-scans using the outer skull bone surface as the skull shell and the inner skull bone surface as the brain shell. The brain shell was used as a brain model for the BlOT calculations. In previous studies with the SSBIOT method, the standard conductivities for the 3 shells, scalp, skull and brain of 0.33: 0.0041: 0.33 Slm, respectively, have been used. In the present study the individual conductivities for the outer two layers for each subject were calculated by electrical stimulation. A current square wave pulse (0.1 rnA and 5 ms duration) was applied through a pair of EEG electrodes, 4 different pairs were usually selected. The voltage change during the stimulation was recorded with the remaining surface electrodes and the conductivity of the scalp and skull could be calculated from the recorded signals (Okamoto et al. 1997). The method was tested in our laboratory by stimulating extracranial electrodes and recording with intracranial electrodes. A fixed value of 0.33 Sim was chosen for the conductivity of the brain and the relative conductivities of scalp:skull:brain were decided. The algorithm for calculating the dipole location follows an iterative procedure both for the SSBIOT as well as the BlOT method. A location of an equivalent dipole source is chosen at random and the surface potentials evoked from this source are calculated for the 21 electrodes. The square differences of the recorded and the calculated potentials are calculated and then the dipole is repeatedly moved in order to minimize the sum of the square differences (Homma et al. 1994). When that is obtained, the location of the dipole source is decided. The residual difference between the measured and calculated potentials (the error) is expressed in percent and referred to as the dipolarity. If there is a perfect match, the dipolarity will be 100% and there is no error. We decided from a previous study with intracranial stimulations (Musha and Homma 1990) to use a dipolarity of
277
98% as a criterion for significant dipole location. A dipole location with dipolarity below 98% was considered as not significant.
Results The stimulation procedure was used to calculate the conductivities of the two outer layers (scalp and skull) of the 3 shell head model. The conductivity of the scalp was 0.072 and 0.0047 Sim for the skull of subject KC, 0.60 for scalp and 0.011 Sim for skull for subject IK. The standard value of 0.33 SI m was used for the brain conductivity in both cases. The SSB-DT method was used to calculate location of the current sources of interictal epileptiform spikes recorded with the surface electrodes in both subjects. The individual conductivities, calculated from the stimulation procedure, were used. We averaged several spikes in order to reduce the noise of the background EEG activity (Fig. I). Both subjects showed bilateral temporal spike activity. The same spike potentials recorded with surface electrodes were simultaneously recorded with intracranial subdural strip electrodes. Since these were subdurally implanted thus recording directly from the brain surface, the impedance from scalp and skull could be disregarded. Interictal spike potentials recorded with the intracranial subdural electrodes were averaged (Fig. 3) and the dipole method was used in the single layer model (BI DT) to calculate the source location. A comparison was made between source location calculated from the surface electrode recording and the intracranial recording for the same spikes (Fig. 7). Source generators of subject KC estimated from surface recordings
temporal lobe (Fig. 2) corresponding to the cortical area of the inferior gyrus on the MRI scan. The current dipole of the negative peak preceding the positive peak was also calculated to have the same location but with an opposite vector moment direction. It was concluded that the negative and the positive peaks are generated from the same source in the right temporal lobe. Six interictal spikes of the L type were averaged from the surface EEG (Fig. I) and the estimated dipole location of the negative peak of the spike was found to be in the left temporal lobe corresponding to the cortex of the inferior temporal gyrus (Fig. 2). The dipolarity was found to be 99.9%. Eight interictal spikes of the H type were averaged and the location of the negative peak was estimated at the midline. Since that location would be unlikely we continued the calculations using the two-dipole algorithm (Homma et al. 1994). We postulated that the calculated dipole would be the summation of two simultaneous generators. With the two-dipole estimation, two simultaneous generator sources were found bilaterally in the temporal lobes in the right and left hippocampus as shown in Fig. 2 with a dipolarity of 99.9%. Source generators of subject KC estimated from subdural recordings
The location of the current sources of the interictal spikes recorded with subdural electrodes were estimated with the B/DT method. The location of the intracranial subdural strip electrodes is illustrated in the lower frame of Fig. 2. The influence of the impedance of the scalp and skull could be excluded and the brain could be regarded as an uniform conductor using the conductivity of 0.33 S/m.
Three different types of interictal epileptiform spikes could visually be detected from the surface EEG recordings, the R, Land H type (Fig. 1). Three interictal spikes of the R type were averaged in order to reduce the background noise. The dipole location of the upward positive peak was estimated with the SSB/DT method. The dipolarity was 99.8% and the location found to be in the right
The R and the L type spikes could be identified from the subdural recording, but not the H type spikes (Fig. 1). Nine interictal spikes of the R type were averaged (Fig. 3) and the dipole estimation with the B/DT method gave a dipolarity of 98.8% and a location in the right temporal lobe in the inferior gyrus overlapping the location calculated from the R type spike of the scalp EEG
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recording (Figs. 2 and 7). Ten interictal spikes of the L type were averaged in the same way (Fig. 3) and the dipole location was estimated to the left
temporal lobe in the inferior gyrus with a dipolarity of 98.6%. The location corresponded to the location calculated from the L type spikes of the scalp EEG
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Fig. 2. The dipole locations of the source generators of subject KC. The upper figures show the dipole locations of R, Land H spikes (filled circles), estimated with the SSBIDT method from surface EEG recordings. Notice that the source for the H type spike is found bilaterally. The lower figures show the dipole locations of the R and L spikes (unfilled circles), estimated with the BIDT method from EEG recordings with subdural electrodes. The location of the surface EEG electrodes is indicated with crosses in the upper figures and the location of the subdural electrodes in the lower figures (subdural electrodes left side (A-C); right side (D-F». R, right; L, left.
(Figs. 2 and Fig. 7). On the other hand, the H type spikes of the scalp EEG were not recorded with subdural electrodes in the case of subject KC (see Discussion). Thus, as seen in Fig. 7, the discrepancy between the dipole locations calculated with the SSBIDT and the BIDT methods was less than 5 mm both for the R and the L type spikes. Source generators of subject IK estimated from surface recordings
In the case of IK, 3 different interictal spikes, type R, H and L, could be detected from the surface EEG recording (Fig. 4). Five spikes of the R type, 4
spikes of the H type and 5 spikes of the L type were averaged and the dipole locations of the different spikes were estimated with the SSBIDT method. The respective dipolarities were 98.6, 98.5 and 97.6%. The dipolarity of the L type did not fully meet the significant dipolarity value of 98%, but was so close that we accepted the SSBIDT estimation. The locations of the different spikes are shown in the upper frame of Fig. 5. The source generator of the R type spikes was located in the right temporal lobe corresponding to the superior temporal gyrus, that of the H type in the left hippocampus and that of the L type in the left temporal lobe corresponding to the superior temporal gyrus.
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We did not use the two-dipole algorithm in this case since there were no midline location of dipoles.
Source generators of subject IK estimated from subdural recordings
The same 3 types of interictal spikes, R, Hand L could also be detected from the intracranial recording with subdural strip electrodes. Eleven spikes of the R type, 4 spikes of the H type and 6 spikes of the L type were collected to be averaged (Fig. 6). The dipole locations for the different types of spikes were estimated with the BIDT method. The different dipolarities were calculated as 98.4, 98.9 and 99.3%, respectively, for R, Hand L type spikes. The location and vector moments are shown in Fig. 5. The source generators were located in the superior temporal gyrus of the right temporal lobe, the hippocampus and the superior temporal gyrus of the left temporal lobe and completely overlapped the locations calculated from the surface EEG recordings with the SSBIDT method (Figs. 5 and 7). The discrepancy between the locations calculated with SSBIDT and BIDT methods were in all cases less than 5 mm. The results from the two subjects (KC and IK) are summarized in Fig. 7. There is almost a complete overlap between dipole location estimated from surface EEG recordings using the SSBIDT method in combination with individual measurement of the conductivity of the scalp and skull and the dipole location estimated from the subdural intracranial EEG recordings using the B/ DT method. The discrepancy between the two methods in dipole location is less than 5 mm. Also the vector moments obtained by the SSBIDT and the B/DT methods are orientated in the same direction. If the intracranial recording is accepted as the golden standard for locating interictal and ictal spike activity, we conclude that the SSBIDT method in combination with individual measurement of the conductivity of the scalp and skull can determine the current dipole location with the same precision as the intracranial recording. On the other hand, the intracranial electrodes, as in the case of subject KC, may not record potentials of source generators far from the electrodes as can be recorded with surface EEG electrodes (see Discussion). The SSBIDT method, however, can estimate dipole location from surface EEG-recordings with
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the same precision as the BlOT method using intracranial recordings, thus making the SSBIOT method a most useful tool to calculate the dipole location of source generators in the human brain.
Discussion The difference in conductivities for scalp and skull between the two subjects can be explained
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Fig. 5. Source generators of the averaged spike types, R, Land H, of subject IK, estimated from surface EEG recordings (filled circles, upper row) and from subdural recordings (unfilled circles, lower row). The location of the surface EEG electrodes is indicated with crosses in the upper row and the location of the subdural electrodes in the lower row. R, right; L, left.
by the scalp conditions, body temperature, sweating as well as the difference in skull bone thickness. The thickness of the skull bone in IK was thinner than that of KC serving as one explanation for the larger conductivity in IK. Differences in the conductivities for scalp and skull will affect the estimation of the calculated dipole location. This underlines the importance of taking the conductivities into consideration when making the dipole analysis. In a previous study (Homma et al. 1994) using the SSBIOT method with fixed relative conductivities for scalp, skull and brain (l: 1/ 80:1), the averaged dislocation was found to be 8.5 mm when comparing calculated dipole location with location of stimulated, intracranially located subdural electrodes. In this study the dislocation between dipole location calculated from intracranial subdural strip electrodes and extracranial surface EEG electrodes was less than 5 mm.
Although the vector moments for the different sources showed the same orientation when calculated from surface and intracranial recordings there is still not a complete overlap with respect to location. There may be several reasons to explain that residual error. At present we have concluded that the dipole location determined by the BlOT method represents the real foci of the source generator. However, the subdural electrodes attached to the cortical surface will only record potentials from source generators close to the electrode (Blom et al. 1989), since the lead field for the source generator is localized to only a small area. In the case of subject KC, the H type spikes recorded from the scalp EEG, were not recorded from the subdural electrodes probably because the subdural strips were not inserted deeply enough. In the case of subject IK, the tip of the subdural strips were more medially inserted, thus recording potentials
283
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1s Fig. 6, Interictal epileptiform spikes of subject IK recorded with 16 subdural electrodes, The R, L and H type spikes were identified from the subdural recording. Eleven spikes of the R type, 4 spikes of the H type and 6 spikes of the L type were averaged, respectively. The averaged spike potentials are shown in the respective right columns.
of deep generator sources as in the hippocampus (compare location of subdural strip electrodes seen in the lower frame of Figs, 2 and 5). In other
words, the subdural electrodes might on some occasions be to selective. Even though we have tried to calculate the individual conductivities of the 3
284
KC
Fig. 7. Source generators of subjects KC and IK estimated with the SSB/DT method from EEG recordings with surface electrodes and with the BlOT method from EEG recordings with subdural electrodes, respectively. The dipole locations calculated from surface recordings are shown with filled circles (the direction of the vector moment of the current is also indicated) and the dipole locations from subdural recordings are shown with unfilled circles. The two methods showed very similar results and the discrepancy between the dipole locations when comparing the same type of spikes calculated with SSBIOT method and BlOT method was less than 5 mm. R, right; L, left.
shells in the realistic head model, the inhomogeneity of the skull bone must be considered, especially since these calculations were performed in patients with intracranial subdural electrodes which are introduced through burr holes in the skull bone. There are topographical differences in the skull bone conductivity such as various bone openings in the skull base and the air-containing mastoid cells in the temporal bone, which will affect the dipole location and it remains to be seen whether these differences can be taken into account in the calculations. Several authors have pointed out the clinical use of dipole analysis from surface EEG in patients
with focal epilepsy (Homma et aI. 1990; Ebersole 1991; Sutherling et aI. 1991; Stefan et aI. 1993; Flink et aI. 1996; Lantz et al., 1997). In epilepsy groups working with preoperative evaluation of patients with intractable epilepsy, there have been studies comparing intracranial EEG recordings with dipole analysis with surface EEG electrodes as well as comparisons between dipole location and structural (MRI) and functional (PET, SPECT) neuroimaging (Lantz et al. 1994; 1996; Flink et al. 1996) showing a good correlation between dipole results and the other localizing methods. Both of the patients investigated in this study
285
appeared to have bilateral interictal spiking which could be concluded from the dipole analysis showing source generators in both temporal lobes. The bilateral foci were obvious in the subdural recordings but at least in one case (KC) not obvious when visually analyzing the surface EEG recordings. The bilateral temporal epileptogenicity was furthermore confirmed by intracranial seizure monitoring. Since the bilateral temporal dysfunction increases the risk of postoperative memory problems, none of the two patients have been operated on even though the PET scans showed lateralizing signs of hypometabolism. Further studies will show whether the SSB/DT method with individual conductivities will be useful also for extra-temporal epileptic foci. However, by introducing individual conductivities into the calculations, the dislocation of the estimated dipole location has decreased, thus increasing the value of the method for clinical use.
Acknowledgements The authors acknowledge the help from professors K.-E. Hagbarth and I. Homma. We also would like to thank Chuo Electronic Company for providing the equipment used in the study. The study was supported by grants from the Swedish Medical Research Council, project no. K98-14X09482-08C, and the Margaretha Hemmet Foundation.
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