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ARTICLE IN PRESS+ModelEPIRES-4153; No. of Pages 8

Epilepsy Research (2009) xxx, xxx—xxx

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Dynamic statistical parametric mapping for analyzingictal magnetoencephalographic spikes in patientswith intractable frontal lobe epilepsy

Naoaki Tanakaa,∗, Andrew J. Coleb, Deidre von Pechmanna,Daniel G. Wakemana, Matti S. Hämäläinena, Hesheng Liua,Joseph R. Madsenc, Blaise F. Bourgeoisd, Steven M. Stufflebeama

a Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA, USAb Department of Neurology, Massachusetts General Hospital, Boston, MA, USAc Department of Neurosurgery, Children’s Hospital Boston, Boston, MA, USAd Department of Neurology, Children’s Hospital Boston, Boston, MA, USA

Received 16 September 2008; received in revised form 28 January 2009; accepted 27 March 2009

KEYWORDSMagnetoencephalog-raphy;Epilepsy;Dynamic statisticalparametric mapping;

Summary The purpose of this study is to assess the clinical value of spatiotemporal sourceanalysis for analyzing ictal magnetoencephalography (MEG). Ictal MEG and simultaneous scalpEEG was recorded in five patients with medically intractable frontal lobe epilepsy. Dynamicstatistical parametric maps (dSPMs) were calculated at the peak of early ictal spikes for thepurpose of estimating the spatiotemporal cortical source distribution. DSPM solutions weremapped onto a cortical surface, which was derived from each patient’s MRI. Equivalent current

Ictal dipoles (ECDs) were calculated using a single-dipole model for comparison with dSPMs. In allpatients, dSPMs tended to have a localized activation, consistent with the clinically determinedictal onset zone, whereas most ECDs were considered to be inappropriate sources accordingto their goodness-of-fit values. Analyzing ictal MEG spikes by using dSPMs may provide useful

valuts re

information in presurgical e© 2009 Elsevier B.V. All righ

Please cite this article in press as: Tanaka, N., et al.,ing ictal magnetoencephalographic spikes in patients withdoi:10.1016/j.eplepsyres.2009.03.023

∗ Corresponding author at: Athinoula A. Martinos Centerfor Biomedical Imaging, 149 Thirteenth Street, Suite 2301,Charlestown, MA 02129, USA. Tel.: +1 617 726 8517;fax: +1 617 726 8626.

E-mail address: [email protected] (N. Tanaka).

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0920-1211/$ — see front matter © 2009 Elsevier B.V. All rights reserved.doi:10.1016/j.eplepsyres.2009.03.023

ation of epilepsy.served.

ntroduction

nvestigating ictal onset zones is essentially important forharacterizing epileptic seizures, which show various clin-

Dynamic statistical parametric mapping for analyz-intractable frontal lobe epilepsy. Epilepsy Res. (2009),

cal symptoms. In presurgical evaluation of epilepsy, ictalnset zones are believed to be highly correlated with thepileptogenic zone (Lüders and Awad, 1991). The most pre-ise localization of the ictal onset zone is traditionallybtained by invasive intracranial EEG recording (Rosenow

dx.doi.org/10.1016/j.eplepsyres.2009.03.023

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ARTICLE+ModelPIRES-4153; No. of Pages 8

nd Lüders, 2001), however, non-invasive methods also mayrovide the localization in addition to or in lieu of intracra-ial EEG.

Magnetoencephalography (MEG) is a non-invasive methodf recording magnetic fields emanating from the brain. Itas been mainly used for source localization of interictalpileptic activities, whereas there are several studies of suc-essful source localization of ictal MEG with a single-dipoleodel (Sutherling et al., 1987; Stefan et al., 1992; Eliashiv

t al., 2002; Tilz et al., 2002; Assaf et al., 2003). However,ctal MEG occasionally failed to localize the ictal onset zoneEliashiv et al., 2002; Tilz et al., 2002). Major possible expla-ations of this failure are considered (1) the early spikes ofn ictal MEG may have low signal-to-noise ratio, loweringhe localization precision, (2) source localization using theingle-dipole modeling may be misleading (Kobayashi et al.,005), by assuming that a single source can explain all theagnetic fields from the brain.Dynamic statistical parametric maps (dSPMs) have

ecently been introduced for evoked MEG analysis (Dale etl., 2000). DSPM provides spatiotemporal source distributionith millisecond temporal resolution by imposing anatom-

cal information about the cortical surface derived fromagnetic resonance images (MRI) and noise normalization

f the minimum norm estimate. Clinical studies of dSPM inatients with partial epilepsy suggest that it has advantagesver a single-dipole model in analyzing interictal MEG spikesShiraishi et al., 2005a,b).

The purpose of the present study was to assess theossible localizing value of using dSPM-derived spatiotem-oral maps in the evaluation of ictal MEG in patients withntractable frontal lobe epilepsy.

atients and methods

atients

e retrospectively reviewed the MEG data from five patientsith medically intractable frontal lobe epilepsy, who hadlinical seizures during MEG recording. All patients under-ent evaluation of their epilepsy, including medical history,

ong-term video-scalp EEG monitoring and structural MRIt Massachusetts General Hospital or Children’s Hospitaloston. The ictal onset zone of each patient was determinedlinically by considering the results of the evaluation prior tobtaining the MEG. Written informed consent was obtainedefore each data acquisition for the MEG research, whichas approved by the institutional review board.

ata acquisition

EG recordings were performed at Athinoula A. Martinosenter for Biomedical Imaging between 2005 and 2007. Theetails of simultaneous MEG and EEG recording have previ-usly been described (Knake et al., 2006). MEG was recordedith a 306-channel (204 planar gradiometers and 102 mag-


etometers), whole-head MEG system (Elekta-Neuromag,elsinki, Finland) in a magnetically shielded chamber. ScalpEG was simultaneously recorded with a non-magnetic 70-hannel electrode cap, based on the 10-10 system. Theatients were recorded in supine position with a sampling

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ate of 600 Hz. Data were digitally filtered at a bandpassidth 0.5—40 Hz in off-line data analysis. In all patients,igh-resolution 3T MRI MPRAGE pulse sequences (TE 3.37 ms,R 2000 ms, voxel size 1 mm × 1 mm × 1 mm) were acquiredith a high-resolution 3T MRI scanner (TIM TRIO, SiemensG, Erlangen, Germany).

ata analysis

EG data were visually examined, and segments contain-ng epileptic discharges were selected from the early partf ictal MEG. For dSPM, an anatomically constrained lin-ar estimation approach was applied, assuming the sourcesre distributed in the cerebral cortex (Dale and Sereno,993). The forward solution, which models the signal pat-ern generated by a unit dipole at each location on theortical surface, was calculated by using a linear colloca-ion single-layer boundary-element method (BEM) with thenner skull boundary approach, for each patient (Hamäläinennd Sarvas, 1989; Oostendorp and Van Oosterom, 1989). Theurface was tessellated with 5120 triangles, providing ade-uate numerical accuracy (Crouzeix et al., 1999; Fuchs etl., 2001; Tarkiainen et al., 2003; de Jongh et al., 2005). Thectivation at each cortical location was estimated by usingnoise-normalized minimum norm estimate (Dale et al.,

000; Liu et al., 2002), which results in an F-distributed esti-ate of the cortical current (Dale et al., 2000). Thus, dSPM

dentifies the locations of statistically increased current-ipolar strength relative to the noise level. The dSPM mapsalculated for the peak of each spike were superimposedn inflated geometrical representations of cortical surfaces,hich were reconstructed from the individual patients’ MRI

Dale et al., 1999; Fischl et al., 1999, 2001).Equivalent current dipoles (ECDs) were also calculated at

he peak of each spike using a single-dipole model withoutelecting a region of interest (i.e., all of the 306 sensorsere used for the analysis). We estimated the numbers and

ocations of ECDs with a goodness of fit (GOF) better than0%, 70% and 80%, separately.

In three patients we also analyzed interictal MEG spikesith both dSPM and single-dipole modeling. The ECDs withOF > 70% were considered adequate as possible corticalources.

esults

verall results

able 1 gives an overview of the clinical profiles of allatients. Four male and one female patients, 14—31 yearsld (mean age: 19.2 years) were studied. All clinical seizuresccurred spontaneously during MEG recording, showing clin-cal symptoms consistent with the habitual seizures of eachatient.

The seizures of Patient 2 were characterized by fre-uent facial twitching of the left side. Ictal EEG started with


hythmic spikes or spike-and-slow-wave complexes (sp-w-c)n the right frontal area, spreading bilaterally in the lat-er part. MRI showed an atrophy of the right frontal andemporal lobes. Ictal onset zone was suggested to be inhe right frontal lobe, based on semiology, ictal scalp EEG,



Dynamic statistical parametric mapping 3

Table 1 Clinical data of the patients.

Patient Age at seizureonset/MEG

Sex Seizure type Scalp EEG(interictal/ictal)

MRI Clinicallydetermined ictalonset zone

1 5/15 M CPS withunresponsiveness,sometimes accompaniedby right hemi-convulsion

LF, RF/LF Multiplesubcortical lesionsin LF lobe

LF lobe

2 13/14 M EPC with left facialtwitching

NA/RF Atrophy of RF, RTlobes, insula

RF lobe

3 8/15 M CPS with head and eyedeviation (left or right)

LF, RF/LF, RF Normal LF and/or RFlobe(s)

4 2/31 M Nocturnal CPS withabrupt arousal andnon-patterned limbmovements

NA/LF, RF Normal LF and/or RFlobe(s)

5 12/21 F Nocturnal CPS withabrupt arousal andrandom body movement

LF, RF/RF RF corticaldysplasia

RF lobe

: lef

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(tIEwere larger with the threshold of GOF > 70% and 60%. The

CPS: complex partial seizure, EPC: epilepsia partialis continua, LF

and MRI. The patient underwent a hemispherectomy of theright side, and has been seizure-free for 6 months post-surgery. Patient 3 showed two types of seizures. They wereaccompanied by head and eye deviation to the left or right,and ictal EEG showed rhythmic sp-w-c bursts dominantly inthe right or left frontal area, respectively. Interictal EEGshowed frequent sp-w-c in the left and the right frontalarea. These seizures were considered to start from the leftor right frontal lobe, corresponding to the two types ofseizures. The seizure occurred during MEG recording wasconsistent with the former type, which was considered toarise from the right frontal lobe. The seizures of Patient 4were accompanied by hypermotor movements of the body,typically seen during sleep. Ictal EEG showed mainly move-ment artifacts, preceded by small spikes in the bilateralfrontal area. The semiology and ictal EEG were consistentwith those of frontal lobe epilepsy. The seizure localiza-


tion of Patient 1 and 5 are described below as illustrativecases.

Table 2 summarizes the results of MEG analyses. In eachpatient, 4—11 early ictal spikes were obtained. All dSPMs

low3

Table 2 Results of ictal MEG analyses by using dSPMs and single-

Patient Interictal (ECDdistribution)

Interictal (dSPMactivation area)

No. of earlyictal spikes

Ic

G

1 LF, RF LF, BF 7 22 N/A N/A 7 43 LF, RF RF, BF 6 14 N/A N/A 4 25 LF, RF RF, BF 11 4

RF: right frontal lobe, LF: left frontal lobe, BF: bilateral frontal lobeslobe, and N/A: not available.

t frontal, RF: right frontal, and NA: not available.

ocalized activity consistent with the clinically determinedctal onset zone at a lobar level in four patients (Patient 1, 3,and 5). In one patient (Patient 2), all dSPMs showed a local-

zed activation at the same location as the ictal onset zone,ith the exception of one dSPM showing larger activationreas.

In three patients (Patient 1, 3 and 5), dSPMs obtainedrom interictal spikes showed widespread activation in uni-ateral or bilateral frontal lobe(s). These activation areasere larger than the activation in ictal dSPMs of eachatient.

One ECD with GOF > 80% were obtained in three patientsPatient 2, 4 and 5). Their locations were consistent withhe clinically determined ictal onset zone of each patient.n other two patients (Patient 1 and 3), there were noCDs with GOF better than 80%. The numbers of ECDs


ocations of these ECDs were consistent with the ictalnset zone in one patient (Patient 5), and some ECDsere inconsistent in other four patients (Patient 1, 2,and 4).

dipole model.

tal (no. of ECDs, location) Ictal (no. of dSPMs,activation area)

OF > 60 GOF > 70 GOF > 80

LF, 2 RF 1 LF 0 7 LFRF, 2 LF 3 RF, 2 LF 1 RF 6 RF, 1 BFRF, 2 RP, 1 LF 1 RF, 2 RP 0 6 RFLF, 1 LT 2 LF, 1 LT 1 LF 4 LFRF 3 RF 1 RF 11 RF

, RP: right parietal lobe, LP: left parietal lobe, LT: left temporal


Please cite this article in press as: Tanaka, N., et al., Dynamic statistical parametric mapping for analyz-ing ictal magnetoencephalographic spikes in patients with intractable frontal lobe epilepsy. Epilepsy Res. (2009),doi:10.1016/j.eplepsyres.2009.03.023


4 N. Tanaka et al.

Figure 1 (A) The early part of ictal MEG and EEG in Patient 1. Rhythmic spike-and-slow-wave complexes are seen in the bilateralfrontal areas after the point shown by an arrow. (B) Contour maps of magnetic fields at the peak of the MEG spike shown by *in (A). (C) The dSPM map at the same peak. The map are displayed on the inflated cortical surface, with darker gray indicatingcortex buried in the sulci, and lighter gray indicating gyral cortex. Activation is seen in the left anterior frontal lobe. One ECD withGOF > 70% is obtained from seven ictal spikes (a white dot). (D) A dSPM map at the peak of a typical interictal spike. Activation isseen in a large part of the left frontal lobe and the right frontal lobe. ECDs with GOF > 70% obtained from interictal spikes (whitedots) are distributed in bilateral frontal lobes. Note that the dSPM maps shown here are obtained from a single spike and ECDs arecalculated from each individual spike.


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The distribution of ECDs obtained from interictal spikeswas similar to the activation pattern in interictal dSPMs ineach patient.

Illustrative cases

Patient 1Patient 1 was a 15-year-old male with neurofibromatosistype I. Seizure onset was at age 5. He had daily seizures withunresponsiveness, sometimes accompanied with head dropand hemi-convulsion of the right side. Interictal EEG showedfrequent spike-and-slow-wave complexes which were dom-inant in the left or right frontal areas. Ictal EEG showedrhythmic spike-and-slow-wave complex bursts dominant inthe left frontal area. MRI showed multiple T2 hyperintenseabnormalities especially prominent in the subcortical whitematter of the left frontal lobe, which could affect the cortexadjacent to the lesion. Semiology was consistent with theleft frontal lobe epilepsy. Ictal EEG showed the left frontalonset of seizures, and interictal EEG was also suggestive offrontal lobe epilepsy. MRI suggested the epileptogenic cor-tex in the left frontal lobe. Overall, the ictal onset zone wasconsidered to be in the left frontal lobe.

The ictal MEG showed bilateral frontal spike bursts, whichwere initially predominantly on the left frontal sensors.Simultaneous EEG showed a similar pattern to the previousevaluation (Fig. 1A). Seven MEG spikes in the early part ofthe seizure were analyzed. The contour maps of magneticfields showed a complicated pattern (Fig. 1B). All seven ictaldSPMs demonstrated activation in the left anterior frontallobe (Table 2). A typical ictal dSPM is shown in Fig. 1C. Thenumbers of ECDs obtained with the threshold of GOF > 60%,70% and 80% were four, one, and zero, respectively (Table 2).The ECD with GOF > 70% was located in the left frontal lobe(Fig. 1C), whereas ECDs with GOF > 60% were distributed inthe left and right frontal lobes. The activation pattern ofthe interictal spikes dSPMs nearly always included a largeportion of the left frontal cortex, and sometimes spread tothe right side. ECDs obtained from the interictal spikes weremainly located in the left frontal lobe, but some were dis-tributed in the right side (Table 2). A typical interictal dSPMand ECDs with GOF > 70% are shown in Fig. 1D.

Patient 5Patient 5 was a 21-year-old female with frequent noctur-nal seizures since age 12. Her habitual seizure consistedof hypermotor movements, sometimes accompanied withscreaming. Interictal EEG showed frequent spikes in thebilateral frontal area. In previous evaluation, ictal EEGshowed mainly movement artifacts, sometimes preceded bysmall spikes in the right frontal area. MRI showed a cor-tical dysplasia in the right anterior frontal lobe (Fig. 2E).The semiology of this patient was consistent with frontallobe epilepsy, as well as interictal EEG. Ictal EEG showedthe right frontal onset of seizures. The MRI lesion suggestedthe epileptogenic cortex in the right frontal lobe. Based on


these findings, ictal onset zone was considered to be in theright frontal lobe.

The early ictal EEG and MEG showed small spike burstspredominantly in the right frontal area (Fig. 2A). Elevenspikes were analyzed. The contour maps of magnetic fields

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howed a single-dipole pattern (Fig. 2B). All eleven dSPMshowed activation in the right anterior frontal lobe. Four,hree and one ECD(s) were obtained with the thresholdf GOF > 60%, 70% and 80%, respectively. These ECDs wereocated in the right frontal lobe. A typical ictal dSPM andCDs with GOF > 70% are shown in Fig. 2C. The activationattern of the interictal spikes dSPMs included a large por-ion of the right frontal lobe or bilateral frontal lobes. ECDsbtained from the interictal spikes were located mainly inhe right frontal lobe, but some were seen in the left frontalobe. A typical interictal dSPM and ECDs with GOF > 70% arehown in Fig. 2D.

This patient underwent a resection of the cortical dyspla-ia (Fig. 2E) and has been seizure free for 13 months afterurgery.

iscussion

n the present study, we estimated ictal onset zones in fiveatients with intractable frontal lobe epilepsy by using bothSPMs and a single-dipole model. In all spikes obtained fromhe early ictal discharges, the dSPM localized activity con-istent with the clinically determined ictal onset zone at aobar level, except for one spike in Patient 2. The dSPM acti-ation in this spike showed larger activation areas, includinghe clinically determined ictal onset zone. Moreover, dSPMsad more restricted activation in these ictal spikes thannterictal spikes. It is well known that the irritative zonebtained from the interictal spikes is often larger than thectal onset zone (Lüders and Awad, 1991). DSPM findings ofhis study are in agreement with this phenomenon.

Since the single-dipole analysis always has the differ-nce between measured and forward-calculated magneticelds, many ictal MEG studies have applied a thresholdf GOF values for selecting ECDs as appropriate sourcesOishi et al., 2002; Tanaka et al., 2004; Yoshinaga et al.,004; Tanaka et al., 2005). The threshold has been sett 80—90% in these studies. This is a form of appropriateias for increasing the likelihood of single-dipole analysis,hen many ECDs are available after eliminating ECDs withlow GOF value. Several MEG studies have selected the

hannels of MEG to be used in the single-dipole analysisor obtaining better GOF values (Bast et al., 2004). Thiss another bias which may be useful only when the selec-ion is adequate for representing the epileptic activity. Inhis study, we used all the MEG channels for single-dipolenalysis. The number of ECDs decreased as the thresh-ld of goodness-of-fit (GOF) values increased. No ECDs ornly one ECD with the threshold of GOF > 80% in each case.he locations of some ECDs obtained with the thresholdsf GOF > 60% and 70% were inconsistent with the clinicallyetermined ictal onset zones. These results may suggesthe usefulness of ECDs may be limited in the evaluation ofhese ictal MEG spikes. Theoretically, dSPMs can representll the magnetic fields by applying a source distributionodel, assuming that the sources are distributed in the large


atch of cortex (Dale and Sereno, 1993; Dale et al., 2000).herefore, thresholds such as GOF values are considerednnecessary for dSPM analysis. On the other hand, deter-ination of the appropriate amount of activated cortex is

n important issue in distributed source models including


Please cite this article in press as: Tanaka, N., et al., Dynamic statistical parametric mapping for analyz-ing ictal magnetoencephalographic spikes in patients with intractable frontal lobe epilepsy. Epilepsy Res. (2009),doi:10.1016/j.eplepsyres.2009.03.023


6 N. Tanaka et al.

Figure 2 (A) The early part of ictal MEG and EEG in Patient 5. Small spike bursts are seen predominantly in the right frontal area.(B) Contour maps of magnetic fields at the peak of the MEG spike shown by * in (A). (C-upper) The dSPM map at the same peak.Activation in dSPM is seen in the right anterior frontal lobe. Three ECDs with GOF > 70% are obtained from 11 ictal spikes (whitedots). (D) A dSPM map at the peak of a typical interictal spike. Activation is seen in a relatively a large part of the right frontallobe. ECDs with GOF > 70% obtained from interictal spikes are distributed in the bilateral frontal lobes. Note that the dSPM mapsshown here are obtained from a single spike and ECDs are calculated from each individual spike. (E-left) Presurgical FLAIR MRI.The abnormal signals in the right anterior frontal lobe suggest a cortical dysplasia. (E-right) Postsurgical FLAIR MRI. The lesion wasremoved by a surgical resection.


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dSPM. In dSPM, this issue is highly dependent on F values forstatistical mapping. Smaller F values would show a largerarea of activation, and larger F values would show no activa-tion. In any case, the inverse solution used for making dSPMsexplains all magnetic fields. We applied F values for repre-senting the strongest activation, based on the assumptionthat epileptic activities are larger than other backgroundactivities. In addition, the activation areas were consis-tent at a lobar level under several different F values in allpatients. Further study will be needed for investigating theaccuracy of dSPM at a sublobar level by comparing dSPMsand the spike involvement on intracranial EEG.

Source localization of ictal discharges becomes difficultafter seizure activity propagates (Tanaka et al., 2004), thusearly ictal spikes may be more accurate for estimating theseizure onset zone (Tilz et al., 2002; Assaf et al., 2003).However, the low signal-to-noise ratio in the early spikesmay complicate obtaining appropriate sources using single-dipole modeling. This may explain the low GOF values andwidespread distribution of ECDs in the present study. Incontrast, dSPMs showed a localized activation which wasreproducible between the different ictal spikes, suggestingthat they may be useful for analyzing these spikes with thelow signal-to-noise ratio.

The small number of patients and the lack of a confidentictal onset zone determined by intracranial EEG may causea limitation to the results of this study. However, we con-sider this study is still valuable for improving MEG analysissince this is the first report in which dSPMs are applied foranalyzing ictal data. Two patients underwent surgery with afavorable outcome, removing the area of cortex which wasconsistent with the results of dSPMs. Further investigationin a larger patient group with intracranial EEG will providean improvement on these issues.

Overall, the results of our patients suggested that dSPMprovided superior source localization of early ictal spikescompared to single-dipole source analysis. By using dSPM,ictal MEG may be more informative than the single-dipoleanalysis alone in presurgical evaluation of epilepsy.

Acknowledgements

This work was supported by National Institutes of Health(P41RR14075, RO1NS037462-07), Mental Illness and Neu-roscience Discovery Institute, NARSAD Young InvestigatorsAward and Japan Epilepsy Research Foundation.

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dynamic statistical parametric mapping for analyzing ictal … · 2016. 12. 29. · and sarvas,...

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