Preoperative multimodal motor mapping: a comparison of magnetoencephalography imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation

Clinical article

Restricted access

Object

Direct cortical stimulation (DCS) is the gold-standard technique for motor mapping during craniotomy. However, preoperative noninvasive motor mapping is becoming increasingly accurate. Two such noninvasive modalities are navigated transcranial magnetic stimulation (TMS) and magnetoencephalography (MEG) imaging. While MEG imaging has already been extensively validated as an accurate modality of noninvasive motor mapping, TMS is less well studied. In this study, the authors compared the accuracy of TMS to both DCS and MEG imaging.

Methods

Patients with tumors in proximity to primary motor cortex underwent preoperative TMS and MEG imaging for motor mapping. The patients subsequently underwent motor mapping via intraoperative DCS. The loci of maximal response were recorded from each modality and compared. Motor strength was assessed at 3 months postoperatively.

Results

Transcranial magnetic stimulation and MEG imaging were performed on 24 patients. Intraoperative DCS yielded 8 positive motor sites in 5 patients. The median distance ± SEM between TMS and DCS motor sites was 2.13 ± 0.29 mm, and between TMS and MEG imaging motor sites was 4.71 ± 1.08 mm. In no patients did DCS motor mapping reveal a motor site that was unrecognized by TMS. Three of 24 patients developed new, early neurological deficit in the form of upper-extremity paresis. At the 3-month follow-up evaluation, 2 of these patients were significantly improved, experiencing difficulty only with fine motor tasks; the remaining patient had improvement to 4/5 strength. There were no deaths over the course of the study.

Conclusions

Maps of the motor system generated with TMS correlate well with those generated by both MEG imaging and DCS. Negative TMS mapping also correlates with negative DCS mapping. Navigated TMS is an accurate modality for noninvasively generating preoperative motor maps.

Abbreviations used in this paper:DCS = direct cortical stimulation; ERD = event-related desynchronization; MEG = magnetoencephalography; MEP = motor evoked potential; TMS = transcranial magnetic stimulation.

Article Information

Address correspondence to: Sri Nagarajan, Ph.D., Department of Radiology, University of California at San Francisco, 513 Parnassus Avenue, S362, San Francisco, California 94143. email: srikantan.nagarajan@ucsf.edu.

Please include this information when citing this paper: published online June 15, 2012; DOI: 10.3171/2012.5.JNS112124.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Axial MR images showing synthetic aperture magnetometry analysis of MEG imaging data in 1 patient, localizing the motor site for the index finger (blue areas).

  • View in gallery

    Images obtained in a patient with a tumor in the somatosensory cortex. Left: Transcranial magnetic stimulation map; no positive motor sites were identified. Right: Intraoperative photograph; numbered squares indicate sensory sites identified with DCS.

  • View in gallery

    Example of a multimodal motor map showing MEG imaging (purple sphere), TMS (orange pins), and DCS (orange spheres) sites overlaid. ADQ = abductor digiti quinti; APB = abductor pollicis brevis; O. oris = orbicularis oris.

  • View in gallery

    Example of a bimodal motor map with MEG imaging (purple sphere) and TMS (orange pins) sites overlaid. This patient had a negative motor map using DCS.

  • View in gallery

    Scatterplot of distances from MEG imaging of the index finger motor site to TMS of the abductor digiti quinti and abductor pollicis brevis motor sites. The labeled horizontal bar in each series represents the median distance.

  • View in gallery

    Bar graph showing the median distance from TMS motor sites (aggregated abductor digiti quinti and abductor pollicis brevis data) to corresponding DCS motor sites and to MEG imaging index finger motor sites (error bar = 95% CI).

  • View in gallery

    Bar graph showing the median distance from interpolated TMS motor sites (midpoint of abductor digiti quinti and abductor pollicis brevis muscles) to corresponding DCS motor sites and to MEG imaging index finger motor sites (error bar = 95% CI).

  • View in gallery

    Scatterplot of distances from TMS motor sites to corresponding DCS motor sites and to MEG imaging index finger motor sites.

References

1

Babiloni CCarducci FCincotti FRossini PMNeuper CPfurtscheller G: Human movement-related potentials vs desynchronization of EEG alpha rhythm: a high-resolution EEG study. Neuroimage 10:6586651999

2

Beisteiner RWindischberger CLanzenberger REdward VCunnington RErdler M: Finger somatotopy in human motor cortex. Neuroimage 13:101610262001

3

Berger MSOjemann GA: Intraoperative brain mapping techniques in neuro-oncology. Stereotact Funct Neurosurg 58:1531611992

4

Berger MSOjemann GALettich E: Neurophysiological monitoring during astrocytoma surgery. Neurosurg Clin N Am 1:65801990

5

Carrabba GFava EGiussani CAcerbi FPortaluri FSonga V: Cortical and subcortical motor mapping in rolandic and perirolandic glioma surgery: impact on postoperative morbidity and extent of resection. J Neurosurg Sci 51:45512007

6

Crone NEMiglioretti DLGordon BLesser RP: Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain 121:Pt 12230123151998

7

Crone NEMiglioretti DLGordon BSieracki JMWilson MTUematsu S: Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. Brain 121:Pt 12227122991998

8

Dalal SSZumer JMAgrawal VHild KESekihara KNagarajan SS: NUTMEG: a neuromagnetic source reconstruction toolbox. Neurol Clin Neurophysiol 52:20042004

9

Dechent PFrahm J: Functional somatotopy of finger representations in human primary motor cortex. Hum Brain Mapp 18:2722832003

10

Duffau HCapelle LSichez JFaillot TAbdennour LLaw Koune JD: Intra-operative direct electrical stimulations of the central nervous system: the Salpêtrière experience with 60 patients. Acta Neurochir (Wien) 141:115711671999

11

Haglund MMBerger MSShamseldin MLettich EOjemann GA: Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery 34:5675761994

12

Hannula HYlioja SPertovaara AKorvenoja ARuohonen JIlmoniemi RJ: Somatotopic blocking of sensation with navigated transcranial magnetic stimulation of the primary somatosensory cortex. Hum Brain Mapp 26:1001092005

13

Hill DLMaurer CR JrMaciunas RJBarwise JAFitzpatrick JMWang MY: Measurement of intraoperative brain surface deformation under a craniotomy. Neurosurgery 43:5145281998

14

Inoue TShimizu HNakasato NKumabe TYoshimoto T: Accuracy and limitation of functional magnetic resonance imaging for identification of the central sulcus: comparison with magnetoencephalography in patients with brain tumors. Neuroimage 10:7387481999

15

Julkunen PSäisänen LDanner NNiskanen EHukkanen TMervaala E: Comparison of navigated and non-navigated transcranial magnetic stimulation for motor cortex mapping, motor threshold and motor evoked potentials. Neuroimage 44:7907952009

16

Keles GELundin DALamborn KRChang EFOjemann GBerger MS: Intraoperative subcortical stimulation mapping for hemispherical perirolandic gliomas located within or adjacent to the descending motor pathways: evaluation of morbidity and assessment of functional outcome in 294 patients. J Neurosurg 100:3693752004

17

Krings TChiappa KHFoltys HReinges MHCosgrove GRThron A: Introducing navigated transcranial magnetic stimulation as a refined brain mapping methodology. Neurosurg Rev 24:1711792001

18

Krings TFoltys HReinges MHKemeny SRohde VSpetzger U: Navigated transcranial magnetic stimulation for presurgical planning—correlation with functional MRI. Minim Invasive Neurosurg 44:2342392001

19

Lin PTBerger MSNagarajan SS: Motor field sensitivity for preoperative localization of motor cortex. J Neurosurg 105:5885942006

20

McKiernan BJMarcario JKKarrer JHCheney PD: Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit, and intrinsic hand muscles during a reach and prehension task. J Neurophysiol 80:196119801998

21

Nagarajan SKirsch HLin PFindlay AHonma SBerger MS: Preoperative localization of hand motor cortex by adaptive spatial filtering of magnetoencephalography data. J Neurosurg 109:2282372008

22

Pang EWDrake JMOtsubo HMartineau AStrantzas SCheyne D: Intraoperative confirmation of hand motor area identified preoperatively by magnetoencephalography. Pediatr Neurosurg 44:3133172008

23

Pfurtscheller G: Functional brain imaging based on ERD/ERS. Vision Res 41:125712602001

24

Pfurtscheller G: Functional topography during sensorimotor activation studied with event-related desynchronization mapping. J Clin Neurophysiol 6:75841989

25

Pfurtscheller G: Mapping of event-related desynchronization and type of derivation. Electroencephalogr Clin Neurophysiol 70:1901931988

26

Pfurtscheller G: Spatiotemporal analysis of alpha frequency components with the ERD technique. Brain Topogr 2:381989

27

Pfurtscheller GBerghold A: Patterns of cortical activation during planning of voluntary movement. Electroencephalogr Clin Neurophysiol 72:2502581989

28

Pfurtscheller GLopes da Silva FH: Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110:184218571999

29

Pfurtscheller GNeuper CBerger J: Source localization using event-related desynchronization (ERD) within the alpha band. Brain Topogr 6:2692751994

30

Pfurtscheller GPregenzer MNeuper C: Visualization of sensorimotor areas involved in preparation for hand movement based on classification of mu and central beta rhythms in single EEG trials in man. Neurosci Lett 181:43461994

31

Picht TMularski SKuehn BVajkoczy PKombos TSuess O: Navigated transcranial magnetic stimulation for preoperative functional diagnostics in brain tumor surgery. Neurosurgery 65:6 Suppl93992009

32

Picht TSchmidt SBrandt SFrey DHannula HNeuvonen T: Preoperative functional mapping for rolandic brain tumor surgery: comparison of navigated transcranial magnetic stimulation to direct cortical stimulation. Neurosurgery 69:5815882011

33

Romstöck JFahlbusch RGanslandt ONimsky CStrauss C: Localisation of the sensorimotor cortex during surgery for brain tumours: feasibility and waveform patterns of somatosensory evoked potentials. J Neurol Neurosurg Psychiatry 72:2212292002

34

Rossini PMBarker ATBerardelli ACaramia MDCaruso GCracco RQ: Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 91:79921994

35

Sanai NBerger MS: Intraoperative stimulation techniques for functional pathway preservation and glioma resection. Neurosurg Focus 28:2E12010

36

Sanai NMirzadeh ZBerger MS: Functional outcome after language mapping for glioma resection. N Engl J Med 358:18272008

37

Sarvas J: Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. Phys Med Biol 32:11221987

38

Schieber MHHibbard LS: How somatotopic is the motor cortex hand area?. Science 261:4894921993

39

Schiffbauer HBerger MSFerrari PFreudenstein DRowley HARoberts TP: Preoperative magnetic source imaging for brain tumor surgery: a quantitative comparison with intraoperative sensory and motor mapping. J Neurosurg 97:133313422002

40

Schiffbauer HBerger MSFerrari PFreudenstein DRowley HARoberts TP: Preoperative magnetic source imaging for brain tumor surgery: a quantitative comparison with intraoperative sensory and motor mapping. Neurosurg Focus 15:1E72003

41

Sekihara KNagarajan SSPoeppel DMarantz A: Asymptotic SNR of scalar and vector minimum-variance beamformers for neuromagnetic source reconstruction. IEEE Trans Biomed Eng 51:172617342004

42

Sekihara KNagarajan SSPoeppel DMarantz AMiyashita Y: Reconstructing spatio-temporal activities of neural sources using an MEG vector beamformer technique. IEEE Trans Biomed Eng 48:7607712001

43

Stancák A JrPfurtscheller G: Desynchronization and recovery of beta rhythms during brisk and slow self-paced finger movements in man. Neurosci Lett 196:21241995

44

Taniguchi MKato AFujita NHirata MTanaka HKihara T: Movement-related desynchronization of the cerebral cortex studied with spatially filtered magnetoencephalography. Neuroimage 12:2983062000

45

Taniguchi MKato ANinomiya HHirata MCheyne DRobinson SE: Cerebral motor control in patients with gliomas around the central sulcus studied with spatially filtered magnetoencephalography. J Neurol Neurosurg Psychiatry 75:4664712004

46

Tarkiainen ALiljestrom MSeppa MSalmelin R: The 3D topography of MEG source localization accuracy: effects of conductor model and noise. Clin Neurophysiol 114:197719922003

47

Vrba JRobinson SE: Signal processing in magnetoencephalography. Methods 25:2492712001

48

Yang TTGallen CCSchwartz BJBloom FE: Noninvasive somatosensory homunculus mapping in humans by using a large-array biomagnetometer. Proc Natl Acad Sci U S A 90:309831021993

TrendMD

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 130 130 46
Full Text Views 159 159 14
PDF Downloads 125 125 9
EPUB Downloads 0 0 0

PubMed

Google Scholar