Task-free presurgical mapping using functional magnetic resonance imaging intrinsic activity

Laboratory investigation

Restricted access

Object

Low-frequency components of the spontaneous functional MR imaging signal provide information about the intrinsic functional and anatomical organization of the brain. The ability to use such methods in individual patients may provide a powerful tool for presurgical planning. The authors explore the feasibility of presurgical motor function mapping in which a task-free paradigm is used.

Methods

Six surgical candidates with tumors or epileptic foci near the motor cortex participated in this study. The investigators directly compared task-elicited activation of the motor system to activation obtained from intrinsic activity correlations. The motor network within the unhealthy hemisphere was identified based on intrinsic activity correlations, allowing distortions of functional anatomy caused by the tumor and epilepsy to be directly visualized. The precision of the motor function mapping was further explored in 1 participant by using direct cortical stimulation.

Results

The motor regions localized based on the spontaneous activity correlations were quite similar to the regions defined by actual movement tasks and cortical stimulation. Using intrinsic activity correlations, it was possible to map the motor cortex in presurgical patients.

Conclusions

This task-free paradigm may provide a powerful approach to map functional anatomy in patients without task compliance and allow multiple brain systems to be determined in a single scanning session.

Abbreviations used in this paper:fcMR = functional connectivity MR; fMR = functional MR.

Article Information

Address correspondence to: Steven M. Stufflebeam, M.D., Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Building 149, 13th Street, Charlestown, Massachusetts 02129. email:sms@nmr.mgh.harvard.edu.

Please include this information when citing this paper: published online April 10, 2009; DOI: 10.3171/2008.10.JNS08846.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Task and fcMR imaging–based mapping localizing similar regions. Hand motor regions defined by actual motor task movements (left column) and task-free fcMR imaging (center column) are plotted on sagittal sections for each patient (overlaid on their structural image). Colors represent Z values, with the threshold set to Z = 0.4–0.5. The overlap of the two techniques is shown in red (right column). Each row displays a different patient, with the sex (M or F) and age (in years) indicated in the rightmost panel. Brain lesions are indicated by the white triangles for the patients in Cases 1, 2, and 4; the patient in Case 3 has no visible lesion.

  • View in gallery

    Functional mapping based on fcMR imaging is anatomically specific. These studies are comparisons of hand and tongue motor regions defined by actual motor task movements (left columns) and task-free fcMR imaging (center columns). The overlap of the two techniques is shown in red (right columns). The upper panels show data from the patient in Case 2, and the lower panels from the patient in Case 4. The right hemisphere is displayed on the right side of the panel. Note the systematic shift of the location of the hand and tongue regions in each patient, which is present for the fcMR analysis. The fcMR analysis of the hand region in the patient in Case 2 is less stable than other measures, possibly due to the location of the seizure activity (see text).

  • View in gallery

    Functional mapping based on fcMR imaging is robust across different image resolutions. These studies are comparisons of hand and tongue motor regions defined by actual motor task movements (left column) and task-free fcMR imaging (center column), similar to those in Fig. 2. The resting-state images were acquired using 3-mm isotropic voxels and 2-second TR, as in the task scans.

  • View in gallery

    Comparison of results of direct cortical stimulation and fcMR imaging. The intraoperative photograph in the upper panel shows the grid placement for the patient in Case 2 and the locations of the electrodes that disrupted hand (14, 22) and tongue (40, 47, 48) movements. The fcMR analysis results are displayed in the lower panels; the hand motor region (left column) and the tongue motor region (right column) are displayed. Activation maps show the results of fcMR imaging analysis from Fig. 2. Filled green circles show the locations of cortical stimulation electrodes that selectively disrupted hand and tongue movements. The hand and tongue regions defined by fcMR imaging correlate with the estimates of the regions based on stimulation.

References

1

Abou–Khalil BSchlaggar BL: Is it time to replace the Wada test?. Neurology 59:1601612002

2

Berger MSCohen WAOjemann GA: Correlation of motor cortex brain mapping data with magnetic resonance imaging. J Neurosurg 72:3833871990

3

Biswal BYetkin FZHaughton VMHyde JS: Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:5375541995

4

Bittar RGOlivier ASadikot AFAndermann FPike GBReutens DC: Presurgical motor and somatosensory cortex mapping with functional magnetic resonance imaging and positron emission tomography. J Neurosurg 91:9159211999

5

Boroojerdi B: Localization of the motor hand area using transcranial magnetic stimulation and functional magnetic resonance imaging. Clin Neurophysiol 110:6997041999

6

Brainard DH: The psychophysics toolbox. Spat Vis 10:4334361997

7

Buckner RLHead DParker JFotenos AFMarcus DMorris JC: A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage 23:7247382004

8

Buckner RLVincent JL: Unrest at rest: default activity and spontaneous network correlations. Neuroimage 37:109110962007

9

Cordes DHaughton VMArfanakis KWendt GJTurski PAMoritz CH: Mapping functionally related regions of brain with functional connectivity MR imaging. AJNR Am J Neuroradiol 21:163616442000

10

Damoiseaux JSRombouts SABarkhof FScheltens PStam CJSmith SM: Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A 103:13848138532006

11

De Luca MBeckmann CFDe Stefano NMatthews PMSmith SM: fMRI resting state networks define distinct modes of long-distance interactions in the human brain. Neuroimage 29:135913672006

12

Fandino JKollias SSWieser HGValavanis AYonekawa Y: Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex. J Neurosurg 91:2382501999

13

Fernandez Gde Greiff Avon Oertzen JReuber MLun SKlaver P: Language mapping in less than 15 minutes: real-time functional MRI during routine clinical investigation. Neuroimage 14:5855942001

14

Fischl BSereno MIDale AM: Cortical surface-based analysis II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:1952071999

15

Fox MDCorbetta MSnyder AZVincent JLRaichle ME: Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. Proc Natl Acad Sci U S A 103:10046100512006

16

Fox MDRaichle ME: Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:7007112007

17

Fransson PSkiöld BHorsch SNordell ABlennow MLagercrantz H: Resting-state networks in the infant brain. Proc Natl Acad Sci U S A 104:15531155362007

18

Friston KJHolmes APWorsley KJPoline JPFrith CDFrackowiak RSJ: Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:1892101995

19

Fukunaga MHorovitz Svan Gelderen Pde Zwart JAJansma JMIkonomidou VN: Large-amplitude, spatially correlated fluctuations in BOLD fMRI signals during extended rest and early sleep stages. Magn Reson Imaging 24:9799922006

20

Gregorie EMGoldring S: Localization of function in the excision of lesions from the sensorimotor region. J Neurosurg 61:104710541984

21

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

22

Haughton VMTurski PAMeyerand BWendt GMoritz CHUlmer J: The clinical applications of functional MR imaging. Neuroimaging Clin N Am 9:2852931999

23

Hirsch JRuge MIKim KHCorrea DDVictor JDRelkin NR: An integrated functional magnetic resonance imaging procedure for preoperative mapping of cortical areas associated with tactile, motor, language, and visual functions. Neurosurgery 47:7117212000

24

Holodny AISchulder MLiu WCWolko JMaldjian JAKalnin AJ: The effect of brain tumors on BOLD functional MR imaging activation in the adjacent motor cortex: implications for image-guided neurosurgery. AJNR Am J Neuroradiol 21:141514222000

25

Hunter MDEickhoff SBMiller TWFarrow TFWilkinson IDWoodruff PW: Neural activity in speech-sensitive auditory cortex during silence. Proc Natl Acad Sci U S A 103:1891932006

26

Iwasaki SNakagawa HFukusumi AKichikawa KKitamura KOtsuji H: Identification of pre- and postcentral gyri on CT and MR images on the basis of the medullary pattern of cerebral white matter. Radiology 179:2072121991

27

Jack CR JrThompson RMButts RKSharbrough FWKelly PJHanson DP: Sensory motor cortex: correlation of presurgical mapping with functional MR imaging and invasive cortical mapping. Radiology 190:85921994

28

Jenkinson MBannister PBrady MSmith S: Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:8258412002

29

Krings TTöpper RWillmes KReinges MHGilsbach JMThron A: Activation in primary and secondary motor areas in patients with CNS neoplasms and weakness. Neurology 58:3813902002

30

Lee MReddy HJohansen-Berg HPendlebury SJenkinson MSmith S: The motor cortex shows adaptive functional changes to brain injury from multiple sclerosis. Ann Neurol 47:6066132000

31

Margulies DSKelly AMUddin LQBiswal BBCastellanos FXMilham MP: Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 37:5795882007

32

Miezin FMMaccotta LOllinger JMPetersen SEBuckner RL: Characterizing the hemodynamic response: effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing. Neuroimage 11:7357592000

33

Mueller WMYetkin FZerrin HThomas AMorris GLSwanson SJ: Functional magnetic resonance imaging mapping of the motor cortex in patients with cerebral tumors. Neurosurgery 39:5155211996

34

Nir YHasson ULevy IYeshurun YMalach R: Widespread functional connectivity and fMRI fluctuations in human visual cortex in the absence of visual stimulation. Neuroimage 30:131313242006

35

Ojemann GA: Individual variability in cortical organization of language. J Neurosurg 50:1641691979

36

Pelli DG: The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spat Vis 10:4374421997

37

Penfield WBoldrey E: Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:3894431937

38

Roux FEBoulanouar KRanjeva JPTremoulet MHenry PManelfe C: Usefulness of motor functional MRI correlated to cortical mapping in rolandic low-grade astrocytomas. Acta Neurochir (Wien) 141:71791999

39

Skirboll SSOjemann GABerger MSLettich EWinn HR: Functional cortex and subcortical white matter located within gliomas. Neurosurgery 38:6786851996

40

Stapleton SRKiriakopoulos EMikulis DDrake JMHoffman HJHumphreys R: Combined utility of functional MRI, cortical mapping, and frameless stereotaxy in the resection of lesions in eloquent areas of brain in children. Pediatr Neurosurg 26:68821997

41

Steinmetz HFurst GFreund HJ: Variation of perisylvian and calcarine anatomic landmarks within stereotaxic proportional coordinates. AJNR Am J Neuroradiol 11:112311301990

42

Urasaki EUematsu SGordon BLesser RP: Cortical tongue area studied by chronically implanted subdural electrodes–with special reference to parietal motor and frontal sensory responses. Brain 117:1171321994

43

Vincent JLPatel GHFox MDSnyder AZBaker JTvan Essen DC: Intrinsic functional architecture in the anaesthetized monkey brain. Nature 447:83862007

44

Vincent JLSnyder AZFox MDShannon BJAndrews JRRaichle ME: Coherent spontaneous activity identifies a hippocampal-parietal memory network. J Neurophysiol 96:351735312006

45

Wada J: A new method for determination of the side of cerebral speech dominance: a preliminary report on the intracarotid injection of sodium amytal in man. Igaku Seibutsugaku 14:2212221949

46

Woolsey CNErickson TCGilson WE: Localization in somatic sensory and motor areas of human cerebral cortex as determined by direct recording of evoked potentials and electrical stimulation. J Neurosurg 51:4765061979

47

Wunderlich GKnorr UHerzog HKiwit JCFreun HJSeitz RJ: Precentral glioma location determines the displacement of cortical hand representation. Neurosurgery 42:18261998

48

Yetkin FZMueller WMMorris GLMcAuliffe TLUlmer JLCox RW: Functional MR activation correlated with intraoperative cortical mapping. AJNR Am J Neuroradiol 18:131113151997

49

Yousry TASchmid UDAlkadhi HSchmidt DPeraud ABuettner A: Localization of the motor hand area to a knob on the precentral gyrus: a new landmark. Brain 120:1411571997

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