sensory motor cortex: correlation of presurgical mapping ... · motor cortex wasperformed intwo...

8
Clifford R. Jack, Jr. MD #{149} Richard M. Thompson, MD #{149} R. Kim Butts, PhD Frank W. Sharbrough, MD #{149} Patrick J. Kelly, MD #{149} Dennis P. Hanson, BS Stephen J. Riederer, PhD #{149} Richard L. Ehman, MD #{149} Nicholas J. Hangiandreou, PhD Gregory D. Cascino, MD Sensory Motor Cortex: Correlation of Presurgical Mapping with Functional MR Imaging and Invasive Cortical Mapping’ 85 Neuroradiology PURPOSE: To describe a clinically useful application of functional mag- netic resonance (MR) imaging-pre- surgical mapping of the sensory mo- tor cortex-and to validate the results with established physiologic tech- niques. MATERIALS AND METHODS: Func- tional MR mapping of the sensory motor cortex was performed in two women, aged 24 and 38 years. Both had intractable, simple partial motor seizures due to tumors located in or near the sensory motor cortex. They subsequently underwent invasive cortical mapping-direct cortical stimulation and/or sensory-evoked- potential recording-to localize the affected sensory motor area prior to tumor resection. RESULTS: In both patients, the func- tional MR study demonstrated task activation of the sensory motor cor- tex. In both cases, results of cortical functional mapping with invasive techniques matched those obtained with functional MR imaging. CONCLUSION: Presurgical mapping of the sensory motor cortex is a po- tentially useful clinical application of functional MR imaging. Index terms: Blood, flow dynamics #{149} Brain, blood flow, 10.919 #{149} Brain, function, 10.919 Epilepsy #{149} Magnetic resonance (MR), vascular studies Radiology 1994; 190:85-92 I From the Departments of Diagnostic Radiol- ogy (C.R.J., R.M.T., R.K.B., S.J.R., R.LE., N.J.H.), Neurology (F.W.S., G.D.C.), Neurosurgery (P.1K.), and Biomedical Imaging Resource (D.P.H.), Mayo Clinic and Foundation, 200 First St SW, Rochester, MN 55905. Received June 2, 1993; revision requested July 27; revision re- ceived August 23; accepted September 7. Sup- ported in part by Public Health Service grants no. ROl NS28374, ROl CA37993, and HL07269- 15. Address reprint requests to CR1. RSNA, 1994 I F surgical resection of a lesion lo- cated in or near functionally es- sential cortex is considered, then lo- calization of functional areas relative to the surgical target (the lesion) must be ascertained to avoid a postopera- tive neurologic deficit. This is particu- larly critical in patients whose only symptom is epilepsy. Such patients tend to have benign or indolent non- life-threatening lesions, and a postop- erative neurologic deficit may repre- sent an unacceptable surgical risk. Traditionally, presurgical functional localization has been accomplished with invasive means: (a) direct cortical stimulation either intraoperatively in the awake patient or postoperatively after subdural grid placement or (b) sensory-evoked-potential studies after operative grid placement. It has been shown recently that functional magnetic resonance (MR) imaging with blood oxygen level- dependent (BOLD) contrast is capable of noninvasively depicting primary sensory areas including the sensory motor cortex (1-9). However, studies to date have used volunteers and there has been no direct validation of the physiologic truth of functional localization with MR imaging. In this article we describe a clinically useful application of functional MR map- ping of the sensory motor cortex for surgical planning. In addition, we compare the results of localization with functional MR imaging with the accepted criterion standard of inva- sive cortical mapping. MATERIALS AND METHODS Case 1 The patient was a 24-year-old woman who had been having simple partial motor seizures since she was 7’/2 years old. When she was evaluated at our institution, she was having two to five seizures per month despite treatment with an optimal antiepi- leptic medical regimen. Her seizures be- gan with an aura of right facial numbness and a painful sensation in the throat fol- lowed by choking and speech arrest. Post- ictally she was dysanthric with a right facial droop. Seizures were not accompa- nied by loss of consciousness. At age 19 years, a computed tomography (CT) scan was reportedly negative, and at age 23 years an MR study demonstrated a left frontoparietal lesion (Fig 1). She was evaluated at our institution as a surgical candidate and was admitted for pro- longed inpatient video-electroencephalo- graphic monitoring with withdrawal of medication. Ictal onset was determined to be of left frontal origin. On the basis of both clinical and electroencephalographic criteria, the site of seizure onset was in or near the left sensory motor cortex. Preop- erative testing also included speech, lan- guage, and neuropsychologic evaluation, the results of which were within normal limits. Physical examination revealed mild right facial weakness, but findings were otherwise negative. Cerebral angiography with amytal testing demonstrated left hemispheric speech dominance. A functional MR examination with task activation of the sensorimotor cortex was performed with use of an approach similar to that described by Connelly et al (8). A series of short Ti-weighted acquisitions in the axial and oblique planes were ob- tamed to localize the tumor. From these Ti-weighted images, several anatomic planes of interest were selected in which to perform functional MR imaging. The functional MR sequence consisted of ob- taming 20 consecutive 3D SPGR images at a single section location with the follow- ing parameters: echo time, 60 msec; repeti- tion time, 80 msec; flip angle, 40#{176}; field of view, 24 cm; section thickness, 4 mm; one signal averaged; a 64 x 64 matrix; and 5.i seconds per image. These images were obtained on a i.5-T system (Signa; GE Medical Systems, Milwaukee, Wis) with standard hardware and software (the only software modification was that permitting use of the coarse acquisition matrix). Dur- ing this 20-image acquisition, the patient Abbreviations: BOLD = blood oxygen level dependent, 3D SPGR = three-dimensional spoiled gradient-recalled acquisition in the steady state.

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Page 1: Sensory Motor Cortex: Correlation of Presurgical Mapping ... · motor cortex wasperformed intwo women, aged 24and38years. Both hadintractable, simple partial motor seizures duetotumors

Clifford R. Jack, Jr. MD #{149}Richard M. Thompson, MD #{149}R. Kim Butts, PhDFrank W. Sharbrough, MD #{149}Patrick J. Kelly, MD #{149}Dennis P. Hanson, BSStephen J. Riederer, PhD #{149}Richard L. Ehman, MD #{149}Nicholas J. Hangiandreou, PhDGregory D. Cascino, MD

Sensory Motor Cortex: Correlation ofPresurgical Mapping with Functional MRImaging and Invasive Cortical Mapping’

85

Neuroradiology

PURPOSE: To describe a clinicallyuseful application of functional mag-netic resonance (MR) imaging-pre-surgical mapping of the sensory mo-tor cortex-and to validate the resultswith established physiologic tech-niques.

MATERIALS AND METHODS: Func-tional MR mapping of the sensorymotor cortex was performed in twowomen, aged 24 and 38 years. Bothhad intractable, simple partial motorseizures due to tumors located in ornear the sensory motor cortex. Theysubsequently underwent invasivecortical mapping-direct cortical

stimulation and/or sensory-evoked-potential recording-to localize theaffected sensory motor area prior totumor resection.

RESULTS: In both patients, the func-tional MR study demonstrated taskactivation of the sensory motor cor-tex. In both cases, results of corticalfunctional mapping with invasivetechniques matched those obtainedwith functional MR imaging.

CONCLUSION: Presurgical mappingof the sensory motor cortex is a po-tentially useful clinical application offunctional MR imaging.

Index terms: Blood, flow dynamics #{149}Brain,

blood flow, 10.919 #{149}Brain, function, 10.919

Epilepsy #{149}Magnetic resonance (MR), vascular

studies

Radiology 1994; 190:85-92

I From the Departments of Diagnostic Radiol-

ogy (C.R.J., R.M.T., R.K.B., S.J.R., R.LE., N.J.H.),Neurology (F.W.S., G.D.C.), Neurosurgery(P.1K.), and Biomedical Imaging Resource(D.P.H.), Mayo Clinic and Foundation, 200 FirstSt SW, Rochester, MN 55905. Received June 2,1993; revision requested July 27; revision re-ceived August 23; accepted September 7. Sup-ported in part by Public Health Service grantsno. ROl NS28374, ROl CA37993, and HL07269-15. Address reprint requests to CR1.

� RSNA, 1994

I F surgical resection of a lesion lo-

cated in or near functionally es-

sential cortex is considered, then lo-

calization of functional areas relative

to the surgical target (the lesion) must

be ascertained to avoid a postopera-

tive neurologic deficit. This is particu-

larly critical in patients whose only

symptom is epilepsy. Such patients

tend to have benign or indolent non-life-threatening lesions, and a postop-

erative neurologic deficit may repre-

sent an unacceptable surgical risk.Traditionally, presurgical functional

localization has been accomplished

with invasive means: (a) direct corticalstimulation either intraoperatively in

the awake patient or postoperatively

after subdural grid placement or

(b) sensory-evoked-potential studies

after operative grid placement.

It has been shown recently thatfunctional magnetic resonance (MR)

imaging with blood oxygen level-

dependent (BOLD) contrast is capableof noninvasively depicting primary

sensory areas including the sensory

motor cortex (1-9). However, studies

to date have used volunteers andthere has been no direct validation of

the physiologic truth of functional

localization with MR imaging. In thisarticle we describe a clinically useful

application of functional MR map-

ping of the sensory motor cortex forsurgical planning. In addition, we

compare the results of localization

with functional MR imaging with theaccepted criterion standard of inva-

sive cortical mapping.

MATERIALS AND METHODS

Case 1

The patient was a 24-year-old womanwho had been having simple partial motorseizures since she was 7’/2 years old. When

she was evaluated at our institution, shewas having two to five seizures per month

despite treatment with an optimal antiepi-leptic medical regimen. Her seizures be-

gan with an aura of right facial numbness

and a painful sensation in the throat fol-lowed by choking and speech arrest. Post-

ictally she was dysanthric with a right

facial droop. Seizures were not accompa-

nied by loss of consciousness. At age 19years, a computed tomography (CT) scanwas reportedly negative, and at age 23

years an MR study demonstrated a leftfrontoparietal lesion (Fig 1). She was

evaluated at our institution as a surgical

candidate and was admitted for pro-

longed inpatient video-electroencephalo-graphic monitoring with withdrawal of

medication. Ictal onset was determined to

be of left frontal origin. On the basis of

both clinical and electroencephalographiccriteria, the site of seizure onset was in or

near the left sensory motor cortex. Preop-erative testing also included speech, lan-guage, and neuropsychologic evaluation,the results of which were within normallimits. Physical examination revealed mild

right facial weakness, but findings were

otherwise negative. Cerebral angiography

with amytal testing demonstrated lefthemispheric speech dominance.

A functional MR examination with taskactivation of the sensorimotor cortex wasperformed with use of an approach similarto that described by Connelly et al (8). Aseries of short Ti-weighted acquisitions inthe axial and oblique planes were ob-

tamed to localize the tumor. From theseTi-weighted images, several anatomicplanes of interest were selected in whichto perform functional MR imaging. The

functional MR sequence consisted of ob-taming 20 consecutive 3D SPGR images ata single section location with the follow-ing parameters: echo time, 60 msec; repeti-tion time, 80 msec; flip angle, 40#{176};field ofview, 24 cm; section thickness, 4 mm; onesignal averaged; a 64 x 64 matrix; and 5.i

seconds per image. These images wereobtained on a i.5-T system (Signa; GEMedical Systems, Milwaukee, Wis) with

standard hardware and software (the only

software modification was that permitting

use of the coarse acquisition matrix). Dur-

ing this 20-image acquisition, the patient

Abbreviations: BOLD = blood oxygen leveldependent, 3D SPGR = three-dimensionalspoiled gradient-recalled acquisition in thesteady state.

Page 2: Sensory Motor Cortex: Correlation of Presurgical Mapping ... · motor cortex wasperformed intwo women, aged 24and38years. Both hadintractable, simple partial motor seizures duetotumors

a. b.

86 #{149}Radiology January 1994

Figure 1. Patient 1. Diagnostic MR images. (a) Axial and (b) reformatted coronal images from a three-dimensional spoiled gradient-recalled

acquisition in the steady state (3D SPGR) sequence. These images demonstrate a peripherally located left frontopanietal tumor, with a complex

relationship to the local normal sulcal anatomy. The inferior border of the tumor is at the brain surface and erodes the adjacent inner table, in-dicating its indolent nature.

alternated between rest and a voluntaryactivation task, which consisted of bilat-eral fingers to thumb opposition and con-traction and relaxation of the lip andlower face muscles to activate the handand lip-lower face portion of the sensorymotor homunculus. The lip-lower facetask was performed with no jaw motion(ie, only facial muscles around the mouth

were moved) to minimize the possibilityof head movement. Image processing con-sisted of simple image subtraction. The 20images were partitioned into four clustersof five inactive, five active, five inactive,and five active images. The first image ofeach cluster was eliminated to produce asteady magnetization state for the firstcluster of images and a physiologic steadystate for the remaining three clusters. Theactive images were then added togetherand subtracted from the sum of the mac-tive images.

To anatomically link areas of activationon functional MR images to cortical sun-face anatomy, a volume rendering of thebrain surface was performed with use of

software (Analyze; Biomedical ImagingResource, Mayo Clinic and Foundation,Rochester, Minn) (10). The brain was seg-mented from overlying structures bymeans of a series of mathematical erode,connect, and dilate morphology opera-lions. The segmented MR imaging datawere then loaded into a program that si-

multaneously displayed the volume-ren-dered image of the brain surface againstthe cross-sectional plane in which thefunctional MR images were obtained.

The patient subsequently underwentsurgical implantation of a series of subdu-ral recording strips. A small craniotomywas performed over the tumor, which had

been localized stereotaxically. Three verti-cally oriented strips were placed above thetumor, and one horizontal T strip wasplaced below the tumor. Each recordingstrip consisted of eight circular stainlesssteel electrode contacts that were 4 mm in

diameter, iO mm in center-to-center dis-tance, and embedded in a 75-mm-longSilastic (Dow Corning, Midland, Mich)sheath. Eight wire leads emerged fromone end of the vertically placed strips andfrom the middle of the horizontally placedT strip. These leads passed through thecraniotomy and were connected to theexternal circuitry. A cortical stimulationstudy was performed the following day.Current was passed between pairs of elec-trodes in a systematic fashion. The rela-tionship between specific pairs of elec-trodes and elicited sensory and/or motorfunctions of the hand, foot, and face wasrecorded. Also recorded were those stimu-lation pains that reproduced the patient’s

aura.A thin-section CT study was then per-

formed with the subdural recording stripsin place. The CT study was co-registered

with a 3D SPGR MR sequence obtainedpreoperatively by using a surface-match-ing algorithm (ii). The position of each

individual electrode contact was extracted

from the registered CT data and was

stored as a separate object in an objectmap. The brain and the tumor were seg-mented from the 3D SPGR images andwere stored as separate objects in the ob-ject map. A volume-rendered image of thebrain surface with the tumor and each in-dividual electrode contact rendered as

separate objects was generated by using a24-bit color compositing multiple-objectvolume-rendering technique (10).

The patient then underwent surgicalremoval of the tumor. Prior to tumor re-moval, intraoperative sensory evoked p0-tential tests were performed. Pathologic

examination revealed a grade 2 oligoden-droglioma. Postoperatively, findings at the

patient’s neurologic examination were un-

changed.

Case 2

The second patient was a 38-year-oldwoman who was well until she experi-enced several secondarily generalizedtonic-clonic seizures at age 30 years. MR

imaging performed at that time demon-

strated a right frontal intraaxial tumor (Fig

2). When she was seen at our institution,the patient was experiencing approxi-mately two seizures per week despite re-ceiving optimal medical therapy. Theseseizures began with an aura of numbness

in the left hand or hemibody, and ap-

proximately iO% of the auras proceeded

to become focal motor seizures involvingthe left upper and lower extremity withspeech arrest but with no loss of con-

sciousness. Preoperatively, single-sectionfunctional MR imaging was performed in

several anatomic planes of interest. Sepa-

rate hand and foot activation tasks werepositioned as outlined for patient 1. Pro-

longed scalp-recorded inpatient video-electroencephalographic monitoring re-vealed right frontal seizure onset. Duringthe surgical procedure, recording stripswere placed over the paracentral cortexand sensory-evoked-potential tests withmedian nerve stimulation were performed

to document the position of the centralsulcus in relation to the tumor. The tumor

Page 3: Sensory Motor Cortex: Correlation of Presurgical Mapping ... · motor cortex wasperformed intwo women, aged 24and38years. Both hadintractable, simple partial motor seizures duetotumors

Figure 2. Patient 2. Diagnostic MR images. Axial (a) T2-weighted and (b) Ti-weighted im-ages reveal an infiltrative right frontal tumor.

Volume 190 #{149}Number I Radiology #{149}87

was removed and identified as a grade 3

oligodendroglioma. The patient experi-enced no motor deficit as a result of sur-

gery.

Case 1

RESULTS

The functional MR images of thispatient performing the task describeddemonstrated clear-cut cortical activa-tion centered between two verticallyoriented gyri. We expected these to bethe pre- and postcentral gyri, with theactivation centered in the central sul-cus. On the basis of the findings in the

functional MR study, we concludedthat the tumor straddled the inferiorportion of the central sulcus (Fig 3).The functional task administeredshould have activated both the handand the lip-lower face portions of thesensorimotor homunculus (Fig 4) (12).

In Figure 3b the majority of the acti-vated area lies well above the tumor;the lowest portion of the activatedstrip is located at the uppermost bor-der of the tumor. On the basis of find-ings in the images in Figure 3, we pre-dicted that resection of the tumorwould involve the lip-lower face por-lion of the sensorimotor homunculusbut not the more cephalic hand area.As a rule, surgical damage to the handor foot portion of the homunculusproduces a severe functional deficit

and is to be avoided, while damage tothe face-lip portion will produce aclinically negligible deficit.

Figure 5 is a schematic drawing of

the position of the four subdural re-cording strips in relation to the tumor

and of the results of the cortical

stimulation studies. Stimulation of thevertical strips revealed the expectedorientation of the sensory motor ho-munculus of Penfleld and Rasmussen(12). From the stimulation studies itwas deduced that strip A was located

over the motor cortex, strip B over thesensory cortex, and strip C posterior

to the sensory cortex (Fig 5). The cen-tral sulcus was therefore located be-tween strips A and B. Intraoperativesensory-evoked-potential recordingwith median nerve stimulation dem-onstrated maximum response at elec-trode 4 on strip B, thereby also con-firming that strip B was over theprimary sensory cortex. Stimulationbetween the lower electrodes onstrips A and B, as well as between

electrodes 4 and 5 on strip D, repro-duced the patient’s aura, a sensationin the throat. Intraoperatively, onlythe most inferior contacts of the threevertically oriented strips and contacts4-6 of strip D were visible (Fig 6). Theremaining contacts were hidden be-neath the intact skull. Intraoperativephotographs (Fig 6) document thatthe portion of the tumor at the brainsurface was located between and infe-rior to contact 8 of strips A and B andabove contacts 4 and 5 of strip D. Be-cause of the limited exposure of the

brain surface provided by the smallcraniotomy and because of the factthat the tumor had distorted normallocal anatomic landmarks, an ana-tomic central sulcus could not beidentified by inspecting the operativefield. Because intraoperative inspec-tion did not provide the desired cor-

relation between the invasive stimula-tion studies and functional MRmapping, the following strategy waspursued.

A volume rendering of the brainsurface was generated with the tumorand electrode contacts rendered asseparate objects (Fig 7). This render-ing demonstrated the relationship ofindividual electrode contacts to boththe tumor and the cortical topogra-

phy that could not be appreciatedintraoperatively. This is a useful tech-nique, because it enables correlationbetween the results of direct corticalstimulation and functional MR imag-ing. Visual comparison of the volume-rendered brain surface images in Fig-

ures 3 and 7 confirmed the impressionformed from the functional MR studythat the tumor straddled the func-tional sensorimotor strip.

Case 2

In patient 2, images of only onetask (opposition of repetitive fingers

to thumb) demonstrated convincingfunctional activation (Fig 8). Failedimages were most likely a result ofpatient motion. As this patient haddifficulty with head motion, the func-

tional image (Fig 8) was generatedwith a single inactive-active cycle.Because of artifacts in this image,color mapping of functional activa-tion onto a Ti-weighted anatomictemplate was not effective. Instead, alinked-cursor display was used toidentify common pixels in the Ti-

weighted and functional images (10).Figure 8b demonstrates a curvilineararea of activation centered on a sulcus(the central sulcus) that is posterior tothe tumor. We inferred from this thatthe tumor extended posteriorly to butdid not directly involve the primarymotor strip. On the basis of findingsin this image, we predicted that resec-lion of the tumor would spare theprimary motor cortex.

At surgery, the craniotomy was notextended beyond the posterior mar-gin of the tumor, and therefore therelationship between the tumor andthe cortical topography posterior to itcould not be appreciated visually.However, intraoperative sensory-evoked-potential recording was per-formed by inserting subdural recording

strips beneath the posterior margin of

the craniotomy flap. Findings at leftmedian nerve stimulation demon-strated that the central sulcus waslocated approximately 2 cm posteriorto the posterior margin of the tumor,thus confirming the impressionformed at functional MR imaging.

Page 4: Sensory Motor Cortex: Correlation of Presurgical Mapping ... · motor cortex wasperformed intwo women, aged 24and38years. Both hadintractable, simple partial motor seizures duetotumors

10

88 #{149}Radiology January 1994

Figure 3. Patient 1. Functional MR images. ++ct�e I +ct��e � �+ct� � act�e I ‘+ct�+e octi�+ �+ct�+e

(a, b) Four-panel collages. The upper leftpanel is a Ti-weighted anatomic template of 20

the cross section in which the corresponding

functional MR imaging sequence was ob- � � �tamed (a small arrow indicates the position �

of the tumor). The upper right panel repre- � � �sents the functional activation image formed � �, I 10

by the addition and subtraction process out- �lined herein. The lower right panel is created I

by assigning a color map to the functionalimage and then fusing that image with the � � I

Ti-weighted anatomic template. The lower 20 30 40 10 20 30 40

left panel represents a volume rendering of Image �umber Image Number

the brain surface with the tumor rendered as C. d.a separate green object and with the plane inwhich the functional MR image was obtained indicated by a line (as in a) or a shaded gray planar surface (as in b). Part a was obtained axially

through the top of the tumor. Activation of the sensory motor cortex bilaterally is seen in the top right functional activation image. The rela-tionship of the activated sensorimotor cortex in the patient’s left hemisphere to the top of the tumor is illustrated in the fused image in the bot-torn right panel. Part b is an oblique section with anterior (ANT), posterior (POST), superior (SUP), and inferior (INF) labeled for orientation inthe Ti-weighted image in the top left panel. The curvilinear area of activation (top and lower right panels) precisely follows the contour of the

central sulcus. The most inferior portion of this activated strip should represent the lip-lower face portion of the homunculus, whereas themore superior portion should represent the hand portion. The tumor is centered on and elevates the most inferior portion of the central sulcus,the top of which is indicated by a large arrow in the lower left images. (c, d) Time course plots of signal intensity in a manually defined regionof interest. Part c is from a region of interest in the left sensorimotor area in a, and part d is from the sensorimotor area in b. Both c and d dem-onstrate a cyclic change in signal intensity, which follows the periodicity of the activation task.

DISCUSSION

Functional activation of the cortexwith MR imaging was first demon-strated by means of a contrast bolus-tracking technique (i3). It has been

subsequently shown that this phe-nomenon can be visualized without

exogenously administered contrastmaterial (1-9). Fox and Raichle (14)demonstrated with positron emissiontomography that appropriately de-signed stimulation paradigms willproduce a local change in a number ofphysiologic parameters from baseline,in appropriate areas of the cortex.

Most relevent to this type of imagingare the facts that cerebral perfusionwill increase locally and will do so inexcess of the oxygen metabolic rate.This results in both an increase in tis-sue perfusion and a paradoxical netdecrease in concentration of deoxyhe-moglobin in the capillary and venousbed of an activated area of cerebralcortex. Oxygenated hemoglobin isdiamagnetic whereas deoxyhemoglobin

is paramagnetic (15,16). The paramag-netic properties of deoxyhemoglobincreate local field inhomogeneities,which decrease intravoxel spin coher-ence in the vicinity of blood vessels

and thereby decrease the signal inten-sity on T2- or T2*�weighted MR images(15-20). Ogawa et al (17,18) suggested

that the state of blood oxygenationmay be a useful contrast parameter atMR imaging, and they coined the ac-ronym BOLD contrast. Two possiblemechanisms may contribute to the in-

creased signal intensity seen in func-tionally activated cortical areas: Oneis the BOLD effect. The other is an in-

creased flow of unsaturated spins into

the imaging section which cycles inphase with the periodicity of the acti-vation task. The precise interrelation-ship between these two mechanisms

Page 5: Sensory Motor Cortex: Correlation of Presurgical Mapping ... · motor cortex wasperformed intwo women, aged 24and38years. Both hadintractable, simple partial motor seizures duetotumors

I

Figure 4. Motor homunculus. Pictorial representation of the loca-tion and relative extent of the different portions of the motor ho-munculus on the precentral gyrus. Analogous sensory areas arerepresented on the postcentral gyros. (Reprinted, with permission,from reference i2.)

sup.

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Figure 5. Patient I. Subdural strips schematic of the position of the four subdural recordstrips (A, B, C, D) in relation to the tumor: anterior (ANT), superior (SUP), posterior (POST),

and inferior (INF). MOT = motor response, SENS = sensory response. The central sulcus lies

between strips in a and b. Results match the Penfield homunculus seen in Figure 4.

Volume 190 #{149}Number 1 Radiology #{149}89

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and observed activation-inducedchange in MR signal intensity is notyet clear. Use of a small flip angle and

a phase-encoding scheme in whichthe central lines of K space are en-coded first should decrease the effectof inflow enhancement; however, nei-

ther of these were employed in thesetwo patients (5,7).

Most functional MR imaging workto date has focused on the BOLD ef-fect. BOLD contrast results from a netdecrease in concentration of deoxyhe-moglobin in the capillary and venous

system during task activation. Ideally,

the accompanying changes in signalintensity at MR imaging serve as aprecise marker of those areas of cortexthat have undergone task activation.However, it is theoretically possiblethat the net influx of oxyhemoglobininto the venous system surroundingan area of activated cortex may bewashed downstream, away from the

specific area of task-activated cortex.Conceivably, alterations in signal in-tensity associated with task activation

could be present in large superficialveins projecting over areas of cerebralcortex that were not involved in theactivation process. If this were thecase, then BOLD functional MR imag-ing would be far less specific and lessuseful for cortical mapping than if thealterations in signal intensity re-mained confined to the capillary bedor to small veins in the sulcus physi-cally adjacent to the areas of cortexthat were directly activated. It hasrecently been shown that the weight-ing of BOLD contrast with respect tovessel size varies as a function of bothstrength of static magnetic field andtype of echo (20,21). Imaging at highfield strength (4 T) and with a spin-echo technique produces greater con-trast weighting for small vessels (ie, 3�im or capillary level) than does imag-ing at lower field strength (1.5 T) orwith a gradient-recalled echo. How-ever, the observed activation-inducedchange in signal intensity is consider-ably smaller with spin-echo than with

POST. gradient-recalled-echo techniques.The inherently small contrast-to-noiseratio makes functional imaging withspin-echo techniques particularlychallenging at i.5 T. The implicationsfor clinical applications of functionalMR imaging are obvious. Few siteswill ever have 4-T whole-body imag-ers. Therefore, clinical applicationswill likely be investigated at 1.5-2.0 Twith use of techniques (ie, gradientecho) that favor visualization of veinsrather than capillaries. This is a prob-lem, however, only if the functionalresolution of the MR technique is toocoarse for the clinical task. In viewingthe functional images of patient 1,particularly those in Figure 3b, it oc-curred to us that the activation signalintensity might partially or com-pletely represent the large central sul-cus vein seen on the patient’s preop-

erative angiogram. However, whenthe morphology of the central sulcus

vein (Fig 9) is compared with that ofthe activation signal intensity in Fig-ure 3, a clear difference can be seen.We therefore conclude that while theactivation signal intensity in Figure 3

Page 6: Sensory Motor Cortex: Correlation of Presurgical Mapping ... · motor cortex wasperformed intwo women, aged 24and38years. Both hadintractable, simple partial motor seizures duetotumors

a. b.

Figure 7. Patient 1. (a) In CT scan with recording strips in place, the individual electrode

contacts in strips A, B, and C can be seen over the left vertex. (b) Lateral view with the

patient’s head rotated slightly downward. The brain surface is rendered as a partially trans-parent object. The tumor is rendered in green, and that portion of the tumor that is at thebrain surface appears brighter than the portion of the tumor that is deep to the brain surface.The eight individual electrode contacts of each of the four subdural strips are rendered asseparate red objects. Strips A, B, C, and D are labeled as they are in Figure 5 and Figure 6. The

central sulcus is shown by means of cortical stimulation to lie between strips A and B. There-fore, the tumor straddles the inferior portion of the central sulcus. Correlation of this imagewith that in Figure 3 confirmed the relationship between the localization of function on thecortical surface with functional MR imaging and that obtained with invasive recording.

90 #{149}Radiology January 1994

Figure 6. Patient 1. Intraoperative photographs. After stereotaxic localization, a small burr hole was drilled directly over the tumor. (a) Corti-cal surface prior to placement of the recording strips and (b) strips on the cortical surface for comparison with Figure 5. The strips are labeled A,

B, C, D as in Figure 5. Note only the most inferior electrode of the three vertical strips and electrodes 4, 5, and 6 of the horizontal strip are vis-

ible in the operative field, because the strips have been slipped beneath the dura beyond the craniotomy. For purposes of orientation, the

patient’s nose is on the reader’s left, the top of the image is the superior part of the head, the electrodes in strip D overlie the sylvian fissureand the inferior pant of the frontoparietal operculum. (c) The cortex after the tumor has been removed. The most inferior portion of the tumorwas entered and the surgical plane extended superiorly beneath the brain surface. From this picture it is difficult to appreciate the entire extentof tumor removal, as the superior portion of the operative bed is concealed beneath undisturbed cerebral cortex. In comparison with Figure 9,note the tumor lies in the base of a U-shaped vein that extends in a cephalic direction, beneath the superior portion of the craniotomy flap.

may in part represent the effects ofvolume averaging of the superficiallylocated central sulcus vein, it is morelikely a result of signal in small veinsin the deeper banks of the central sul-cus that lie directly adjacent to theactivated cortex.

The method employed here to gen-erate functional MR images involvedsimple addition and subtraction of thetime-course images. A drawback ofthis approach is that motion (brain orblood pulsation or bulk head motion)during data acquisition will tend tocorrupt what is already a procedurewith low signal-to-noise ratio. Thenmlike high-intensity artifacts at thebrain surface in Figures 3b and 8bdemonstrate this problem. Pulsatilemotion of cerebrospinal fluid-whichis probably not a major problem inthe images discussed herein becauseof the radio-frequency spoiling andlarge flip angle-will also corrupt

functional images obtained with tech-niques that produce a high signal in-tensity in cerebrospinal fluid. Severalattempts at producing functional MRimages in patient 2 failed to show anyobvious result, probably because ofhead motion during serial image ac-

quisition. More sophisticated imageprocessing procedures have been pro-posed such as t test or z maps de-signed to minimize these artifacts(22). A most promising approach by

Bandettini et al (23) involves pixel-by-pixel thresholding according to the

cross correlation between the shape

of the time-course image data andthat of the stimulus cycle.

Presurgical mapping of the sensori-motor cortex is an appealing clinicalapplication of functional MR imaging.To our knowledge, results of func-

tional MR studies published to datehave not included rigorous physi-ologic correlation between presumedfunctional localization with functionalMR imaging and actual localizationwith established invasive recordingtechniques. Surgery for epilepsy nearfunctionally essential cortical areas isone of the few instances in which di-rect invasive brain mapping is mdi-

cated clinically, thus providing a

unique opportunity for verifying thephysiologic truth of functional MRimaging. Because this procedure isrelatively uncommon (even in centers

with a large volume of epilepsy sur-gery), experience with this correlation

will accumulate slowly on a case-by-case basis. The two cases presented

herein preliminarily support the fidel-ity of functional MR imaging in local-

izing the sensory motor cortex. Theprobable localization of the activation

signal in small cortical veins (versus

capillaries) does not appear to ham-

per this application significantly. Prior

to widespread performance of func-tional MR imaging for this or otherclinical uses, its accuracy must be vali-

dated against that of standard meth-

Page 7: Sensory Motor Cortex: Correlation of Presurgical Mapping ... · motor cortex wasperformed intwo women, aged 24and38years. Both hadintractable, simple partial motor seizures duetotumors

active

0/2

h’:, .

:� �

� :s� . �

Image Number

a. c.

Figure 8. Patient 2. Functional MR imaging study. (a) Coronal scout image with oblique axialplanes cross referenced. (b) Images were obtained in section location 2. At top left is an ob-

liquely oriented Ti-weighted image through the tumor. Posterior (POST), superior (SUP),

and inferior (INF) are indicated for orientation. Functional image at top right, obtainedthrough the same section location as the Ti-weighted map shows a hand movement activa-lion task. A small S-shaped area of activation (arrow at top right) is seen in the posteroinferioraspect of the image, corresponding to hand activation. The middle and lower panel demon-

strate a linked cursor display. The intersection of the cross hairs in the Ti-weighted image con-responds to the same spatial coordinates in the adjacent functional image. These demonstrate

that the S-shaped area of functional activation is centered on a sulcus (the central sulcus) that

is located posterior and inferior to the tumor. On the basis of findings in the functional MR

imaging study, we predicted that the primary motor cortex was located posterior to the tu-mor. (c) Time course plot of signal intensity in region of interest defined manually in the sen-sonimotor area in b. This was a single inactive-active cycle, as the patient had difficulty with

head motion.

b.

Volume 190 #{149}Number 1 Radiology #{149}91

Figure 9. Patient 1. Angiograms. (a) A lucent area (arrow) is seen in the midportion of the plain skull angiogram. (b) The venous phase of the

angiogram demonstrates that this lucency is located precisely in the anteroinfenior aspect of a U-shaped draining cortical vein (arrows). (c) Asubtraction angiogram demonstrates the central cortical vein more clearly (arrows). Proof of the anatomic relationship between the tumor and

this vein is obtained by comparing the shape of this vein in the angiogram with the shape of the draining vein that hugs the inferior aspect of

the tumor in the intraoperative photographs of Figure 6. In turn, by comparing the shape of the vein with the curvilinear shape of the area of

functional activation in Figure 3, one can see that although they are both located in the central sulcus, there is only a moderate physical corre-spondence between the two. The shape of the functional activation (Fig 3) is more complex and follows the curving contour of the portion ofthe central sulcus that lies deep to the surface. In contrast, the large central sulcus vein is less convoluted and lies on the brain surface.

ods of brain mapping. The cases re-

ported herein illustrate a paradigmfor performing these necessary vali-dation studies. Because subdural re-cording grids or strips often lie par-tially under intact skull and may shift

position during surgery, accurate in-traoperative assessment of electrode

position is difficult. Therefore, thefunctional-anatomic link betweenfunctional MR imaging and direct re-cording demonstrated in Figures 3and 7 is particularly useful. #{149}Acknowledgments: The authors thank BrendaMaxwell and Cindy Pfremmer of Mayo Bio-

medical Imaging Resource for manuscript typ-ing.

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