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(Radiology. 1999;210:529-538.)
© RSNA, 1999

Neuroradiology

Presurgical Evaluation of the Motor Hand Area with Functional MR Imaging in Patients with Tumors and Dysplastic Lesions

Eric Achten, MD, PhD2,1, Graeme D. Jackson, MD, PhD1,4, Julie A. Cameron, MD2, David F. Abbott, PhD1, Damien L. Stella, MD2 and Gavin C. A. Fabinyi, MD3

1 Brain Imaging Research Institute (E.A., G.D.J., D.F.A.)
2 Departments of Radiology (J.A.C., D.L.S.)
3 Neurosurgery (G.C.A.F.)
4 Neurology (G.D.J.), Austin and Repatriation Medical Centre, Studley Rd, Heidelberg 3084, Victoria, Australia.


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To test an optimized functional magnetic resonance (MR) imaging procedure to depict the motor hand representation area (HRA) in patients with epilepsy lesions near the central sulcus.

MATERIALS AND METHODS: Fast low-angle shot MR imaging was performed with an oblique single-section imaging technique in eight control subjects (10 hemispheres) and six patients (12 hemispheres). Three series of five activation images (obtained while subjects performed repetitive finger-to-thumb opposition movements) and five rest images were acquired. Each hemisphere was studied in three adjacent sections. Difference maps (obtained with simple subtraction between activation and rest images) were compared with t-test maps.

RESULTS: In control subjects, the HRA was visible in 27 of 30 sections. Qualitatively, activation was seen better on t-test maps in 14 and on difference maps in four of these sections. In all patients, motor activation could be seen in the hemisphere that contained the lesion. This activation was considered normal in four patients. In two patients, the HRA was deformed. Functional MR imaging activation in the motor area was confirmed with Penfield stimulation in five patients.

CONCLUSION: Functional MR imaging findings in the preoperative assessment of dysplastic lesions around the central sulcus are the same as for tumors. t-test maps are superior to difference maps in the treatment of motor functional MR imaging data.

Index terms: Brain, function, 13.121416, 13.91 • Brain neoplasms, MR, 13.12149 • Epilepsy, 13.30, 13.75 • Magnetic resonance (MR), 13.91


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
During surgical planning for patients with lesions in the frontal and parietal lobes, it is important to map the proximity or involvement of the primary motor and sensory cortices (1). Because these eloquent areas border the central sulcus, detection of this anatomic structure is also of prime importance (2). The central sulcus can be identified on anatomic grounds, but high interobserver variability has been reported (3). Pathologic conditions such as tumors might alter the location of the central sulcus and the related eloquent areas (4), and, in cases of dysplasia, trauma, or ischemia, the eloquent zones for certain functions may be shifted to other brain areas (5). Surgical exploration of such lesions to alleviate associated intractable epilepsy requires knowledge of the location of bordering brain functions to provide a better outcome—preferably without neurologic deficit (1,2,6–8).

In 1937, Penfield and Boldrey (1) described a method of direct electric cortical stimulation to map areas connected to function. This work resulted later (9) in the well-known sensorimotor homunculus. More recently, noninvasive functional magnetic resonance (MR) imaging relying on blood oxygen level–dependent, or BOLD, contrast was introduced (10–16) to depict functional brain tissue. Because the signal intensity differences between activated and nonactivated states are very small and other sources of signal variation are present (17,18)—for example, brain pulsation, cerebrospinal fluid (CSF) pulsation, and involuntary motion—relating signal intensity changes to paradigm timing by using statistical methods has improved the selectivity of activated brain lesions over that with simple subtraction techniques (19).

Several studies have addressed the beneficial use of functional MR imaging presurgically to identify the central sulcus and eloquent cortex (20–30) in patients with tumors or arteriovenous malformations (25,29). Five studies (20,22,23,27,28) investigated tumor proximity to the central sulcus and compared the functional MR imaging localization of the motor cortex to findings of invasive cortical stimulation. A general conclusion was that noninvasive preoperative mapping of the eloquent cortex allowed for a better-prepared surgical approach and better patient information. We could find no reference in the current medical literature (Medline database; National Library of Medicine, National Institutes of Health, U.S. Department of Health and Human Services, Bethesda, Md, 1997) on the role of functional MR imaging in the management of dysplastic lesions.

To incorporate functional MR imaging as a routine clinical protocol on a system without echo-planar imaging capabilities and to help in surgical planning, we tested a simple standardized finger-to-thumb opposition paradigm for functional MR imaging in control subjects by using the oblique section orientation (16) to depict the primary motor hand representation area (HRA) in the contralateral hemisphere. Patients with complex partial epilepsy due to dysplastic lesions and tumors near the central sulcus were examined by using this protocol in conjunction with brain stimulation before surgery.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Eight control subjects with neurologically normal findings (four men, four women; mean age ± SD, 35 years ± 18) and six patients with intractable complex partial seizures (Table 1), two with a tumor in the frontal lobe and four with suspected dysplastic lesions near the central sulcus, underwent functional MR imaging for the purpose of depicting the motor HRA and the central sulcus. All subjects gave informed consent after the nature of the procedure had been fully explained. The procedure described was approved by the institutional review board.


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  		TABLE 1. Patient Diagnostic and Therapeutic Data
 
After the extensive preoperative work-up, including neuropsychologic testing, video-electroencephalography, MR imaging, functional MR imaging, positron emission tomography, and single photon emission computed tomography (SPECT), all patients were selected for elective surgery. In five of the six patients, this was preceded by the positioning of subdural electrode strips over the lesion for electric cortical stimulation to detect a nearby eloquent cortex. The lesions served as a reference landmark for comparing the functional MR imaging findings and the cortical stimulation findings. One patient underwent biopsy guided with the Stealth frameless stereotaxic technique (Stealth Technologies, Marine, Ill).

MR Imaging
MR imaging was performed with a clinical system without echo-planar imaging capacity at 1.5 T (Magnetom SP4000; Siemens Medical Systems, Erlangen, Germany) by using a standard quadrature head coil. To optimize the magnetic field homogeneity for the functional MR imaging study, automated global head shimming was performed before imaging. T1-weighted scout images (300/10 [repetition time msec/echo time msec], 192 x 256 matrix, two signals acquired, 250-mm field of view, 5-mm section thickness) were acquired in the sagittal plane, and coronal T1-weighted scout images (300/10, 192 x 256 matrix, two signals acquired, 250-mm field of view, 5-mm section thickness) were subsequently acquired at the approximate level of the central sulcus. For the functional MR imaging studies, we used an oblique section position tangential to the central sulcus for a more extensive view of the brain structures around the central sulcus (Fig 1). To attain appropriate section positioning for functional MR imaging, a series of anatomic T1-weighted images (300/10, 192 x 256 matrix, two signals acquired, 250-mm field of view, 5-mm section thickness) was acquired parallel to the line from the superior sagittal sinus to the sylvian fissure at the approximate level of the central sulcus (Fig 1). After viewing the oblique T1-weighted images, three optimal sections for functional MR imaging were selected (Fig 1). Single-section functional MR imaging was performed by using an unspoiled fast low-angle shot (FLASH) sequence (91/60, 40° flip angle, 28-Hz-per-pixel bandwidth, 64 x 128 matrix, two signals acquired, 250-mm field of view, 5-mm section thickness). The acquisition time was 7 seconds per image, and a delay was chosen such that an image was acquired every 9 seconds during the paradigm testing.



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  		Figure 1a. Localizing the sections for functional MR imaging. (a) Coronal T1-weighted localizer MR image (300/15). (b–d) Three oblique T1-weighted localizer images (300/15) from which (b) superficial to (d) deep oblique sections for functional MR imaging were selected. b–d were acquired parallel to the line from the superior sagittal sinus to the sylvian fissure at the approximate level of the central sulcus (16). Note that the central sulcus (arrowheads) and the motor HRA (arrow) can easily be seen in b–d.

 


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  		Figure 1b. Localizing the sections for functional MR imaging. (a) Coronal T1-weighted localizer MR image (300/15). (b–d) Three oblique T1-weighted localizer images (300/15) from which (b) superficial to (d) deep oblique sections for functional MR imaging were selected. b–d were acquired parallel to the line from the superior sagittal sinus to the sylvian fissure at the approximate level of the central sulcus (16). Note that the central sulcus (arrowheads) and the motor HRA (arrow) can easily be seen in b–d.

 


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  		Figure 1c. Localizing the sections for functional MR imaging. (a) Coronal T1-weighted localizer MR image (300/15). (b–d) Three oblique T1-weighted localizer images (300/15) from which (b) superficial to (d) deep oblique sections for functional MR imaging were selected. b–d were acquired parallel to the line from the superior sagittal sinus to the sylvian fissure at the approximate level of the central sulcus (16). Note that the central sulcus (arrowheads) and the motor HRA (arrow) can easily be seen in b–d.

 


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  		Figure 1d. Localizing the sections for functional MR imaging. (a) Coronal T1-weighted localizer MR image (300/15). (b–d) Three oblique T1-weighted localizer images (300/15) from which (b) superficial to (d) deep oblique sections for functional MR imaging were selected. b–d were acquired parallel to the line from the superior sagittal sinus to the sylvian fissure at the approximate level of the central sulcus (16). Note that the central sulcus (arrowheads) and the motor HRA (arrow) can easily be seen in b–d.

 
Paradigm
The motor task involved repetitive finger-to-thumb opposition. All fingers were used simultaneously. The active hand was positioned beside the body on the imager table to minimize involvement of other muscle groups. Before the subjects were positioned in the MR system, they were instructed how to keep their heads still and how to perform the finger-to-thumb opposition movements at a rate of approximately two per second. We did not monitor the rate of movement. The control subjects were all right-handed and exercised their dominant right hand while the left cortex was imaged. Two control subjects had both sides examined. In patients, the side of the brain with the lesion was examined while they exercised the opposite hand. In patient 5, activation ipsilateral to the hand movement (ie, in the normal hemisphere) was also examined, and in patients 4 and 5, activation of the contralateral normal side was also studied. Functional images were acquired in blocks of five control (rest) images followed by five activation images. Each cycle of five rest and five activation images took 90 seconds and was repeated three times. Three sections were studied, but in patient 5, additional ipsilateral activation and activation in the contralateral cortex were studied by using only two sections.

Data Treatment
The functional MR imaging data were transferred to a workstation, where they were analyzed by using software developed at our institution by one of the team (D.F.A.) by using IDL (Interactive Data Language; Research Systems, Boulder, Colo). The images were initially inspected for patient motion by using a stack display (Fig 2). The ordinate of each stack is the time axis, and the abscissa represents a predefined pixel row or column from the sequential images. The operator can move the cursor around in the original images and by clicking select the intersecting row and column. Conversely, clicking on a stack displays the corresponding image in the time series. When the head was immobile during the imaging procedure, straight vertical lines were seen in the space-time stacks. Physiologic motion such as brain pulsation or pulsation in vessels is visible as regular small-amplitude undulations in some parts of the stack display. Gross head movement shows as wobbling or discontinuous lines throughout the stacks (Fig 2).



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  		Figure 2a. Stack displays used to detect motion. The abscissa of the stack images is the pixel values of a predefined row (XZ) and corresponding column (YZ) selected interactively by putting a crosshair on any image in the functional MR imaging time series. The ordinate is the same pixel row and/or column from all the images in the time series. (a) Stack for the control subject in whom the images in Figure 3 were obtained. No movement was present; in the Z direction of the stack (ordinate), no wobbling or shift of lines is visible. (b) Stack for patient 3 shows wobbling and shifts (arrows) in the Z direction, an indication of unacceptable motion.

 


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  		Figure 2b. Stack displays used to detect motion. The abscissa of the stack images is the pixel values of a predefined row (XZ) and corresponding column (YZ) selected interactively by putting a crosshair on any image in the functional MR imaging time series. The ordinate is the same pixel row and/or column from all the images in the time series. (a) Stack for the control subject in whom the images in Figure 3 were obtained. No movement was present; in the Z direction of the stack (ordinate), no wobbling or shift of lines is visible. (b) Stack for patient 3 shows wobbling and shifts (arrows) in the Z direction, an indication of unacceptable motion.

 
The first image obtained immediately after a paradigm shift (from rest to activation or vice versa) was omitted from analysis to minimize the effect of the well-known time lag (14) between an alteration in the motor task and recordable activation or deactivation. An automatic floor-filtering procedure was then applied to remove pixels outside the brain. For the remaining pixels, two different algorithms were used to extract activation-induced signal intensity changes in control subjects. In the first algorithm, the difference method, the normalized signal intensity change Diffxy between activated and rest states for each pixel was calculated as

where xya is the active-phase value of the pixel with coordinates {x,y} and xyr is the signal intensity of the same pixel during rest. Difference maps were displayed by using a color scale that depicted differences from 0% as blue to 8% as yellow (Fig 3a). The difference maps were then overlaid onto the corresponding anatomic T1-weighted image with a cutoff at 2%, seen as green (Fig 3b). The second data treatment consisted of a Student t test. A single-tailed (positive) t statistic was calculated for each pixel to discriminate between activated and rest states. Because the first image obtained after each paradigm shift was discarded, 12 data points in each state were compared. Subsequently, t-test maps were depicted in a color scale ranging from a t of 0, seen as black, to a t of 8, seen as yellow (Fig 3c) and were overlaid on the anatomic T1-weighted image by using a cutoff at a t of 2.75, seen as green (Fig 3d). For the number of sections used, a t greater than 2.75 corresponded to a P value of less than .006 (without correcting for multiple comparisons). The brain area was typically about 3,000 pixels, so at this threshold one might reasonably expect to see about 18 isolated single-pixel false-positive activations randomly distributed on the resultant t-test map. The number of active pixels (t > 2.75) was calculated on the t-test maps only around the central sulcus and in the HRA by using a simple region of interest that included either of these structures. The central sulcus was included for the whole length that it could be seen (Table 2).



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  		Figure 3a. Typical results of the analysis: difference maps and t-test maps. (a–c) T1-weighted axial oblique localizer images (300/15) obtained in a control subject overlaid with color-coded and thresholded (difference > 2%) difference maps at three consecutive levels from superficial to deep. (d–f) T1-weighted axial oblique localizer images (300/15) overlaid with color-coded and thresholded (t > 2.75) t-test maps. Typical artifacts in a–c are the important edge phenomena due to CSF pulsation (solid arrows) and the more prominent spurious covariance of unrelated pixels (arrowheads). Note the omega-shaped (open arrow in a–f) motor HRA, with an excellent depiction of the same in e. Three sections were sufficient to include all the activated pixels in the HRA.

 


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  		Figure 3b. Typical results of the analysis: difference maps and t-test maps. (a–c) T1-weighted axial oblique localizer images (300/15) obtained in a control subject overlaid with color-coded and thresholded (difference > 2%) difference maps at three consecutive levels from superficial to deep. (d–f) T1-weighted axial oblique localizer images (300/15) overlaid with color-coded and thresholded (t > 2.75) t-test maps. Typical artifacts in a–c are the important edge phenomena due to CSF pulsation (solid arrows) and the more prominent spurious covariance of unrelated pixels (arrowheads). Note the omega-shaped (open arrow in a–f) motor HRA, with an excellent depiction of the same in e. Three sections were sufficient to include all the activated pixels in the HRA.

 


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  		Figure 3c. Typical results of the analysis: difference maps and t-test maps. (a–c) T1-weighted axial oblique localizer images (300/15) obtained in a control subject overlaid with color-coded and thresholded (difference > 2%) difference maps at three consecutive levels from superficial to deep. (d–f) T1-weighted axial oblique localizer images (300/15) overlaid with color-coded and thresholded (t > 2.75) t-test maps. Typical artifacts in a–c are the important edge phenomena due to CSF pulsation (solid arrows) and the more prominent spurious covariance of unrelated pixels (arrowheads). Note the omega-shaped (open arrow in a–f) motor HRA, with an excellent depiction of the same in e. Three sections were sufficient to include all the activated pixels in the HRA.

 


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  		Figure 3d. Typical results of the analysis: difference maps and t-test maps. (a–c) T1-weighted axial oblique localizer images (300/15) obtained in a control subject overlaid with color-coded and thresholded (difference > 2%) difference maps at three consecutive levels from superficial to deep. (d–f) T1-weighted axial oblique localizer images (300/15) overlaid with color-coded and thresholded (t > 2.75) t-test maps. Typical artifacts in a–c are the important edge phenomena due to CSF pulsation (solid arrows) and the more prominent spurious covariance of unrelated pixels (arrowheads). Note the omega-shaped (open arrow in a–f) motor HRA, with an excellent depiction of the same in e. Three sections were sufficient to include all the activated pixels in the HRA.

 


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  		Figure 3e. Typical results of the analysis: difference maps and t-test maps. (a–c) T1-weighted axial oblique localizer images (300/15) obtained in a control subject overlaid with color-coded and thresholded (difference > 2%) difference maps at three consecutive levels from superficial to deep. (d–f) T1-weighted axial oblique localizer images (300/15) overlaid with color-coded and thresholded (t > 2.75) t-test maps. Typical artifacts in a–c are the important edge phenomena due to CSF pulsation (solid arrows) and the more prominent spurious covariance of unrelated pixels (arrowheads). Note the omega-shaped (open arrow in a–f) motor HRA, with an excellent depiction of the same in e. Three sections were sufficient to include all the activated pixels in the HRA.

 


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  		Figure 3f. Typical results of the analysis: difference maps and t-test maps. (a–c) T1-weighted axial oblique localizer images (300/15) obtained in a control subject overlaid with color-coded and thresholded (difference > 2%) difference maps at three consecutive levels from superficial to deep. (d–f) T1-weighted axial oblique localizer images (300/15) overlaid with color-coded and thresholded (t > 2.75) t-test maps. Typical artifacts in a–c are the important edge phenomena due to CSF pulsation (solid arrows) and the more prominent spurious covariance of unrelated pixels (arrowheads). Note the omega-shaped (open arrow in a–f) motor HRA, with an excellent depiction of the same in e. Three sections were sufficient to include all the activated pixels in the HRA.

 

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  		TABLE 2. Activated Volumes Measured in t-Test Maps Around the Central Sulcus and at the HRA in Eight Healthy Control Subjects
 
In a consensus reading, the difference and t-test maps in control subjects were qualitatively compared by two observers (E.A., J.A.C.) for the presence and conspicuity of HRA activation, activation along the venous outflow in the central sulcus, activation outside the central sulcus area—for example, the supplementary motor cortex and sensory cortex, spurious activation, and CSF pulsation (Table 3). For the patients, only t-test maps were calculated, and evidence was provided for the position of the central sulcus and the HRA with respect to the lesions.


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  		TABLE 3. Functional MR Imaging Features in Healthy Control Subjects: Section-by-Section Comparison of Difference Maps and t-Test Maps
 

   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Control Subjects
Table 3 shows the combined results of the analysis of the activation maps in control subjects, with emphasis on the differences between the difference maps and the t-test maps.

Qualitative and quantitative activation in the HRA.—The HRA was visible in 27 of the 30 sections studied and in all 10 hemispheres. Activation of the HRA was appreciated on both difference maps and t-test maps. In 14 of the 27 sections where the HRA was activated, the qualitative demonstration of the activation was considered better on the t-test maps than on the difference maps (Table 3), and in only four of the 27 sections was it slightly better on the difference maps. In all 10 hemispheres, the HRA was shaped like an omega (22,32) (Fig 3). The intensity of activation expressed as an activated volume varied widely (Table 2). Roughly half the activation around the central sulcus (2.02 mL ± 1.23 [mean ± SD) was found in the HRA (1.10 mL ± 0.49); the remainder was due to venous outflow or spurious activation in single pixels or small groups of pixels in the border of the central sulcus.

Concomitant focal activation seen in the supplementary motor area.—In two of the 30 sections (two of 10 hemispheres), activation was seen in the medial aspects of the superior frontal gyrus, which were believed to be the supplementary motor area. In one case, it was seen only on the t-test maps.

Coactivation of the sensory cortex.—In eight of the 30 sections (four of the 10 hemispheres studied), activation was seen in the sensory cortex at the level of the HRA. Both analytic techniques yielded similar results in depicting this functional zone, with two activations seen better on the difference maps and one seen better on the t-test maps.

Venous outflow visualization.—Activation was sometimes transported to the larger venous outflow channels, which drain the blood of the HRA into the superior sagittal sinus. In five of the 10 hemispheres (eight of the 30 sections), covarying signal intensity changes along the central sulcus were present toward the superior sagittal sinus and were believed to represent such "transported activated blood." A possible contribution of upper arm and shoulder muscles in finger-to-thumb opposition tasks to support the moving fingers could not be excluded. In one control subject, a two-dimensional time-of-flight MR angiogram confirmed the presence of a large cortical vein.

Artifacts due to CSF pulsation, physiologic motion, and system noise.—Gross deleterious head motion did not degrade any of the studies in control subjects. Two major forms of artifacts were recognized on the functional maps: CSF pulsation and spurious activation, defined as activation seen in small groups of pixels in unrelated areas or at particular high t values in isolated single pixels. The t-test maps were in general much less subject to the effects of physiologic or involuntary motion (Table 3). All difference maps showed CSF pulsation artifacts in the borders of the images (Fig 3), while this degraded functional images only minimally in five of the 30 sections on t-test maps.

Spurious activation, defined as activation in single pixels or small groups of pixels in areas outside the expected motor area, was found in 19 of the 30 sections studied. This was always more apparent on the difference maps. We presume that this resulted from minimal head motion or gradient noise, because in none of the normal images could any obvious brain motion be detected by using the stack display. Superior sagittal sinus pulsations were sometimes seen in the stack display as an undulating line in the time direction with a regular frequency. This did not result in any statistically significant covariance on the t-test maps and was projected in the CSF pulsation artifact band on the difference maps.

Patients
All six patients had complex partial epilepsy refractory to medication; four were suspected to have lesions on the right side; two, on the left side. On the basis of clinical and electrophysiologic data, the seizures originated in the vicinity of the lesions. On MR images, two had a tumor and three revealed possible dysplastic lesions (Table 1). A last patient had normal MR imaging findings, but a left-side frontoparietal hot spot was found by using ictal technetium 99m hexamethyl-propyleneamine oxime, or HMPAO, SPECT, which suggested cryptogenic dysplasia.

Because activation was better appreciated on the t-test maps in control subjects and the t-test maps were clearly less sensitive to physiologic motion or gradient noise, only t-test maps were calculated and analyzed for the patients. Activation in the HRA was seen in all hemispheres on the side of the lesion, but a large quantitative variability well in the range depicted by normal hemispheres was present (Table 4).


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  		TABLE 4. Activated Pixels and Volumes
 
Patients with a tumor.—In patient 4, who had a tumor and arm weakness due to the lesion, the central sulcus was clearly elongated and the precentral gray matter was stretched and thinned (Fig 4). The other patient with a tumor, patient 3, had no neurologic deficit, and the position and shape of the central sulcus and HRA were unchanged. Results of electric cortical stimulation after grid positioning (Table 5) over the tumor corroborated the functional MR imaging localization of the central sulcus and HRA in patient 3, and the tumor was removed. Because functional MR imaging showed that the HRA was deformed by and positioned too closely to the tumor in patient 4, a large craniotomy and open biopsy were performed with frameless stereotactic guidance (Stealth; Stealth Technologies). The integration of functional data and anatomy allowed the surgeon (G.C.A.F.) to stay well clear of the motor strip. No additional functional deficit was present in either of these patients after the operation.



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  		Figure 4a. Patient 4. Displacement of the central sulcus by a tumor adjacent to the precentral gyrus in the right hemisphere. (a) T1-weighted axial image (13/15) shows that the central sulcus and the adjoining cortex (arrow) are stretched and slightly displaced. (b–d) T1-weighted axial images (300/15) show that the activation of the HRA (arrow) is stretched as well but is present in the expected area. The proximity of the tumor to the eloquent cortex was confirmed with Penfield stimulation. Superficial to deep levels are shown in b–d. Only biopsy was performed; the lesion was classified as astrocytoma grade II.

 


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  		Figure 4b. Patient 4. Displacement of the central sulcus by a tumor adjacent to the precentral gyrus in the right hemisphere. (a) T1-weighted axial image (13/15) shows that the central sulcus and the adjoining cortex (arrow) are stretched and slightly displaced. (b–d) T1-weighted axial images (300/15) show that the activation of the HRA (arrow) is stretched as well but is present in the expected area. The proximity of the tumor to the eloquent cortex was confirmed with Penfield stimulation. Superficial to deep levels are shown in b–d. Only biopsy was performed; the lesion was classified as astrocytoma grade II.

 


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  		Figure 4c. Patient 4. Displacement of the central sulcus by a tumor adjacent to the precentral gyrus in the right hemisphere. (a) T1-weighted axial image (13/15) shows that the central sulcus and the adjoining cortex (arrow) are stretched and slightly displaced. (b–d) T1-weighted axial images (300/15) show that the activation of the HRA (arrow) is stretched as well but is present in the expected area. The proximity of the tumor to the eloquent cortex was confirmed with Penfield stimulation. Superficial to deep levels are shown in b–d. Only biopsy was performed; the lesion was classified as astrocytoma grade II.

 


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  		Figure 4d. Patient 4. Displacement of the central sulcus by a tumor adjacent to the precentral gyrus in the right hemisphere. (a) T1-weighted axial image (13/15) shows that the central sulcus and the adjoining cortex (arrow) are stretched and slightly displaced. (b–d) T1-weighted axial images (300/15) show that the activation of the HRA (arrow) is stretched as well but is present in the expected area. The proximity of the tumor to the eloquent cortex was confirmed with Penfield stimulation. Superficial to deep levels are shown in b–d. Only biopsy was performed; the lesion was classified as astrocytoma grade II.

 

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  		TABLE 5. Morphology and Activation at Functional MR Imaging according to Grid Position and Excision
 
Patients with dysplastic lesions.—In two patients (patients 1 and 2) with suspected cortical dysplasias and in one (patient 6) with normal MR imaging findings but with an ictal hot spot at SPECT, the HRA on the side of involvement was readily detected with functional MR imaging and appeared normal. Findings of cortical stimulation confirmed that resection could be performed without touching the eloquent cortex (Table 5). Patients 1, 2, and 6 underwent partial lobectomy guided with MR imaging and results of the functional tests. None of these patients had a neurologic deficit after the operation. In patient 1, resection did not improve the epilepsy. The pathologist described mild dysplastic changes in the resected tissue.

In one patient suspected to have dysplasia (patient 5), the central sulcus on the side of the lesion was deformed so that it could not be recognized on the oblique localizer images with certainty. Upon left-hand finger movement, motor activation in the right hemisphere was believed to be present in two distinct spots bordering the lesion (Fig 5) and also in the sensory cortex and the superior parietal lobule (Brodmann areas 5 and 7 [33,34]). The latter area was also activated in the ipsilateral hemisphere (not shown). Movement of the right hand resulted in activation in a normal HRA in the left precentral cortex. Cortical stimulation showed a complex and deformed motor representation (right HRA) of the left hand in the border of the lesion, as predicted at functional MR imaging. Therefore, only partial lesion resection was performed with reference to the findings of functional MR imaging and cortical stimulation (Table 5). This resulted in an improvement of the hand function (less spasticity) on the left side and in a worthwhile improvement in seizure activity.



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  		Figure 5a. Patient 5. Alteration of the HRA by a dysplastic lesion in a patient with intractable epilepsy. (a) T2-weighted axial (3,287/90) and (b) T1-weighted coronal (3,150/27/300 [repetition time msec/echo time msec/inversion time msec]) images clearly show a dysplastic lesion (arrow) in the right frontal lobe. The central sulcus is deformed and difficult to identify. (c, d) Functional MR images (600/15; 40° flip angle) show motor activation (solid arrow) at two locations in the border of the lesion. Activation of the sensory cortex (open arrow in d) at the level of the hand and activation in the posterior parietal cortex (Brodmann areas 5 and 7) were prominent. These activations were confirmed by means of Penfield stimulation.

 


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  		Figure 5b. Patient 5. Alteration of the HRA by a dysplastic lesion in a patient with intractable epilepsy. (a) T2-weighted axial (3,287/90) and (b) T1-weighted coronal (3,150/27/300 [repetition time msec/echo time msec/inversion time msec]) images clearly show a dysplastic lesion (arrow) in the right frontal lobe. The central sulcus is deformed and difficult to identify. (c, d) Functional MR images (600/15; 40° flip angle) show motor activation (solid arrow) at two locations in the border of the lesion. Activation of the sensory cortex (open arrow in d) at the level of the hand and activation in the posterior parietal cortex (Brodmann areas 5 and 7) were prominent. These activations were confirmed by means of Penfield stimulation.

 


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  		Figure 5c. Patient 5. Alteration of the HRA by a dysplastic lesion in a patient with intractable epilepsy. (a) T2-weighted axial (3,287/90) and (b) T1-weighted coronal (3,150/27/300 [repetition time msec/echo time msec/inversion time msec]) images clearly show a dysplastic lesion (arrow) in the right frontal lobe. The central sulcus is deformed and difficult to identify. (c, d) Functional MR images (600/15; 40° flip angle) show motor activation (solid arrow) at two locations in the border of the lesion. Activation of the sensory cortex (open arrow in d) at the level of the hand and activation in the posterior parietal cortex (Brodmann areas 5 and 7) were prominent. These activations were confirmed by means of Penfield stimulation.

 


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  		Figure 5d. Patient 5. Alteration of the HRA by a dysplastic lesion in a patient with intractable epilepsy. (a) T2-weighted axial (3,287/90) and (b) T1-weighted coronal (3,150/27/300 [repetition time msec/echo time msec/inversion time msec]) images clearly show a dysplastic lesion (arrow) in the right frontal lobe. The central sulcus is deformed and difficult to identify. (c, d) Functional MR images (600/15; 40° flip angle) show motor activation (solid arrow) at two locations in the border of the lesion. Activation of the sensory cortex (open arrow in d) at the level of the hand and activation in the posterior parietal cortex (Brodmann areas 5 and 7) were prominent. These activations were confirmed by means of Penfield stimulation.

 
Patient motion and artifacts.—Movement was hardly an issue in this study and ruined only two functional MR imaging sections in one of the patients with a tumor (patient 3); a third section that had no appreciable motion artifacts showed normal focal activation in the HRA, and the position of the central sulcus and HRA could be deduced with respect to the tumor. In this case, head movement was easily detected by inspecting the stack display, where a discontinuity of the lines in the time direction was noted (Fig 2). Spurious activation was present in small amounts on all t-test maps, but this was not a problem in the effort of depicting the HRA and the central sulcus.


   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Although several ways exist of using only anatomic landmarks to find the central sulcus in the normal brain on MR images (35,36), the surgeon is confronted with a different perspective. A limited craniotomy provides a limited view of the brain, and cortical stimulation is generally necessary to map eloquent functional zones with respect to resectable lesions. Noninvasive mapping gives the advantage of planning the approach in advance, and functional MR imaging is particularly helpful in cases where function might be shifted owing to disease or other focal abnormality (4,21,22). On the oblique axial sections used in our protocol, the topography of a larger part of the undistorted central sulcus could readily be recognized in all control subjects and in four of the six patients, but finding the activation in the HRA and relating it to the anatomic position of the lesions helped the surgeons in making important decisions related to approach and resectability.

Functional Activation and the Depiction of the HRA and Central Sulcus
The paradigm here has been used in many other studies (20–30) and is robust in producing activation in the motor cortex. In none of the control subjects or patients were we unable to detect HRA activation. We also confirm the presence of an omega-shaped structure in the precentral gyrus that corresponds to the somatotopic HRA (22,33). This knoblike structure could easily be spotted on the oblique sections and is situated just below the level of the end of the superior frontal sulcus (Fig 1). Brain activation related to the paradigm that we used was most consistent in this area, in patients and in control subjects. Although quantitatively diminished activation has been described in one study of tumor-bearing hemispheres (26), this was not found in our study. The findings of this study support the idea that functional MR imaging is useful in the management of tumors near the central sulcus.

The detection and surgical treatment of dysplastic lesions in the brain has taken a new élan because of improvements in detection with the use of MR imaging (32,34,37,38). Many patients with refractory epilepsy due to dysplasia can now be treated surgically. The use of functional MR imaging in the detection of the eloquent cortex before surgery in patients with dysplasia is not very different from its use in patients with tumors. The proximity of dysplastic lesions to these eloquent areas and the involvement with possible plasticity can be studied. Our understanding of the plasticity involved in dysplasia, however, is still in its early stage. In three of the patients with dysplastic lesions (patients 1, 2, and 6), only proximity was an issue, and the functional response to the paradigm was as it was in the normal hemispheres. The surgeons were reassured by this finding before the surgical procedure. HRA activation was distorted in the last patient with dysplasia (patient 5), and the option of partial resection was discussed with the patient before surgery. In all cases, the information from functional MR imaging opened up the possibility of discussing functional implications and possible risks before any intervention and was considered an advantage for both surgeons and patients alike.

Oblique Section Selection
In all mentioned clinical studies (21–30) except one (20), axial sections through both hemispheres were used. The use of oblique section orientation to study unilateral sensorimotor cortex activation, as opposed to plain axial section orientation, was, to our knowledge, first published by Connelly et al (16). It was stated that, while the axial plane is suitable for simultaneous examination of both left and right sensorimotor areas, oblique planes through one hemisphere were preferable for viewing more detailed functional anatomy because a larger part of the central sulcus and adjacent cortical areas were obviously present in one section. Oblique sections also offered a view similar to what the surgeon would see when opening the skull. This method has been used with success in one clinical study (20).

Using oblique sections disclosed several advantages. First, fewer sections were needed to depict the whole length of the cortex around the central sulcus. This is an advantage for systems that do not possess echo-planar imaging capabilities and use single-section techniques to study activation. Second, the correspondence of the omega-shaped structure in the precentral gyrus to the somatotopic HRA is very easily detected and recognized (22,33). Third, oblique sections are better in simulating the intraoperative views and help in presurgical planning for lesions (16,20).

Disadvantages might be that no contralateral information is present and sometimes the other side has to be studied separately, as in cases where a possible pre- or perinatal lesion responsible for intractable epilepsy could have caused the motor function of the contralateral hand or arm to be transposed to the ipsilateral side (4,39,40). This, however, can be solved by assessing possible ipsilateral activation in a sequential setting, at the expense of a longer time in the imager. Ipsilateral activation was studied in one patient (patient 5) because the lesion was bordering the anatomic HRA in a deformed precentral cortex and an abnormal activation pattern was seen. In this study, no ipsilateral activation of the primary motor cortex was found, but ipsilateral activation of the posterior parietal area (Brodmann areas 5 and 7) was present.

In the other patients with dysplasia, the anatomy of the central sulcus and the HRA and the functional MR imaging findings were normal on the pathologic side. In these patients, no ipsilateral activation was studied because it was concluded from the functional MR imaging data that surgical resection could remain clear of the primary motor cortex.

Quantification of the Activation
Quantification of the amount of activation showed a large variation in the activated volume or number of pixels. The amplitude of the response depends on factors such as movement rate, motivation, concentration, and coverage of the HRA (41,42). Coverage was considered complete because additional sections studied in a pilot study showed no deeper activation, and the most superficial section was the first to show cortex. No monitoring of the motor task was performed here, but instruction before the subject entered the magnet was such that a finger-to-thumb opposition was performed at approximately 2 Hz. Motivation and concentration on the task are extremely hard to assess, and no debriefing on these parameters was performed. The large variability may be an expression of all the aforementioned limitations of the study. In respect to the planned surgical procedure, quantification of the response was less important than localization of the HRA and the central sulcus, tasks that were performed with great precision by using our method.

Activation in Other Functional Areas
In two control subjects, activation was observed in the supplementary motor area. Pujol et al (28) have also reported inconstant activation of this area. Supplementary motor area visualization is in general more consistent with more complex motor tasks (43). In four control subjects, low-level activation was also found around the postcentral sulcus, in the primary sensory area. This coactivation of the sensory cortex is presumably due to the involvement of a sensory component in these subjects when the fingertips touch the thumb. In this study, the activation along the postcentral sulcus was always less than the motor activation in the HRA but projected at the same level.

In patient 5, the posterior parietal lobes were activated bilaterally during movement of the functionally impaired left hand. These areas (Brodmann areas 5 and 7) have functionality similar to the supplementary motor area but focus more on sensory aspects of motion (44,45). Because the supplementary motor area on the side of the lesion was dysplastic and the patient was hemiparetic, activation of these posterior parietal regions probably indicates the use of a complex strategy to move the fingers.

Transported Activation along the Venous Outflow
On some sections, activation was visible in the central sulcus connecting the HRA to the superior sagittal sinus and most probably corresponded to draining venous structures. This likely occurred because of the sequence used for functional MR imaging (46–48). The arm was not immobilized in a sling, and therefore other muscle groups, especially from the arm and shoulder, could be weakly activated by means of simple finger movement. This can also contribute to a more widespread activation seen along the central sulcus in some subjects.

Artifacts: Physiologic and Involuntary Head Motion
Several authors (20,24,28,29) have reported the degrading of functional studies by voluntary and involuntary motion. Jack et al (20) had motion-related problems with one of two patients with tumors, five of 17 patients in the study by Righini et al (24) moved too much, Pujol et al (28) reported a high failure rate of functional MR imaging experiments in four patients with epilepsy, and Maldjian et al (29) reported two of 23 failed studies in six patients. In only one patient (patient 3) in our study was movement noted to be deleterious to the detection of activation in the HRA in two sections (two of the 25 sections studied in patients). The stack display revealed the head movement as a disruption in the vertical straight lines. Nevertheless, activation in the HRA was unambiguously seen on the first section studied in this subject, and this was sufficient to predict the location of the central sulcus and motor cortex with respect to the tumor. We believe that the low number of failures in this study is in part due to good patient instruction and reasonably short session times (about 60 minutes), but that the patients were young, had chronic epilepsy, and had been in the MR imager several times before for long imaging protocols most likely also contributes to the high success rate.

Gross motion between the anatomic and functional studies can be a problem for coregistration. We did not assess whether such gross motion occurred between the acquisition of the anatomic images and the functional study. In the control subjects, the activated HRA pixels were always projected correctly on the anatomic images, and, in the patients who underwent Penfield stimulation, the activated areas corresponded to the stimulated areas. This means that gross motion between anatomic and functional studies was not a substantial problem in our work. In the future, though, and for the study of anatomic substrates of normal or abnormal function, we believe that this should be tested.

Data Treatment
Data treatment in this study again shows the advantage of a statistical method over simple subtraction of images (19). In approximately half the normal sections studied, t-test maps were better at depicting the site of the hand representation than were difference maps. The disadvantage of the subtraction technique is mainly due to large arbitrary signal intensity changes in areas of CSF and brain pulsation and the greater sensitivity to head motion–induced signal intensity differences. By using FLASH images with high CSF signal intensity, CSF pulsation artifacts occurred mainly at the border areas of the brain on difference maps.

In conclusion, the optimized protocol used in this study allows for robust activation of the motor HRA in control subjects and patients alike and provides useful information for the surgical preparation and management of lesions around the central sulcus. Statistical t-test mapping was superior to simple subtraction in the overall assessment of the functional MR imaging data. Findings of this study also imply that the problems to be addressed with, and answers to be given by, functional MR imaging of the motor cortex in patients with dysplastic lesions near the central sulcus are similar to those for patients with tumors.


   Footnotes
 
E.A.'s primary affiliation is with the Department of Radiology, University Hospital Gent, Belgium. Back

Address reprint requests to G.D.J.

Abbreviations: CSF = cerebrospinal fluid FLASH = fast low-angle shot HRA = hand representation area

Author contributions: Guarantor of integrity of entire study, G.D.J.; study concepts and design, E.A., G.D.J., D.F.A.; definition of intellectual content, E.A., G.D.J., D.F.A.; literature research, E.A., D.L.S.; clinical studies, G.D.J.; data acquisition, E.A., J.A.C., D.L.S., G.C.A.F.; data analysis, E.A., J.A.C., D.F.A.; statistical analysis, D.F.A.; manuscript preparation, E.A., J.A.C.; manuscript editing, E.A.; manuscript review, G.D.J., D.F.A.

Received November 5, 1997; revision requested January 22, 1998; revision received April 27, 1998; accepted August 10, 1998.
   References
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 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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