J Neurosurg 90:591Ð598, 1999

Integration of preoperative and intraoperative functional
brain mapping in a frameless stereotactic environment for
lesions near eloquent cortex
Technical note
JEFFREY D. MCDONALD, M.D., PH.D., BRIAN W. CHONG, M.D., JEFFREY D. LEWINE, PH.D.,
GREG JONES, PH.D., ROBERT B. BURR, PH.D., PAUL R. MCDONALD, B.SC.,
SPENCER B. KOEHLER, PH.D., JAY TSURUDA, M.D., WILLIAM W. ORRISON, M.D.,
AND M. PETER HEILBRUN, M.D.
Departments of Neurosurgery and Radiology, University of Utah School of Medicine, Salt Lake City,
Utah
U The authors present a method of incorporating preoperative noninvasive functional brain mapping data into the
frameless stereotactic magnetic resonance (MR) imaging dataset used for image-guided resection of brain lesions
located near eloquent cortex. They report the use of functional (f)MR imaging and magnetic source (MS) imaging for
preoperative mapping of eloquent cortex in difficult cases of brain tumor resection such as those in which there are
large expansive masses or in which reoperations are required and the anatomy is distorted from prior treatments. To
correlate methods of preoperative and intraoperative mapping localization directly, the authors have developed techniques of importing preoperative MS and fMR imaging data into an image-guided frameless stereotactic computer
workstation. The data appear as a seamless overlay on the same preoperative volumetric MR imaging dataset used for
stereotactic guidance during the operation. Intraoperatively identified functional locations mapped by cortical stimulation are recorded as digitally registered points. This approach should prove useful in assessing the accuracy and reliability of various preoperative functional brain mapping techniques.

KEY WORDS ¥ brain neoplasm ¥ electrocorticography ¥ functional brain mapping ¥
functional magnetic resonance imaging ¥ image-guided surgery ¥ magnetoencephalography

I

N patients with intracranial neoplasms or arteriovenous

malformations (AVMs) that require surgical resection,
these anomalies often are found to be adjacent to, or
within, a region of the brain that is critical for motor, sensory, or cognitive functioning. In these cases, it is important to know as much as possible about the local functional organization of the brain before surgery because this
can aid in planning the surgical approach and in defining
realistic goals and limits of lesion resectability. This information can also be of assistance in advising patients
regarding treatment risks and therapeutic options, such as
the choice of surgical resection or biopsy. Available data
such as standard magnetic resonance (MR) imaging anatomical landmarks3 and standard brain atlases provide
some general information about brain functional anatomical localization; however, differences between individual
patients can be significant.13,18 Also, in patients with large
intracranial masses, the local anatomy may be distorted so

J. Neurosurg. / Volume 90 / March, 1999

that it can be difficult to identify important neuroanatomical landmarks accurately, based on preoperative MR imaging alone.8,17,19
We have instituted a prospective multimodality regimen
of preoperative noninvasive functional brain mapping for
patients with brain tumors or AVMs near eloquent cortex.
The techniques used include magnetoencephalography
(MEG) and functional (f)MR imaging, as well as other
modalities. Magnetoencephalography detects minute regional alterations in magnetic flux associated with neuronal electrical activity related to a particular task.7 Using
mathematical models, the location of the neuronal generators of the specific signal components can be inferred. In
magnetic source (MS) imaging, MEG source locations
are plotted on spatially aligned MR images to produce
MS localization images. Magnetic source imaging analysis appears to be very promising for the accurate noninvasive mapping of motor and sensory areas, seizure focus
591

J. D. McDonald, et al.
identification, and, possibly, language localization.6,10,11
Functional MR imaging can be used to predict brain functional areas based on small regional alterations in blood
flow associated with neuronal activation and may be especially useful for identifying areas of motor and language
function.5,12 Direct cortical stimulation and recording techniques4,16 allow the surgeon to map specific areas of motor
cortex activation and, in the awake patient, specific cortical areas associated with reading or picture naming, expressive speech, and somatosensory cortex activation.
To correlate methods of preoperative and intraoperative
mapping localization directly, we have developed techniques of importing preoperative MS and fMR imaging
data into an image-guided frameless stereotactic computer
workstation. The data appear as a seamless overlay on
the same preoperative volumetric MR imaging dataset
used for stereotactic guidance during the operation. Intraoperatively identified functional locations mapped by
cortical stimulation are recorded as digitally registered
points. Direct cross-modality correlation and verification
of preoperative and intraoperative functional maps are
thus achievable within the frameless stereotactic working
environment. In this report we demonstrate the technical
feasibility and usefulness of this adjunct to functional
brain mapping through illustrative cases.
Description of Technique
Patients undergo MEG recording for which five to eight
surgical fiducial markers are placed on the scalp. A largearray whole-head 122-channel biomagnetometer is positioned over the head and a visual, auditory, somatesthetic,
motor, or dichotic listening task is presented to the patient
as appropriate for the location of the brain lesion. A multiple dipole spatial/temporal model is used to characterize MS locations for MS imaging.9 Neuromagnetic data
are recorded with a precise relationship to the anatomical
landmarks on the patientÕs head, which are defined via
a three-dimensional digitizer and fiducial markers. Data
analysis for MEG is performed using a software package
with overlay of MEG sources as slice data points onto an
anatomical volumetric T1-weighted MR image obtained
immediately following the MEG examination.
The choice of MR imaging parameters is determined by
the prerequisites of the image integration software. Image
integration of the preoperative functional mapping with
the anatomical MR imaging dataset is performed within
the frameless stereotactic workstation. It is a requirement
of the current software (version 2.6) that the volume datasets be generated from isotropic voxels (that is, data
points or voxels are the same dimension in the x, y, and z
planes, specifically 1 mm).
A three-dimensional volume gradient-echo sequence is
used to acquire the anatomical MR image (stereotactic
study) on one of two 1.5-tesla MR imaging systems (Picker or GE). Using the Picker MR imager, images are
obtained using the following parameters: a 15-msec repetition time (TR), a 4.47-msec echo time (TE), and one excitation; a 20û flip angle (FA); 200 contiguous slices measuring 1 mm each; a 256 3 256 matrix; and a 25.6-cm
field of view (FOV). Using the GE unit, the parameters
included: a 22-msec TR, minimum TE, and one excita592

tion; a 45û FA; 160 to 180 contiguous slices, each measuring 1 mm; a 256 3 256 matrix; and a 25.6-cm FOV.
The fMR image is obtained on the day after the MEG
examination. Data are acquired using the GE MR imager
with a multiphase, single-shot, gradient-echo evoked potential index image. Imaging parameters include: a 3000msec TR, 60-msec TE, and one excitation; a 90û FA; 5mm-thick slices with a 2-mm gap; six slice locations with
80 phases per location for a total of 480 sections; a 64 3
64 matrix; and a 25.6-cm FOV. For fMR imaging, the patient is presented with a visual, auditory, somatesthetic,
motor, language, or mnemonic stimulus task. Stimuli or
tasks are presented in alternating 30-second time periods
(for example, finger flexion alternating with a rest period)
time-locked to image acquisition. The functional data are
initially analyzed off line by using a Sun workstation
equipped with an image processing software package.
Data processing consists of pixel-by-pixel statistical analysis using either a temporal correlation between a reference waveform and the task-generated function, or an unpaired Student t-test in which images acquired during
performance of the task (for example, finger flexion) are
compared with images acquired during the alternating
condition (for example, rest).1,2 The reference waveform is
in the shape of a ÒboxcarÓ of alternating task conditions
with an initial 6-second delay, approximating the delay
between the task performance and the physiological response. Analysis is performed on the 64 3 64Ðpixel echoplanar images and a statistical threshold is set by using
either cross-correlation values or z-scores generated from
the unpaired Student t-test analysis. Statistical maps are
either overlaid directly onto the corresponding 256 3
256Ðpixel anatomical image or rendered via spatial transformation into the anatomical volume. The spatial transformation is calculated using the Automated Image Registration package within the Medx program.
Integration of preoperative functional mapping is performed within the StealthStation frameless stereotactic
workstation using the ImMerge software module. Briefly, the MS imaging dataset output from NeuroMag in
DICOM version 3.0 format is transferred via the computer network directly to the hard disk of the StealthStation
computer by using a conversion utility called ÒstorecpÓ
written within our department and a modification of the
DICOM Toolkit version 3.11 public domain software to
set the DICOM-formatted images on the hard drive. This
program also outputs the information manually to create
the required ÒattributesÓ file, containing pixel size, slice
thickness, FOV, and other volumetric information. The
DICOM images on the hard drive are converted into files
compatible with StealthStation software using a utility
written within our department entitled Òdicom2stax.Ó This
creates a stereotactic dataset that can be opened as the
ÒreferenceÓ dataset in ImMerge. We load our fMR imaging dataset, containing mapped functional points generated within Medx, as the ÒworkingÓ dataset in ImMerge.
The Medx output is currently not available in DICOM format and thus must be transferred by file transfer protocol
in isotropic Analyze format to the StealthStation. The ImMerge software scales and transforms the MS and fMR
imaging datasets into two-dimensionally matched volumes loadable into the cranial program of the StealthJ. Neurosurg. / Volume 90 / March, 1999

Integrated functional brain mapping
Station as ÒVolume IÓ and ÒVolume II,Ó respectively.
Merging of these two datasets is performed by following
standard ImMerge guidelines using anatomical landmarks, after which the merged functional dataset (containing both MS imagingÐ and fMR imagingÐmapped
points of function) is used in the operating room as the
stereotactic dataset.
The patient undergoes surgery within 1 to 4 days after
the preoperative functional brain mapping analysis has
been completed. Point-merge and surface-merge registration of the merged preoperative stereotactic MR imaging
datasets with the fiducial markers on the patientÕs scalp is
performed in the usual manner. Before biopsy or resection
of the lesion, the patient undergoes a craniotomy followed
by standard cortical stimulation for intraoperative mapping of language, sensory, and/or motor functional areas.
Cortical stimulation is performed using an Ojemann-type
bipolar current electrode (60 Hz, 1-msec pulse, 0.5Ð10mA current) according to methods previously described.16
During awake procedures, patients receive a continuous
infusion of propofol/remifentanyl. Continuous electroencephalography recording is performed during mapping to
monitor after-discharge potentials. When generalization
of after-discharge potentials is identified, immediate termination of these potentials is achieved by intravenous
administration of 50 to 100 mg of thiopental and/or cortical administration of ice-cold lactated RingerÕs solution,
as previously described.15
Areas of function that are intraoperatively mapped are
stored digitally within the StealthStation Surgical Plan
mode as Òtargets.Ó The direct correlation of these intraoperatively identified functional targets with the preoperative functional map can be performed quantitatively by
measuring the distance in millimeters between preoperatively and intraoperatively identified areas of identical
function (such as motor cortex localization of a finger
contraction task identified both preoperatively on fMR
imaging analysis and intraoperatively by motor cortex
stimulation). If similar, but not identical, functional tasks
are mapped preoperatively and intraoperatively (such as
leg somatosensory cortex identified preoperatively on MS
imaging and a distal leg motor contraction function identified intraoperatively by cortical stimulation, or hand
motor cortex identified with a finger flexion task on preoperative fMR imaging and an area of motor cortex identified by intraoperative stimulation with production of
complex handÐwrist flexion), then correlation across mapping modalities can be performed qualitatively by localization and mapping of the homunculus of the patientÕs
primary motor and somatosensory cortex.
Sources of Supplies and Equipment

The whole-head 122-channel biomagnetometer was obtained from NeuroMag Ltd. (Helsinki, Finland), as was
the NeuroMag software package. Two 1.5-tesla MR imaging systems were used in this study: the Picker Eclipse
Power Drive 250, available from Picker International
(Cleveland, OH), and the GE Signa Echo Speed, available
from General Electric Medical Systems (Milwaukee, WI).
The StealthStation frameless stereotactic (Silicon Graphics O2) workstation and StealthStation software (version
2.6) were purchased from Sofamor Danek USA (MemJ. Neurosurg. / Volume 90 / March, 1999

phis, TN) as was the ImMerge software module, which
was used with the workstation to integrate preoperative
functional mapping. Initial analysis of functional data was
performed using a Sun workstation obtained from Sun
Microsystems (Palo Alto, CA) equipped with the Medx
software package available from Sensor Systems Inc.
(Sterling, VA). Analyze software was obtained from CNSoftware (Wilmington, DE).
An Ojemann-type bipolar current electrode, manufactured by Radionics, Inc. (Burlington, MA), was used for
the cortical stimulation.
Illustrative Cases
Our experience to date with these techniques is summarized in Table 1. For the purposes of this technical report,
two illustrative cases are presented in more detail.
Case 1

This 25-year-old right-handed man experienced a single
generalized tonicÐclonic seizure.
Examination. The patient was neurologically intact on
referral to the neurosurgery service for consultation. Neuroimaging demonstrated a large lesion within, or just anterior to, the primary motor cortex. The anatomical MR
images were ambiguous with regard to the location of the
central sulcus, based on standard criteria (Fig. 1aÐd) and,
thus, preoperative functional analysis was performed to
assist in the assessment of the surgical risk of attempted
resection of the lesion. Functional MR imaging (Fig. 1e)
and MS imaging analysis (Fig. 2) produced discordant
results with respect to motor cortex identification.
Operation. We performed an awake craniotomy with
intraoperative cortical stimulation for definitive localization of primary motor and somatosensory cortex, as well
as areas associated with direct expressive speech arrest.
For this case, MS imaging data were imported preoperatively into the frameless stereotactic workstation dataset
and agreement was verified during intraoperative mapping with the identified locations for motor and somatosensory function (Fig. 2). The lesion was confirmed to
be located nearly wholly within a markedly expanded primary motor gyrus. Attempted resection of the lesion was
judged inappropriate given the high risk of significant
neurological deficit, and only biopsy of the lesion was
performed.
Pathological Findings and Postoperative Course. The
pathological diagnosis was benign oligodendroglioma.
Given the large volume of the lesion, the patient underwent external-beam radiotherapy to 54 Gy and he remains
neurologically intact 6 months postoperatively.
Case 2

This 42-year-old right-handed woman had undergone
two prior craniotomies in 1986 and 1990 for resection of
a right frontal oligoastrocytoma located anterior to the primary motor cortex. She received external-beam radiotherapy to 54 Gy in 1987 and multiple cycles of procarbazine-lomustine-vincristine chemotherapy, which were
completed in 1992.
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J. D. McDonald, et al.
TABLE 1
Summary of patient characteristics and preoperative and intraoperative mapping techniques used*
Case
No.

Age
(yrs),
Sex

1
2
3
4
5
6
7
8
9

25, M
42, F
45, F
42, F
37, F
45, F
37, F
56, M
32, F

Pathological Diagnosis

Lesion
Type

Lesion Location

Preop
Mapping
Modalities

oligodendroglioma
mixed oligoastrocytoma
oligodendroglioma
anaplastic astrocytoma
mixed oligoastrocytoma
anaplastic astrocytoma
glioblastoma
oligodendroglioma
oligodendroglioma

new
recurrent
recurrent
recurrent
recurrent
recurrent
recurrent
new
recurrent

lt parietal
rt posterior frontal
rt posterior frontal
rt posterior frontal
rt parietal
lt frontal
rt parietotemporal
lt frontal
lt frontal

MSI
fMRI, MSI
fMRI, MSI
fMRI, MSI
fMRI, MSI
fMRI, MSI
fMRI, MSI
fMRI, MSI
fMRI, MSI

Additional
Preop
Analysis Anesthesia

fMRI
Ñ
Ñ
Ñ
Ñ
Wada
Wada
Ñ
Wada

awake
general
general
general
general
awake
awake
awake
awake

Intraop
Functional Mapping

speech, motor, somatosensory
motor
motor
motor
motor
speech, motor
speech, motor, somatosensory
speech, motor, somatosensory
speech, motor, somatosensory

* All patients except the one in Case 1 underwent resection of the lesion. Abbreviations: fMRI = fMR imaging; MSI = MS imaging; Wada = intracarotid
amobarbital test; Ñ = not applicable.
Data imported into StealthStation.

Examination. Because the patient had experienced progressive leg weakness in the year preceding the present
admission, an MR image was obtained that documented progression of her residual/recurrent tumor (Fig. 3).
The patient underwent preoperative noninvasive functional analysis with fMR and MS imaging and the data
were imported into the frameless stereotactic workstation

before surgery. This allowed direct correlation with functional points mapped during surgery by cortical stimulation. This analysis confirmed highly concordant localization of function across the testing modalities (Fig. 4).
The mapping data, combined with standard use of the
stereotactic surgical anatomical information, facilitated a
near-total resection of the lesion.

FIG. 1. Case 1. Anatomical MR images (aÐd) and fMR images (e) obtained in a patient who presented with a generalized seizure and a large left frontoparietal mass consistent with a low-grade glioma on MR imaging. Localization of the
central sulcus by MR imaging anatomical criteria on high T2-weighted images (aÐc) suggested posterior displacement of
motor cortex (asterisk) by the large tumor mass. The parasagittal anatomy (d) revealed the cingulate sulcus to be terminated in two symmetrical sulci (small arrows), making unambiguous identification of the marginal sulcus and rolandic
cortex difficult. Functional MR imaging analysis for hand motor activity (e) supported the identification of primary motor
cortex as seen in panels a through c.

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Integrated functional brain mapping

FIG. 2. Case 1. a: Intraoperative photograph obtained in the same patient, who underwent an awake craniotomy with intraoperative functional mapping by cortical stimulation. Anatomical margins of the tumor at the cortical surface are outlined (black arrows). Points 1 and 2 =
expressive speech interruption; point 3 = face motor; point 4 = hand motor with finger and wrist contraction; point 5 = finger somatosensory; point 6 = thumb somatosensory; and points 7 and 8 = tongue somatosensory. The large, expanded gyrus involved with tumor is seen
between points 3 and 4. Close correlation between functional locations mapped preoperatively and intraoperatively is shown (bÐd).
b: Magnetic source imaging revealing the hand motor point is 2 cm deep within the same gyrus and within the same coronal plane as the
intraoperatively mapped location for hand motor activation (point 4). c: Magnetic source imaging revealing the hand somatosensory point
is 5 mm deep within the same gyrus and within the same coronal plane as the intraoperatively mapped location for hand somatosensory function (point 5). d: Magnetic source imaging revealing that the tongue somatosensory point is located within the same axial plane, 1.5 cm
deep and slightly posterior to the intraoperatively mapped location of identical function (point 8). The unlabeled MS imaging points in the
sagittal views of panels b and c are that of tongue somatosensory function, seen in the axial view in panel d. MSI = magnetic source imaging; somato = somatosensory.

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J. D. McDonald, et al.
Postoperative Course. A transient postoperative supplemental motor area deficit,14 which produced moderate
contralateral arm and leg weakness, resolved by 4 weeks
postoperatively.

FIG. 3. Case 2. Preoperative axial (left) and sagittal (right) gadolinium-enhanced T1-weighted MR images.

Discussion
An increasingly common technique of modern neurosurgical practice is the determination of functional brain
organization during surgery with cortical stimulation mapping techniques. The goal of the use of this technique is to
delineate critical areas of brain function so that they can
be preserved during lesion resection, thus minimizing the
direct risk of neurological deficit from the surgery. Although intraoperative mapping is still considered by most

FIG. 4. Case 2. Close correlation between preoperatively mapped functional points determined by MS and fMR imaging with intraoperatively mapped functional points determined by cortical stimulation in the patient. The correlation illustrated here is for hand somatomotor function. a: Image saved from the StealthStation monitor, with the red pointer dot
on the location of hand motor activation (finger contraction) mapped by cortical stimulation. In the trajectory orientation
looking down the central sulcus, slightly off-coronal (upper left), off-sagittal (lower left), and off-axial (upper right)
views are presented. b: Enlarged view of the central sulcus. With a setting of 0.5 on the alpha sliding scale of the
StealthStation (allowing a continuous blending between ÒVolume IÓ of the cranial program, containing mapped MS
imaging information, and ÒVolume II,Ó containing mapped fMR imaging information), both the preoperatively mapped
point for hand somatosensory function determined by MS imaging (white line on primary somatosensory gyrus, inferior
to the red dot) and the preoperatively mapped location for hand somatomotor function determined by fMR imaging (large
white dot located at the depth of the sulcus, spanning from motor to somatosensory cortex) are visualized. c: Pure MS
imagingÐmapped function, with the alpha scale of the StealthStation set to 0.0. d: Pure fMR imagingÐmapped function,
with the alpha scale set to 1. Median n. somato = median nerve somatosensory; MSI = magnetic source imaging.

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Integrated functional brain mapping
neurosurgeons to be the Ògold standardÓ of functional
mapping, there are several reasons why reliable preoperative noninvasive functional analysis is often desirable.
First, with intraoperative mapping, relevant data become
available only during the surgical procedure, after the
patient has already committed to an open procedure for
attempted lesion resection (as opposed to a needle biopsy). Second, intraoperative mapping procedures usually
require a larger craniotomy opening to expose not only the
lesion to be resected, but also the adjacent functional cortex to be mapped. Third, intraoperative mapping often
places greater demands on the patient. It lengthens the
duration of the operation, requiring the patient to be in the
operating room longer, and intraoperative speech mapping, of course, requires the patient to undergo an awake
craniotomy assisted by local anesthesia. If preoperative
noninvasive functional brain mapping techniques can be
developed and demonstrated to be highly accurate and
reliable in both normal and pathological settings, then
these may eventually reduce the need for the performance
of intraoperative functional cortical mapping. The cost effectiveness of this approach should be demonstrable
through the guidance of presurgical decision making, saving individual patients from unneeded craniotomies when
needle biopsy alone might be appropriate.
To assess the accuracy and reliability of preoperative
functional brain mapping techniques by direct correlation
with intraoperative localization of function determined by
cortical stimulation, we believe the techniques reported
here for importing preoperative MS and fMR imaging
data into an image-guided frameless stereotactic computer workstation will prove useful. Use of the frameless
stereotactic workstation for recording mapping data facilitates direct correlation of points of function mapped
preoperatively with those mapped intraoperatively. This
occurs not only because mapping results are directly recorded into digital computer file format, but also because
of the ability to rotate the digital volume representing the
patientÕs brain so that it can be viewed at any point in any
plane, rather than only in traditional true axial, coronal, or
sagittal planes (see Fig. 4). This approach should also
prove useful in identifying possible susceptibilities of the
specific preoperative mapping techniques themselves to
the occurrence of signal artifact or alteration due to local
pathological processes, such as anatomical expansion of
functional cortex by infiltrating low-grade neoplasms
(Case 1), anatomical distortion due to tumor recurrence
after previous treatment (Case 2), possible signal alteration due to peritumoral interstitial edema, or altered
regional blood flow adjacent to AVMs. An example of this
includes the apparently false localization of the motor cortex by fMR imaging analysis in Case 1. With this methodology, the data exist in a digital format amenable to
archiving and compiling into future standard digital functional neuroanatomical atlases. Although additional experience will be required for the quantitative analysis of the
accuracy and concordance of the functional maps produced by each testing modality, we have found this approach to be extremely useful in the care of patients with
brain tumors or AVMs near eloquent cortex.
Conclusions
We have outlined methods to incorporate preoperative
J. Neurosurg. / Volume 90 / March, 1999

functional brain mapping data into the operative frameless
stereotactic dataset used to guide resection of brain tumors
or AVMs located near functional cortex. This approach
should allow the direct correlation within the digital
frameless stereotactic environment of various noninvasive
preoperative testing modalities (such as fMR imaging and
MS imaging discussed in this report) with intraoperative
brain mapping by cortical stimulation, as well as permit
direct intermodality crosscorrelation. The standardized
application of these techniques in the functional mapping
of patients with lesions near eloquent cortex should facilitate our understanding of the accuracy of the various testing modalities, as well as the relative susceptibility of each
modality to pathological states such as anatomical distortion caused by expansive masses, prior treatment, interstitial edema, and regional alterations in blood flow.
Financial Disclosure
Dr. Heilbrun is a consultant to Sofamor Danek USA. The MEG
facility at the University of Utah School of Medicine (the Center for
Advanced Medical Technologies) has received an institutional research support grant from Picker International, Inc.
Acknowledgments
The authors wish to acknowledge the expert clinical care of these
patients provided by Shelly OÕMeara, R.N. We also acknowledge
the contribution of Edward Kinghorn, Ph.D., in the performance of
the preoperative neurocognitive assessment of the patients reported.
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Manuscript received June 24, 1998.
Accepted in final form October 9, 1998.
Address reprint requests to: Jeffrey D. McDonald, M.D., Ph.D.,
Department of Neurosurgery, University of Utah School of Medicine, 50 North Medical Drive, Salt Lake City, Utah 84132. email:
jdm@suzy.med.utah.edu.

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