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Preoperative Magnetoencephalographic
Sensory Cortex Mapping
Ajay Niranjan Erika J.C. Laing Fahad J. Laghari R. Mark Richardson
L. Dade Lunsford
Department of Neurological Surgery, University of Pittsburgh and UPMC Brain Mapping Center, Pittsburgh, Pa., USA
E-Mail karger@karger.com
200 Lothrop Street, Pittsburgh, PA 15213 (USA)
www.karger.com/sfn
E-Mail niranjana @ upmc.edu
Electrophysiological methods such as EEG and MEG four head position indicator coils were glued to their scalp using
have been increasingly utilized to localize cortical regions collodion adhesive. Two bipolar electro-oculography electrodes
were placed above and below the right eye to monitor vertical eye
active during somatosensory stimulation. EEG and MEG movements, and diagonally below and to the right of the right eye
provide excellent temporal resolution, on the order of and above and to the left of the left eye to monitor horizontal eye
milliseconds, offering the opportunity to localize primary movements. A single bipolar ECG channel was used to record car-
and secondary somatosensory responses separately for diac activity from the chest. Patients with epilepsy (n = 17) under-
higher specificity. went simultaneous EEG recordings during an MEG epilepsy re-
cording procedure that took place immediately before the mea-
MEG is a useful noninvasive tool to preoperatively de- surement of somatosensory evoked fields. Before entering the
termine functional somatosensory cortex [1–5]. Studies MSR for MEG recording, the positions of the head position indica-
that compare MEG-derived maps of sensory motor acti- tor coils were digitized with the help of a Polhemus Isotrak 3D-
vation to invasive procedures such as electrocorticogra- digitizer (Polhemus, Inc., Colchester, Vt., USA) included in the
phy indicate high concordance rates [6–9]. MEG addi- MEG system. Fiducial landmarks, nasion and left and right preau-
ricular points, were digitized to be utilized for later coregistration
tionally has excellent spatial resolution, sometimes as of the MEG and structural MRI data. Additional anatomical points
good as 2–3 mm for sources in the cerebral cortex [10, 11] (up to 150) on the face and scalp were digitized to further facilitate
making it an ideal tool to localize somatosensory respons- fusion of MEG data with a reconstructed volumetric MRI image.
es. Advances in computer hardware and software during During the MEG data acquisition, patients sat comfortably in
the past three decades have further contributed to the an upright sitting position in the MSR with the head positioned in
a helmet containing the 306 MEG sensors. A patient’s head posi-
evolution of MEG by improving the data analysis and re- tion within the sensor array was determined before each MEG re-
ducing the turnaround time of reports. These factors, cording by registering the position of the four indicator coils that
coupled with its ability to replicate the measurement if were attached to the head of the patient. For this purpose, a brief
needed, potentially render MEG the preferable method to weak electrical pulse was sent to the coils. The positions of the coils
study and to disentangle the cortical representation of were identified by the MEG sensors, defining the head position
with respect to the machine’s fixed coordinate system, and allow-
dermatomes in the human brain. In this report we present ing for later integration of MEG and MRI data. The knowledge
our experience in sensory cortex localization for patients about head position allowed for post-hoc correction of head move-
with brain tumors, arteriovenous malformations and ep- ment artifacts. Visual and two-way audio communications with
ilepsy, and we assess its effect on patient outcomes after the patient were maintained throughout the session.
neurosurgical procedures.
Somatosensory Stimulation Paradigm
Somatosensory stimulation was performed electrically using
bipolar adhesive electrodes placed on the skin over the course of
Materials and Methods median nerve at the wrist. The sensory paradigm was delivered us-
ing internally driven Neuromag software (Elekta Neuromag Oy).
Patients Demographics Constant current pulses with a duration of 0.2 ms were used. Aver-
Forty-five consecutive patients underwent sensory cortex lo- age stimulation rate was 1 Hz. The amount of current was deter-
calization using MEG between September of 2010 and April of mined for each patient individually by one MEG technician who
2012. Thirteen had glial neoplasms, 6 had meningiomas, 6 had a gradually increased the voltage while another technician moni-
brain metastasis, 1 had a cavernous malformation, 2 arteriove- tored the elicited response until a small thumb twitch was ob-
nous malformations, and 17 had epilepsy. Ages ranged from 16 to served. Patients were polled to ensure that the stimulation level was
77 years (mean = 47). Twenty-three patients were female. not uncomfortable. A minimum of 200 epochs were recorded for
all stimulations. Stimulations were made either to the median
Magnetoencephalographic Procedures nerve contralateral to the site of the brain anomaly (n = 16), or for
MEG was performed prior to surgery on an outpatient basis both median nerves (n = 29). If recording from both median
(fig. 1). Noninvasive mapping of the somatosensory cortex was nerves, the data collection was done separately for the left and right
achieved using a whole-head 306 channel Neuromag® Vectorview sides in consecutive acquisitions during a single MEG session.
System (Elekta Neuromag Oy, Helsinki, Finland), which is con- During MEG recordings, patients were asked to remain motionless
tained in a magnetically shielded room (MSR). The MSR is con- and avoid blinking or eye movements, aided by maintaining their
structed from layers of aluminum and μ-metal, an alloy of ex- gaze on a fixation mark placed on a screen placed in front of them.
tremely high magnetic permeability that is designed to occlude
extraneous electric and magnetic fields. The room is approximate- Neuroanatomic MRI Acquisition
ly 4.6 × 3.6 × 3 m in dimension. High-resolution MRI was acquired in order to provide the
The patients were first checked for any abnormal magnetic ac- brain anatomical detail needed for both MRI coregistration as well
tivity by placing them in the unit and recording initial MEG sig- as eventual surgical neuronavigation. For brain tumors and vascu-
nals. If any magnetic activity was detected, a degausser was some- lar malformations a contrast-enhanced 3D spoiled gradient–re-
times used to demagnetize the patient. Once a patient was cleared called acquisition in steady state (SPGR) sequence with 2-mm ax-
for MEG recording they were taken to the preparation room where ial images covering the entire head was obtained. For patients with
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–200 fT
42 ms
Right
a b –200 fT
c d
Fig. 1. Example of the MEG signals and their source equivalent ly 42 ms after stimulation. c The magnetic field pattern of the hel-
from a patient with a right parietal glioblastoma. a View of the en- met at the peak response is shown, with blue (light gray) indicating
tire 306 sensor helmet (nose pointing upwards) shows somatosen- the magnetic flux into the head, and red (dark gray) out of the
sory evoked magnetic fields distributed in the left parietal region head. The center of the arrow depicts the location of the ECD, the
of the helmet. b Butterfly plot of the same responses, with all pari- arrow’s direction indicates the current orientation, and the arrow
etal channels overlaid by left or right hemisphere, shows that the size indicates the strength of the ECD. d The SEF source projected
primary peak of activity to electrical stimulation of the right me- onto an axial MRI can be used for intraoperative guidance. In this
dian nerve is elicited predominantly in the left hemisphere (fT re- example, the peak SEF activity at 42 ms after stimulation localizes
fers to femtoteslas). The peak for this patient occurs approximate- to this patient’s postcentral sulcus, anterior to the brain tumor.
medically intractable epilepsy, a brain volume imaging (BRAVO) then preprocessed using a bandpass filter of 1–40 Hz. Data from
sequence with 1.2-mm-thick axial images that covered the entire 23 patients was also down sampled by a factor of 4–250 Hz. Trials
head was obtained. The acquisition field of view was kept broad with eye blinks or any other form of distortion from a noise source
enough to include the nose and the cranial vertex, both of which were rejected before averaging. The averaging time window con-
are crucial for coregistration with MEG data. MRIs were trans- sisted of 200 ms proceeding and 1,000 ms following each individ-
ferred through the ethernet system to the MEG workstations. ual stimulation utilizing the preceding 200 ms for baseline correc-
tion. The average number of trials for each SEF was 176 (SD =
Data Analysis 41.6). Once averaged, the evoked fields were reviewed and source
Sensory evoked fields (SEF) are the magnetic fields generated modeling was applied to the MEG data. Data analysis was per-
by activation of sensory cortex in response to external stimulation. formed using the Elekta Neuromag Toolbox® and MNE Suite
Evoked fields were recorded at a sampling rate of 1,000 Hz and from the Harvard Martinos Center.
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Fig. 2. Representative source locations for the somatosensory re- toma in a 47-year-old female. b Postcentral sulcus localization
sponses of 2 patients. Arrows point to a black circle, whose size anterior to the right parietal glioblastoma in a 59-year-old fe-
is equivalent to the 95% confidence volume of the patient’s pri- male. Both patients underwent image-guided surgery after pre-
mary somatosensory dipole. a Somatosensory cortex localization surgical brain mapping and suffered no postoperative somato-
at the central sulcus anterior to the left fronto-parietal astrocy- sensory deficits.
tailed t test assuming unequal variances of the remaining suming unequal variances was completed on the data as
data found a significant difference between the confi- separated into age groups. Groups were split by age in two
dence volumes of central and postcentral sulcus localiza- separate ways. First, comparing age groups above and be-
tions, with central sulcus localizations having statistically low the median age of 47 revealed no statistical difference
larger confidence volumes (p = 0.08). Figure 3 depicts the in the peak SEF latencies of these groups (p = 0.27). A
confidence volume values with outliers removed. second split wherein patients were grouped above and
below the age 35 also revealed no significant difference in
Effect of Age peak SEF latencies (p = 0.47).
Because some of the background literature suggested
that age can play a role in the latency of the somatosen- Effect of Brain lesion
sory peaks, a brief exploration of the effect of age was Previous literature suggests that SEFs may be larger in
completed. Figure 4 shows a scatter plot of peak latency magnitude in the hemisphere that contains a mass lesion,
by patient age, revealing no association between age and compared to the nonaffected hemisphere [12]. Of this pa-
the somatosensory peak latency. A two-tailed t test as- tient group, 8 patients had lesions near the central sulcus.
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G-Fit (%)
80
60 40
40
20
20
0 0
a Central sulcus Postcentral sulcus b Central sulcus Postcentral sulcus
Outliers included 95% confidence volume Outliers excluded 95% confidence volume
1,000 1,000
Confidence volume (mm3)
600 600
400 400
200 200
0 0
c Central sulcus Postcentral sulcus d Central sulcus Postcentral sulcus
Fig. 3. Graphs representing the quality measure of the dipoles re- fit requirement. There were several outliers in the size of confi-
ported for central and postcentral localizations. Peak latency and dence volumes, so after correction for outliers, it is seen on the
an initial analysis of the confidence volume showed no statistical rightmost graph that the size of the confidence volume from the
difference. The goodness-of-fit parameter was statistically higher postcentral sulcus is significantly smaller than those generated
for postcentral sulcus localizations than central sulcus localiza- from the central sulcus, indicating slightly but significantly more
tions, though both were well above a minimum 90% goodness-of- precise localizations for activities elicited in the postcentral sulcus.
Only 5 of these patients have data for both left and right
140
side stimulations, and of those 5, 2 patients had parasagit-
120
Latency of peak activity (ms)
tal tumors that crossed the midline, i.e. the tumor affected
both hemispheres. In 2 of these patients there was a large 100
hemispheric asymmetry in the magnitude of the SEF re- 80
sponse; however, the direction of the asymmetry was op-
posite that of previous findings. In both patients, the mag- 60
0
Clinical Outcomes 10 20 30 40 50 60 70 80
Ten epilepsy patients are still awaiting surgery. One Age of patient
patient with a cavernous malformation and 1 patient
with motor cortex arteriovenous malformations elected
Fig. 4. Peak latency by patient age. Scatter plot showing that con-
conservative management. Thirty-two patients under- trary to suggestions from prior literature, age appeared to have no
went craniotomy. Their surgical access routes were effect on the latency of the somatosensory peak generated in this
planned specifically to avoid regions identified by the so- population of patients.
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