INTRAOPERATIVE MOTOR MAPPING OF THE CEREBRAL
PEDUNCLE DURING RESECTION OF A MIDBRAIN
CAVERNOUS MALFORMATION: TECHNICAL CASE REPORT
Alfredo QuiñonesHinojosa, M.D.
Department of Neurological
Surgery, University of California,
San Francisco,
San Francisco, California

Russ Lyon, M.S., D.ABNM.
Department of Neurological
Surgery and Neurophysiology,
University of California,
San Francisco,
San Francisco, California

Rose Du, M.D., Ph.D.
Department of Neurological
Surgery, University of California,
San Francisco,
San Francisco, California

Michael T. Lawton, M.D.
Department of Neurological
Surgery, Center for Stroke and
Cerebrovascular Disease,
University of California,
San Francisco,
San Francisco, California
Reprint requests:
Alfredo Quiñones-Hinojosa, M.D.,
Department of Neurological
Surgery, University of California,
San Francisco,
505 Parnassus Avenue,
Moffitt Hospital, Room M779,
Box 0112,
San Francisco, CA 94143-0112.
Email: quinones@post.harvard.edu
Received, January 13, 2004.
Accepted, January 7, 2005.

NEUROSURGERY

OBJECTIVE AND IMPORTANCE: Brainstem cavernous malformations that seem to
come to a pial or ependymal surface on preoperative magnetic resonance imaging
studies may, in fact, be covered by an intact layer of neural tissue. For cavernous
malformations in the cerebral peduncle, intraoperative stimulation mapping with a
miniaturized probe can determine whether this overlying tissue harbors fibers in the
corticospinal tract. In addition, intermittent monitoring with transcranial motor evoked
potentials (TcMEPs) helps to protect this vital pathway during resection of the lesion.
CLINICAL PRESENTATION: A 20-year-old woman collapsed after a cavernous malformation in the left cerebral peduncle hemorrhaged into the pons, midbrain, and
thalamus. She presented with right hemiparesis and left oculomotor palsy.
INTERVENTION: The cavernous malformation was completely resected through a left
orbitozygomatic craniotomy and transsylvian approach. Stimulation mapping of the
cerebral peduncle with a Kartush probe (Medtronic Xomed, Inc., Jacksonville, FL)
identified the corticospinal tract lateral to the lesion, and a layer of tissue over the
lesion harbored no motor fibers. TcMEP monitoring helped to guide the resection, with
increased voltage thresholds and altered waveform morphologies indicating transient
impaired motor conduction. All TcMEP changes returned to baseline by the end of the
procedure, and the patient’s hemiparesis improved after surgery.
CONCLUSION: Stimulation mapping of the corticospinal tract and intermittent TcMEPs is a safe and simple surgical adjunct. Expanded monitoring of the motor pathway
during the resection of cerebral peduncle cavernous malformations may improve the
safety of these operations.
KEY WORDS: Cavernous malformation, Intraoperative stimulation, Motor evoked potential,
Neuromonitoring, Subarachnoid hemorrhage
Neurosurgery 54[ONS Suppl 2]:ONS-439, 2005

C

avernous malformations are vascular
anomalies with cavernous spaces lined
by endothelial cells and collagen, lacking smooth muscle or intervening neural tissue, filled with blood at various stages of degradation, and surrounded by gliotic brain.
Most cavernous malformations are supratentorial, but 10 to 23% are located in the posterior fossa with a predilection for the pons (12).
Asymptomatic patients with incidentally detected brainstem cavernous malformations are
usually managed conservatively, whereas
symptomatic patients with lesions that come
to a pial or ependymal surface are candidates
for microsurgical resection. Past reluctance to
operate on these lesions in densely eloquent
brainstem has largely been overcome as a result of advances in microsurgical and cranial

DOI: 10.1227/01.NEU.0000156784.46143.A5

base surgical techniques, neuroanesthesia,
neurophysiological monitoring, and frameless
stereotactic navigation (5, 9, 13, 16, 19–21, 25,
27). Still, appropriate patient selection depends on a careful assessment of whether or
not the cavernous malformation comes to a
surgically accessible surface. T1-weighted
magnetic resonance imaging (MRI) in axial,
coronal, and sagittal sections remains the best
measure of a lesion’s surface accessibility, and
even this modality is unclear in some cases.
Ideally, MRI demonstrates a lesion bulging
into the subarachnoid or ventricular space,
leaving little doubt as to its accessibility. However, even T1-weighted MRI may overestimate surface representation. An embedded lesion at the surface of the brainstem without
apparent overlying neural tissue may, in fact,

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QUIÑONES-HINOJOSA ET AL.

be covered by a thin intact layer. This situation raises an
intraoperative dilemma: does this layer contain functional
tissue such that the operation should be aborted, or can this
layer be traversed safely to expose and remove the lesion?
We report the intraoperative use of a miniaturized stimulating probe to map the corticospinal tract as it coursed
through the cerebral peduncle and around a cavernous malformation. In this case, motor mapping helped to resolve the
dilemma regarding overlying neural tissue and the proximity
of functional tissue to the lesion. Intraoperative neurophysiological monitoring with somatosensory evoked potentials and
cranial nerve monitoring (21) has been reported with similar
cases, providing feedback during manipulation and resection
of cavernous malformations. However, somatosensory
evoked potentials measure conduction along the dorsal columns in the spinal cord, medial lemniscus in the brainstem
and thalamus, and primary sensory cortex in the cerebral
hemispheres, but they do not monitor motor pathways, whose
injury can be even more debilitating. To our knowledge, this
case details the first reported use of cerebral peduncle mapping in the resection of a brainstem cavernous malformation.
In addition, transcranial motor evoked potentials (TcMEPs)
were used to monitor the integrity of motor pathways during
the resection.

CASE REPORT
A 20-year-old previously healthy woman collapsed in August 2003. Her urine was positive for amphetamines. Computed tomographic scans of the head revealed hemorrhage in
the left pons, midbrain, and thalamus. Brain MRI revealed
multiple cavernous malformations in the left midbrain, bilateral posterior temporal lobes, and left cerebellar hemisphere.
The patient was initially stuporous with dense right hemiparesis, but she improved with rehabilitation during the next 2
months. She was referred to the senior author (MTL) at that
time for definitive treatment.
Before surgery, the patient was alert and obeying commands but nonverbal. She communicated by blinking her
eyes. She had left oculomotor nerve palsy and right abducens
nerve palsy. Her corneal, cough, and gag reflexes were intact.
She had a right facial droop. Her left upper and lower extremities had normal strength, but her right upper extremity had
2/5 strength and her right lower extremity had 4/5 strength.
Her sensation was intact to light touch throughout. Her
follow-up MRI scan (Fig. 1) demonstrated resolution of blood
around the cavernous malformation and an embedded lesion
that seemed to come to the surface of the left cerebral peduncle. The lesion extended posteriorly to the inferior colliculus.

Surgical Intervention
The patient was taken to the operating room, where she was
anesthetized with desflurane at 2 to 3% (⬍0.5 maximum allowable concentration) and continuous propofol infusion (50–
125 ␮g/kg/min). Narcotic administration included remifen-

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tanil or fentanyl boluses. No
paralytic agents were used
after
induction
and
intubation.
Multipulse
transcranial
electrical stimulation was
generated with a CV-2
constant-voltage stimulator
(Cadwell Laboratories, Inc.,
Kennewick, WA). An investigational device exemption
was granted by the United
States Food and Drug Administration for clinical application of this equipment. FIGURE 1. Preoperative MRI scan
TcMEP stimulation parame- (axial T2-weighted image) showing
ters included one to nine the cavernous malformation in the
pulses at an adjustable dura- cerebral peduncle. The hematoma
tion of 50 to 500 microsec- cavity seemed to come to the surface
onds, with a pulse genera- of the cerebral peduncle without any
overlying neural tissue. Other cavtion interval (interstimulus
ernous malformations were also
interval) that was adjusted observed in the left cerebellum and
between 0.1 and 9.9 millisec- bilateral temporal lobes.
onds. Stimuli were delivered
through two “corkscrew” scalp stimulating electrodes (Nicolet
Biomedical, Inc., Madison, WI) placed by the neuromonitoring
team at the standardized 10 to 20 electrode positions of C1 and
C2 overlying motor cortex. Stimulation was conducted during
pauses in the dissection, with clear communication between
the neurosurgeon and neurophysiologist. TcMEPs were
quickly assessed within 15 seconds, without interrupting the
flow of the surgical procedure. TcMEP responses were used to
monitor the effects of the dissection and traction on the
malformation.
A left orbitozygomatic craniotomy was performed with a
wide sylvian fissure split, lateral retraction of the temporal
lobe, and opening of the tentorial incisura. When the cerebral
peduncle was fully exposed, a thin layer of hemosiderinstained neural tissue was encountered overlying the cavernous malformation. Frameless stereotaxy with the Stealth Navigation system (Medtronic Sofamor Danek, Inc., Memphis,
TN) confirmed the location of the lesion.
Motor mapping of the cerebral peduncle was performed
using the Ojemann stimulator (Model OCS-1; Radionics, Inc.,
Burlington, MA), and electromyographic monitoring of specific muscles was performed according to Yingling et al. (24).
The stimulator delivered 60-Hz pulses with a 1-millisecond
pulse length. Instead of the Ojemann bipolar stimulator probe,
a Kartush side-by-side bipolar stimulator probe (Medtronic
Xomed, Inc., Jacksonville, FL) was used (Fig. 2). A custommade banana plug/protected din adapter connected the Kartush probe to the Ojemann stimulator.
Electromyelographic (EMG) activity recorded from TcMEP
stimulation and functional mapping of the cerebral peduncle
was recorded using subdermal needle electrodes (29 gauge,
1.5 cm in length; Medtronic Xomed), which were placed ap-

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MAPPING THE CEREBRAL PEDUNCLE

FIGURE 2. Photograph comparing the Ojemann stimulator (Model
OCS-1) (bottom) with the Kartush stimulator (top). Inset, the tips of
Ojemann stimulator (left) are spaced 5 mm apart, whereas the finer tips of
the Kartush stimulator (right) are spaced less than 2 mm apart.

proximately 4 cm apart in the thenar-hypothenar eminences
bilaterally as well as in the tibialis anterior, extensor hallicus
longus, and foot flexors bilaterally. All electrophysiological
responses were recorded using a 16-channel Cadwell Cascade
system (Cadwell Laboratories, Inc.). Recording and filtering
parameters for functional mapping were used in a “free-run”
EMG mode with a bandpass of 30 to 500 Hz and a display gain
of 100 V per division. These traces were displayed at a time
base of 500 milliseconds per division to allow better discrimination of individual motor unit potentials. TcMEPs were set
at 30 to 1000 Hz, a time base of 100 milliseconds, and a display
gain of 50 to 100 mV per division.

FIGURE 3. A, intraoperative photograph (surgeon’s view from a leftsided orbitozygomatic approach) showing the appearance of the left cerebral
peduncle. A thin layer of hemosiderin-stained tissue covers the cavernous
malformation. The number “1” lies on the corticospinal tract, lateral to the
cavernous malformation, as determined by direct stimulation mapping
with the Kartush stimulator. PCA, posterior cerebral artery; SCA, superior cerebellar artery. B, drawing showing the relationship between the
corticospinal tract and a right-sided cavernous malformation in the cerebral peduncle. C and D, tracings showing that stimulation of the corticospinal tract produced positive EMG recordings in the right extensor hallucis longus (REH) (C) and the right tibialis anterior (RTA) (D). RHand,
right hand; RFT, right foot.

RESULTS
Direct stimulation mapping of the neural tissue overlying
the cavernous malformation did not elicit any motor activity
(Fig. 3A). As the stimulator was moved laterally from the
cavernous malformation, activity was observed grossly in the
right arm biceps muscle. No EMG activity was elicited in the
right hand muscles. With progressively more lateral stimulation, EMG activity was observed first in the anterior tibialis,
then in the extensor hallucis longus, and finally in the foot
flexors (Fig. 3, B–D). Muscle activity correlated with the expected somatotopic organization of the cerebral peduncle.
Thus, motor mapping revealed that the corticospinal tract was
lateral to the cavernous malformation and that no functional
tract resided in the thin layer between the surface of the
peduncle and the lesion. The fibers of the cerebral peduncle
were then separated, the hemorrhage cavity was accessed, and
the cavernous malformation was completely resected.
TcMEPs were obtained after sustained manipulation of the
lesion. Acute changes were detected in the TcMEPs, consisting
of an increased voltage threshold (125 V) and an altered waveform (Fig. 4). After a pause of 1 to 2 minutes in the dissection,
the TcMEP waveform returned to baseline. Repeated motor
mapping of the peduncle with the Kartush probe confirmed
the functional integrity of the cortical spinal tract. These TcMEP changes occurred three separate times, each one correlating with mild traction on the lesion and resolving shortly
after the lesion was released. TcMEPs were unchanged from
their baseline at the completion of the resection.

NEUROSURGERY

FIGURE 4. Tracings showing TcMEPs during resection of the cavernous
malformation. A, baseline TcMEPs demonstrated a robust polyphasic
response. B, TcMEPs obtained after the cavernous malformation was
manipulated with a micropituitary were noted to have an increase in the
voltage threshold (125 V), a change in the waveform morphology from
polyphasic to biphasic, and a decrease in amplitude and duration of the
response. The waveform returned to baseline a few minutes after release of
the cavernous malformation. RTA, right tibialis anterior; REH, right
extensor hallucis longus; RFT, right foot.

After surgery, the patient’s right hemiparesis was worse
temporarily but gradually improved beyond her preoperative
strength. At the time of discharge to an acute rehabilitation
center 2 weeks after surgery, her right upper extremity
strength was 4⫹/5 proximally and 2/5 distally, and her right
lower extremity strength was 4⫹/5 proximally and 5/5 distally. Her left upper and lower extremities remained at a
strength of 5/5. She was able to ambulate with assistance. Her

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QUIÑONES-HINOJOSA ET AL.

sensation remained intact to
light touch. Postoperative
MRI revealed complete resection of the cavernous malformation (Fig. 5).

DISCUSSION
During the resection of
cavernous malformations involving the midbrain and cerebral peduncle, protection
of the corticospinal tract and
preservation of motor function are the neurosurgeon’s
primary concerns. In this report, we demonstrate that direct stimulation mapping
and intermittent monitoring
with TcMEPs can be useful
in addressing these concerns. We demonstrated that
a motor potential can be obtained by stimulating the pe- FIGURE 5. A, intraoperative photograph demonstrating the resection
duncle directly and that Tccavity after removal of the cavernous
MEP recordings can be malformation. PCA, posterior ceretransiently altered during bral artery; SCA, superior cerebellar
the resection of a brainstem artery. B, postoperative T2-weighted
cavernous
malformation. MRI scan documenting complete
of
the
cavernous
Each can be added to the resection
neuromonitoring
regimen malformation.
easily and safely; together,
they may have contributed to this patient’s favorable outcome.
Detailed mapping and monitoring of the motor pathway seem
to be justified in select neurosurgical cases such as this one.

Cerebral Peduncle Mapping
One could argue that if a cavernous malformation was
properly selected for microsurgical resection, the lesion would
always be at the pial or ependymal surface, functional tissue
would be pushed aside by the lesion and/or its hematoma,
and mapping would be unnecessary because there would be
no violation of intact brain. However, this case demonstrates
that a thin layer of overlying tissue can be missed by preoperative MRI. Furthermore, even when a lesion in the cerebral
peduncle clearly extends through the pial surface, knowing
exactly where the corticospinal tract is can help the neurosurgeon to protect it during the dissection around and mobilization of the lesion. Most of all, the information derived from
mapping eliminates the unsettling uncertainty that comes
from not knowing exactly where this vital tract lies.
In this case, the tissue overlying the cavernous malformation did not contain functional corticospinal tract, informing
the neurosurgeon that the obvious trajectory to the lesion
would be safe. In other cases in which the overlying tissue

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contains functional corticospinal tract, the surgical plan can be
modified to avoid a postoperative motor deficit by finding an
alternative route to the cavernous malformation through noneloquent tissue or by aborting the procedure. Although “negative” peduncle mapping in our case did not alter the surgical
plan, “positive” mapping in these other cases may be even
more beneficial.
The Kartush stimulator probe is a significant improvement
over the standard Ojemann stimulator probe and is essential
for this technique application. The tips of the Ojemann probe
are nearly 2 mm in diameter, with 5-mm spacing between the
cathode and anode tips. These dimensions make it bulky and
dangerous for such a narrow surgical corridor and not discriminating enough for such a small tract. In contrast, the
Kartush probe has less than 2-mm spacing between the tips
and an overall width of approximately 2.5 mm, making it
more maneuverable and accurate. It has been used for dorsal
sulcus mapping and intramedullary mapping during the resection of intrinsic spinal cord tumors (18). It requires a banana plug/protected din adapter to connect to the Ojemann
stimulus generator, but this adapter was easily made by our
bioengineering staff.
There are other miniaturized stimulation probes that might
also work, namely, a bayoneted probe described by Duffau
and Sichez (7). These authors initially described a bipolar
probe with 3-mm spacing between the tips used for tectal
mapping during the resection of a midbrain cavernous malformation. This device was, by their own account, “not precise
enough” (8, p 61) and “without good ergonomics under the
microscope” (8, p 61), prompting a modification to 2-mm
spacing between the tips. At this time, the device used by
Duffau and his colleagues is commercially available in Europe. The Kartush probe is readily available in the United
States and is approved by the United States Food and Drug
Administration for intracranial procedures.
EMG monitoring is an important element of our mapping
technique. Others have relied solely on observation of gross
motor responses during stimulation, but monitoring of EMG
responses has been demonstrated to increase sensitivity in
localizing primary motor cortex and subcortical pathways
with electrical stimulation (24). In our case, EMG activity was
occasionally observed after stimulation mapping that had no
associated gross movement. Therefore, the sensitivity of mapping was enhanced by careful observation of EMG responses
in this patient and, generally, in patients whose gross motor
responses may already be diminished by hemorrhage from a
cavernous malformation.

TcMEP Monitoring
Although stimulation mapping identifies where the corticospinal tract is located in the cerebral peduncle, TcMEPs
provide an easier method of intermittently monitoring conduction along the tract, and thus the integrity of the tract,
during the procedure. TcMEPs are compound action potentials recorded in muscles after cortical stimulation, reflecting

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MAPPING THE CEREBRAL PEDUNCLE

conduction along the corticospinal tract, anterior horn cells,
and peripheral nerves. TcMEP monitoring has been used during brain and spinal cord tumor resections (4, 6, 14, 18, 23, 26),
during spinal reconstructions (1–3, 10, 11, 15, 26), and during
aneurysm surgery (17, 22). The technique adds little time to
the operation (less than 30 min, most of which is spent placing
additional electrodes initially during anesthesia preparations)
and can be easily incorporated into the electrophysiological
monitoring routine. TcMEPs elicit some patient movement
that can be dangerous if performed during microsurgical dissection, making communication between the neurosurgeon
and electrophysiologist essential to coordinate pauses in the
dissection for TcMEPs. The advantage of monitoring the motor pathway with TcMEPs rather than with stimulation mapping is that it is quicker and easier, requiring only a pause in
the dissection rather than moving the Kartush probe in and
out of the surgical field. In addition, TcMEPs seem to be more
sensitive to deleterious effects from manipulation of the cavernous malformation or surrounding brain. Changes in voltage thresholds and waveform morphology are harbingers of a
compromised tract that are not apparent with stimulation
mapping. Therefore, TcMEPs are better suited to detect evolving changes in motor conduction. Frequent TcMEP checks are
needed to identify these evolving trends before motor responses are lost completely. A definite correlation between
TcMEP changes and clinical symptoms cannot be verified
from this single case but may emerge in future studies.
These techniques of mapping and monitoring the motor
pathway have applications other than for cavernous malformations in the cerebral peduncle. Microsurgical resection of
cavernous malformations along the corticospinal tract in the
internal capsule, pons, and anterior medulla might also benefit
from these techniques. Location aside, they may play a role
whenever there is shadow of a doubt about a lesion’s surface
accessibility, particularly when the lesion seems to be embedded in the brain rather than protruding from it. In these cases,
monitoring the motor pathway may supplement other techniques like somatosensory evoked potentials, brainstem auditory evoked potentials, and cranial nerve monitoring (21).

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Acknowledgment
None of the authors of this study has any financial interest in any of the
instruments or methodologies used in this study.

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COMMENTS

thank the authors for reminding us that the Kartush stimulator can be used in this application.

C

avernous malformations of the brainstem are among the
most challenging lesions to treat surgically. First, one
must decide when to intervene surgically. We recommend
operative resection if the lesion reaches the surface and the
patient has experienced multiple hemorrhages associated with
progressive neurological decline.
Once the decision to operate has been made, a surgical
approach must be selected. To do so, we use the two-point
method (1). One point is placed in the center of the lesion, and
a second point is placed at the surface of the lesion. A straight
line is drawn connecting the points to the external surface of
the skull. This trajectory dictates the most direct surgical approach, and the appropriate craniotomy can be chosen.
If the two-point method dictates a trajectory that traverses
functional brainstem tissue, intraoperative neurophysiological
monitoring can be an invaluable tool. The facial colliculus, for
example, can be stimulated on the floor of the fourth ventricle
when a suboccipital approach is contemplated. The authors
describe a modification of a Kartush stimulator used after a
banana plug adapter is connected to the Ojemann stimulus
generator. This probe has a narrow profile, has a thin shaft,
and is amenable for use in deep areas of the brainstem. Despite stimulation at the entry point, no corresponding electromyographic response was obtained. The probe was invaluable
for reassuring the surgeons that the entry point was safe. As in
electrocorticography, however, this probe primarily stimulates the surface. Deep within the brainstem, there is no guarantee that eloquent tissue involving cranial nerve nuclei will
not be disrupted.
The authors also indicate that magnetic resonance imaging
might be subject to misinterpretation in terms of the location
of the lesion with respect to the surface. We agree. Preoperatively, we also use T1- rather than T2-weighted imaging to
determine whether a lesion reaches the surface and is therefore safe to resect. This nice case report demonstrates the use
of intraoperative motor mapping of the cerebral peduncle
during resection of a midbrain cavernous malformation. We

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Randall W. Porter
Sam Javedan
Robert F. Spetzler
Phoenix, Arizona

1. Brown AP, Thompson BG, Spetzler RF: The two point method: Evaluating
brain stem lesions. BNI Q 12:20–24, 1996

T

he authors have described an elegant technique for mapping the cerebral peduncle during resection of a midbrain
cavernous malformation. This technique assisted the surgeon
in precisely localizing the corticospinal tracts, which had been
displaced posteriorly and laterally by the hematoma and cavernous malformation, and in achieving a complete resection
without incurring any new permanent neurological deficit.
Successful removal of brainstem cavernous malformations
requires a precise and delicate microsurgical technique and,
very importantly, appropriate patient selection. To successfully remove these challenging lesions, the malformation
and/or associated hematoma must come to an approachable
surface of the brainstem. If any significant functional brainstem tissue lies between the surgeon and the lesion, new and
potentially devastating neurological deficits can be expected.
As the authors have clearly stated, the appearance of these
lesions on magnetic resonance imaging can be misleading. In
most instances, surgical exposure will clearly demonstrate
gross discoloration at the site at which the lesion comes closest
to the brainstem surface. Not infrequently, however, the surgeon must make a judgment as to where the initial incision
into the brainstem must be made. This report clearly demonstrates the usefulness of this elegant technique not only in
selecting the precise site for entering the hematoma cavity but
also in aiding the surgeon during microsurgical resection of
the malformation.
Daniel L. Barrow
Atlanta, Georgia

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