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Acta Neurochir (Wien) (2006) 148: 499–509

DOI 10.1007/s00701-005-0672-6

Neurosurgical Concept
The importance of brainstem mapping in brainstem surgical
anatomy before the fourth ventricle and implication
for intraoperative neurophysiological mapping

N. Morota1 and V. Deletis2

1
Department of Neurosurgery, National Children’s Medical Center, National Center for Child Health and Development, Tokyo, Japan
2
Division of Intraoperative Neurophysiology, St. Lukes=Roosevelt Hospital, New York, USA

Received April 5, 2005; accepted September 27, 2005; published online December 30, 2005
# Springer-Verlag 2005

Summary Despite the recent advancement of MRI to depict the lesion in


the brain stem, BSM remains as the only way to provide surgical
Brain stem mapping (BSM) is an intraoperative neurophysiological anatomy in the operative field. BSM could guide a neurosurgeon
procedure to localize cranial motor nuclei on the floor of the fourth to the inside of brain stem while preventing direct damage to
ventricle. BSM enables neurosurgeon to understand functional anatomy the cranial motor nuclei on the floor of the fourth ventricle. It
on the distorted floor of the fourth ventricle, thus, it is emerging as an is expected that understanding its advantage and limitations would
indispensable tool for challenging brain stem surgery. The authors help neurosurgeon to perform safer surgery to the brain stem
described the detail of BSM with the special emphasis on its clinical lesion.
application for the brain stem lesion. Surgical implications based on the
result of brains stem mapping would be also informative before planning Keywords: Brain stem; intraoperative neurophysiology; surgery;
a brain stem surgery through the floor of fourth ventricle. cranial motor neucleus; fourth ventricle.

Fig. 1. Preoperative MRI T1 weighted images of a 29-year-old woman with systemic capillary hemangiomas revealed a large upper pontine
hematoma predominantly located in the right pons
500 N. Morota and V. Deletis

Introduction anatomical relationship between the lesion and vital


structures is the essential for safe surgery [10, 11].
Recent advances in neuro-imaging enabled us to pre-
However, what we need to know during brain stem sur-
cisely locate the lesion even in the brain stem which used
gery is the surgical anatomy which implies the func-
to be called ‘‘no man’s land’’. It still poses challenge to
tional anatomy under an operating microscope. Normal
neurosurgeons [1, 3, 7, 9, 15–17]. Understanding the

Fig. 2. A postoperative CT scan taken im-


mediately after surgery (left) and a MRI T1
weighted image taken a week after surgery
showed nearly complete removal of the he-
matoma

Fig. 3. Schematic drawing of representative patterns of the CMN (cranial motor nucleus) displacement by a brain stem tumor at the various site. An
upper pontine tumor bisects and displaces the facial nuclei caudally. A lower pontine tumor displaces them rostrally. A medullary tumor tends to
compress one or some of the lower cranial nerve nuclei ventrally. A cervico-medullary junction spinal cord tumor pushed the lower cranial nuclei
rostrally. (modified from ref. 13)
The importance of brainstem mapping in brainstem surgical anatomy 501

anatomical landmarks could be distorted by the brain Conventional intra-operative neurophysiology such as
stem lesion. Intra-operative neurophysiology will help to auditory brain stem response and somatosensory evoked
reveal functional anatomy [3, 5, 8, 12, 19]. potential monitoring may help the surgeon. Motor
evoked potential (MEP) monitoring will assure the sur-
geon that the functional integrity of the motor pathway
Case discussion
remains stable [2]. Nevertheless, this information is not
A 29-year-old woman, who had systemic capillary essential for a neurosurgeon who intends to approach the
angioma and suffered from mild mental retardation, brain stem lesion through the floor of the fourth ventri-
visited our center for progressive left hemiparesis and cle. Information we need is the precise localization of
right facial palsy. MRI showed a large pontine hema- the cranial motor nuclei (CMN) on the floor of the fourth
toma (Fig. 1) and she was referred to the Department of ventricle where anatomical landmarks are lost because
Neurosurgery. Since the paresis was progressive, surgi- of the lesion.
cal indication to evacuate and resect the suspected The answer to the first question is brain stem map-
angioma would be applied for her. ping (BSM). BSM is a neurophysiological technique
The question that neurosurgeons ask is how to remove to localize the motor cranial nerve nuclei on the floor
the hematoma while preserving neurological function, of the fourth ventricle. The patient underwent removal
especially the motor function of the cranial nerves. of the hematoma and angioma utilizing BSM without

Fig. 4. Surgical anatomy of the floor of the fourth ventricle during brain stem surgery is shown. The facial nucleus is often mapped around the edge of
the tumor exposed in the floor of the fourth ventricle (upper). Myelotomy should be directed opposite the mapped nuclei. The unmapped lower CMN
before tumor resection usually locates ventral to the medullary tumor. Attention should be paid at the bottom of the tumor cavity (middle). A large low
grade spinal cord tumor often extends into the fourth ventricle by pushing the caudal part of the floor of the fourth ventricle toward the rostrally.
Undermining the caudal end of the floor of the fourth ventricle would be required to preserve the functional integrity of the lower CMN (lower)
502 N. Morota and V. Deletis

compromising the neurological deficit. Postoperative Recording.


neuro-imagings showed satisfactory evacuation of the Epoch time: 20 msec
hematoma (Fig. 2). Filter: 20–3000 Hz
Amplification: 10.000 times
Neurophysiological aspect Muscles for EMG recording:
CMN VII: orbicularis oculi & oris
BSM enables the surgeon to locate motor cranial nerve
CMN IX=X: posterior pharyngeal wall or cri-
nuclei within the distorted floor of the fourth ventricle
cothyroid
by delivering electrical stimulation through a hand held
CMN XII: lateral wall of the intrinsic tongue
mono-polar probe and recording the muscle response by
muscle
EMG [3, 12, 13, 19, 20]. It should be confirmed before-
hand that the influence of the muscle relaxant does not For stimulation, we prefer to use a hand-held mono-
interfere with the EMG recording in BSM. Otherwise, polar probe for precise localization of the CMN. The tip
any type of anesthesia is compatible with BSM. of the probe is round and of moderate size to prevent
Standard parameters for BSM is shown below: damaging the floor of the fourth ventricle during stimu-
lation. EMG responses are usually recorded by sticking
Stimulation.
a pair of needle electrodes to the targeted muscle. The
Cathode: hand-held monopolar probe (diameter of
electrodes should be secured on the face and the lip
the tip: 0.75 mm)
tightly before turning the patient to the prone position.
Anode: cervical muscles in the operative field or Fz
Wave form: square wave, single pulse
Duration of stimulation: 0.2 msec
Application during the operation
Frequency: 1.0–4.0 Hz
Intensity: 2.0 mA for screening, then squeeze inten- The threshold intensity depends on the pathology, the
sity to detect threshold. degree of brain stem compression and the distance to the

Fig. 5. Upper: MRI of a 35-year-old patient with a cervicomedullary junction tumor. The heterogeneously enhanced partly exophytic tumor is
found on the dorsal side of the medullae. Lower: Intraoperative photographs demonstrate a hand-held monopolar probe placed on the tumor
extending over the obex (left), on the upper half of the floor of the fourth ventricle searching for the facial nucleus (center). The tumor was partially
removed without significant neurological deficit. Myelotomy on the dorsal medulla is shown (right)
The importance of brainstem mapping in brainstem surgical anatomy

Fig. 6. Schematic drawing of BSM for the facial nucleus. The facial nucleus was located on the point when stimulated at the threshold intensity. None or a weaker response was recorded when stimulation
is carried out just a few mm away from the facial nucleus
503
504

Fig. 7. Schematic drawing of BSM for the lower CMN. No CMN was mapped through the tumor surface before tumor resection (left). The bilateral hypoglossal and right glossopharyngeal=vagus nuclei
N. Morota and V. Deletis

were located after tumor resection on the obex. No response was obtained from the residual tumor cavity on the dorsal medulla (right)
The importance of brainstem mapping in brainstem surgical anatomy 505

CMN. In some instances, the threshold could be as low thus the initial BSM before tumor resection may fail to
as 0.2–0.4 mA, which often used during the case with locate them. The surgeon should be prepared to repeat
the brain stem hematoma. Brain stem tumors tend to BSM intermittently since the unmapped CMN can be
require higher threshold intensity up to 2.0 mA. Atten- detected near the bottom of the tumor cavity. Once the
tion is paid so as not to stimulate one point more than 5 unmapped CMN is located, it is recommended to leave
seconds for safety reasons. After exposing the floor of the rest of the tumor in order to preserve the CMN
the fourth ventricle, a surgeon starts to stimulate the function. Interpretation of the result of BSM in a medul-
floor 2.0 mA. Once the muscle response is recorded, lary lesion is not simple compared with that of a pontine
the intensity is squeezed up stepwise to the threshold. lesion, because the functional integrity of the lower
Using the threshold intensity, the CMN can be precisely CMN consists of both afferent and efferent pathways
located by moving the stimulation probe every 1 mm. which form a reflex circuit in the brain stem. Preserved
For a neurosurgeon, BSM is a straightforward techni- BSM does not mean the lower CMN function is pre-
que [5, 8, 12, 19]. The presence of the muscle response served. It means the efferent pathway is preserved. Post-
directly tells you the CMN there. If expected responses operative dysphagia and dysarthria can develop despite
are not required, there are two possibilities. One is preserved EMG responses following BSM.
mechanical failure of the stimulation or recording sys- The cervicomedullary junction spinal cord tumor
tem. The other is that the CMN could be located ventral (CMJ SCT) shows a different displacement pattern. A
to the brain stem pathology. No response does not neces- CMJ SCT may extend into the fourth ventricle when it is
sarily mean there is no CMN. Repeated stimulation large [6]. It pushes the lower CMN rostrally. Direct
through the intra brain stem pathology would be re- approach to the rostral end of the tumor through the floor
quired to detect the CMN in this situation. This is espe- of the fourth ventricle can damage the lower CMN.
cially true in patients with medullary tumor which tends Undermining the floor of the fourth ventricle from the
to grow in an exophytic fashion. caudal side enables the surgeon to avoid direct damage
to the lower CMN.
From surgical view point, it would be safe to say that
Neurosurgical implication for brain neurosurgeons should be aware of the risk of damaging
stem surgery the CMN at the edge of pontine tumors, at the bottom of
Previous study revealed the localization specific
displacement pattern of the CMN on the floor of the
fourth ventricle [13]. The study subjected the brain stem
tumor and the displacement pattern can be different in
hematoma and other lesions [14]. The result is briefly
reviewed here (Fig. 3).
A pontine tumor is inclined to grow in an intrinsic
fashion and expose its part on the floor when it grows.
The facial nuclei are displaced in the floor of the fourth
ventricle but no displacement is observed regarding the
lower motor nuclei. When the tumor locates in the upper
pons near the midline, the facial nuclei tend to be
bisected and displaced caudally. On the contrary, if the
tumor is in the lower pons, they are displaced rostrally.
In case of pontine hematoma, displacement could be
observed on the unilateral facial nucleus either toward
the rostral or caudal side with midline shift based on the
hematoma location. Presence of EMG response follow-
ing BSM usually correlates with the postoperative func-
tional preservation.
Fig. 8. Schematic representation of the result of BSM. The facial nu-
A medullary tumor enlarges its volume more in an
cleus is not displaced in the floor of the fourth ventricle. The hypo-
exophytic fashion than a pontine tumor. The tumor tends glossal nuclei were localized ventral to the rostral end of the tumor
to compress one or some of the lower CMN ventrally, which extended into the fourth ventricle
506 N. Morota and V. Deletis

medullary tumors, and at the rostral edge of the CMJ to the upper cervical cord (Fig. 5). On admission, she showed right facial
hypalgesia, left vocal cord palsy and mild left hemiparesis. Tumor
SCT [14]. This idea will help neurosurgeons to design a resection with the use of BSM was scheduled. At surgery, the dorsal
safe surgical approach to the brain stem from the floor of medulla to the upper cervical cord showed marked swelling and a part of
the fourth ventricle (Fig. 4). the tumor was exposed at the caudal end of the fourth ventricle. Some
landmarks on the floor of the fourth ventricle like the stria medullares
were able to be confirmed, but the facial colliculus was not discerned
and the obex was hidden ventral to the tumor. BSM located the facial
Case presentation colliculus near the normal anatomical position, suggesting that there was
no displacement of the upper half of the brain stem (Fig. 6). No EMG
Case 1
response was recorded when the tumor exposed at the caudal end of the
This 35-year-old woman noticed right facial dysesthesia and dysar- fourth ventricle and the dorsal medulla was mapped with the stimulation
thria 2 years ago. Sensory disturbance of the upper extremities and intensity of 2.0 mA. The tumor at the caudal end of the fourth ventricle
dysphagia followed. MRI revealed a tumor located at the dorsal medulla and a part of the dorsal medulla were removed. The second attempt of

Fig. 9. MRI and CT scans of a 4-year-old girl with a recurrent ependymoma. The exophytic tumor located on the dorsal medulla on the floor of the
fourth ventricle

Fig. 10. Intra-operative photographs of case 2. Left: Intra-operative view of the floor of the fourth ventricle before tumor resection. Two exophytic
tumors are observed. Right: BSM located the rt.facial nucleus (asterisk) just beneath a thin layer of the tumor on the upper half of the floor of the
fourth ventricle. The tumor was left untouched for functional preservation of the facial nucleus. Other exophytic tumors were resected
The importance of brainstem mapping in brainstem surgical anatomy

Fig. 11. Result of the intra-operative neurophysiology is shown. Upper left: intra-operative photograph of BSM. The probe is touching the floor of the fourth ventricle where the facial nucleus was located.
Upper center: BSM for searching the CMN. Upper right: BSM for pin point localization of the CMN (Oc Orbicularis Ocuri muscle, Or Orbicularis oris muscle, T Intrinsic tongue muscle). The lower
demonstrates the CBT monitoring during tumor resection. Functional integrity of the bilateral facial and hypoglossal nuclei was monitored and preserved
507
508 N. Morota and V. Deletis

BSM successfully located the hypoglossal nuclei bilaterally and the right prepare for the risk of damaging the CMN at the caudal
glossopharyngeal=vagus nuclei at and near the obex, which became
visible after tumor resection (Fig. 7). Because the pathological report end of the tumor cavity when initial BSM before start-
suggested the tumor as a germinoma, further resection was halted. The ing tumor resection failed to localize the CMN. Three-
patient awoke from surgery following 2 days of respiratory control. dimensional anatomical relationship between the brain
Transient deterioration of dysphagia was observed but no other neuro-
stem lesion and the displaced CMN is the key for safe
logical deficit developed during the hospital stay. Figure 8 demonstrates
the relationship between the brain stem tumor and the CMN in this case brain stem surgery.
(Fig. 8). The basic concept of BSM would be applied for the
other CMN in different locations or other neurophysiol-
ogical modalities [21]. Mapping the occulomotor and
Case 2
trochlear nuclei would be helpful for the midbrain and
This 4-year-old girl underwent gross total resection of an ependy-
moma of the fourth ventricle when she was a year old. The tumor
pineal region surgery [18]. Mapping the corticospinal
recurrence on the floor of the fourth ventricle was depicted on MRI tract using the MEP would be required for midbrain
and surgical resection was scheduled 3 years after the first operation lesions approached by the subtemporal route [3].
(Fig. 9). Intra-operative neurophysiology for the surgery was BSM and BSM is a relatively new neurophysiological procedure
the MEP monitoring of the CMN which we called the corticobulbar tract
(CBT) monitoring [4]. After preparing for BSM and the CBT monitoring but is getting a more and more indispensable tool for
the floor of the fourth ventricle was exposed. Recurrent exophytic safe brain stem surgery [5, 8, 12, 19]. Surgical anatomy
tumors were recognized together with a thin layer of recurrence which of the floor of the fourth ventricle is often distorted and
was not detected on the preoperative MRI on the upper half of the floor
of the fourth ventricle. BSM located the right facial nucleus just beneath difficult to recognize even under microscopic observa-
a thin layer of the recurrent tumor (Fig. 10). It was decided to leave the tion. BSM can disclose the CMN by neurophysiological
thin layer of the tumor and remove the exophytic part of the tumor. The means and transform the surgical anatomy into a func-
CBT monitoring was performed during the tumor resection (Fig. 11).
tional one. The silent area demonstrated by BSM is the
The girl woke up without any sign of the neurological deficit after
surgery. key approach route to the brain stem while preserving
the function of CMN. The true safe entry zone to the
brain stem can be revealed only by BSM.
Discussion
BSM is a neurophysiological technique to localize the References
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Academic Press, New York, pp 319–335 since its introduction more than 15 years ago. One of the authors
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analysis of 75 cases. J Neurosurg 79: 845–852 I agree that MEP and AEP as well as SEP are not very helpful for this
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of the brainstem: experience with 100 patients. J Neurosurg 90: convince definitely those neurosurgeons dealing with brainstem surgery.
50–58 Surgical results can be optimal by performing brainstem mapping.
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47: 1170–1177 Correspondence: Nobuhito Morota, Department of Neurosurgery,
19. Strauss C, Romstock J, Nimsky C, Fahlbusch R (1993) Intraopera- National Children’s Medical Center, National Center for Child Health
tive identification of motor areas of the rhomboid fossa using direct and Development, 1-10-2 Okura, Setagaya-Ku, Tokyo, Japan 157-8535.
stimulation. J Neurosurg 79: 393–399 e-mail: morota-n@ncchd.go.jp