brainstem maping

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

DOI 10.1007/s00701-005-0672-6

Neurosurgical ConceptThe importance of brainstem mapping in brainstem surgicalanatomy before the fourth ventricle and implicationfor 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, Japan2 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

Brain stem mapping (BSM) is an intraoperative neurophysiological

procedure to localize cranial motor nuclei on the floor of the fourth

ventricle. BSM enables neurosurgeon to understand functional anatomy

on the distorted floor of the fourth ventricle, thus, it is emerging as an

indispensable tool for challenging brain stem surgery. The authors

described the detail of BSM with the special emphasis on its clinical

application for the brain stem lesion. Surgical implications based on the

result of brains stem mapping would be also informative before planning

a brain stem surgery through the floor of fourth ventricle.

Despite the recent advancement of MRI to depict the lesion in

the brain stem, BSM remains as the only way to provide surgical

anatomy in the operative field. BSM could guide a neurosurgeon

to the inside of brain stem while preventing direct damage to

the cranial motor nuclei on the floor of the fourth ventricle. It

is expected that understanding its advantage and limitations would

help neurosurgeon to perform safer surgery to the brain stem

lesion.

Keywords: Brain stem; intraoperative neurophysiology; surgery;

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

Introduction

Recent advances in neuro-imaging enabled us to pre-

cisely locate the lesion even in the brain stem which used

to be called ‘‘no man’s land’’. It still poses challenge to

neurosurgeons [1, 3, 7, 9, 15–17]. Understanding the

anatomical relationship between the lesion and vital

structures is the essential for safe surgery [10, 11].

However, what we need to know during brain stem sur-

gery is the surgical anatomy which implies the func-

tional anatomy under an operating microscope. Normal

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)

500 N. Morota and V. Deletis

anatomical landmarks could be distorted by the brain

stem lesion. Intra-operative neurophysiology will help to

reveal functional anatomy [3, 5, 8, 12, 19].

Case discussion

A 29-year-old woman, who had systemic capillary

angioma and suffered from mild mental retardation,

visited our center for progressive left hemiparesis and

right facial palsy. MRI showed a large pontine hema-

toma (Fig. 1) and she was referred to the Department of

Neurosurgery. Since the paresis was progressive, surgi-

cal indication to evacuate and resect the suspected

angioma would be applied for her.

The question that neurosurgeons ask is how to remove

the hematoma while preserving neurological function,

especially the motor function of the cranial nerves.

Conventional intra-operative neurophysiology such as

auditory brain stem response and somatosensory evoked

potential monitoring may help the surgeon. Motor

evoked potential (MEP) monitoring will assure the sur-

geon that the functional integrity of the motor pathway

remains stable [2]. Nevertheless, this information is not

essential for a neurosurgeon who intends to approach the

brain stem lesion through the floor of the fourth ventri-

cle. Information we need is the precise localization of

the cranial motor nuclei (CMN) on the floor of the fourth

ventricle where anatomical landmarks are lost because

of the lesion.

The answer to the first question is brain stem map-

ping (BSM). BSM is a neurophysiological technique

to localize the motor cranial nerve nuclei on the floor

of the fourth ventricle. The patient underwent removal

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)

The importance of brainstem mapping in brainstem surgical anatomy 501

compromising the neurological deficit. Postoperative

neuro-imagings showed satisfactory evacuation of the

hematoma (Fig. 2).

Neurophysiological aspect

BSM enables the surgeon to locate motor cranial nerve

nuclei within the distorted floor of the fourth ventricle

by delivering electrical stimulation through a hand held

mono-polar probe and recording the muscle response by

EMG [3, 12, 13, 19, 20]. It should be confirmed before-

hand that the influence of the muscle relaxant does not

interfere with the EMG recording in BSM. Otherwise,

any type of anesthesia is compatible with BSM.

Standard parameters for BSM is shown below:

Stimulation.

Cathode: hand-held monopolar probe (diameter of

the tip: 0.75 mm)

Anode: cervical muscles in the operative field or Fz

Wave form: square wave, single pulse

Duration of stimulation: 0.2 msec

Frequency: 1.0–4.0 Hz

Intensity: 2.0 mA for screening, then squeeze inten-

sity to detect threshold.

Recording.

Epoch time: 20 msec

Filter: 20–3000 Hz

Amplification: 10.000 times

Muscles for EMG recording:

CMN VII: orbicularis oculi & oris

CMN IX=X: posterior pharyngeal wall or cri-

cothyroid

CMN XII: lateral wall of the intrinsic tongue

muscle

For stimulation, we prefer to use a hand-held mono-

polar probe for precise localization of the CMN. The tip

of the probe is round and of moderate size to prevent

damaging the floor of the fourth ventricle during stimu-

lation. EMG responses are usually recorded by sticking

a pair of needle electrodes to the targeted muscle. The

electrodes should be secured on the face and the lip

tightly before turning the patient to the prone position.

Application during the operation

The threshold intensity depends on the pathology, the

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)


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CMN. In some instances, the threshold could be as low

as 0.2–0.4 mA, which often used during the case with

the brain stem hematoma. Brain stem tumors tend to

require higher threshold intensity up to 2.0 mA. Atten-

tion is paid so as not to stimulate one point more than 5

seconds for safety reasons. After exposing the floor of

the fourth ventricle, a surgeon starts to stimulate the

floor 2.0 mA. Once the muscle response is recorded,

the intensity is squeezed up stepwise to the threshold.

Using the threshold intensity, the CMN can be precisely

located by moving the stimulation probe every 1 mm.

For a neurosurgeon, BSM is a straightforward techni-

que [5, 8, 12, 19]. The presence of the muscle response

directly tells you the CMN there. If expected responses

are not required, there are two possibilities. One is

mechanical failure of the stimulation or recording sys-

tem. The other is that the CMN could be located ventral

to the brain stem pathology. No response does not neces-

sarily mean there is no CMN. Repeated stimulation

through the intra brain stem pathology would be re-

quired to detect the CMN in this situation. This is espe-

cially true in patients with medullary tumor which tends

to grow in an exophytic fashion.

Neurosurgical implication for brain

stem surgery

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.

A medullary tumor enlarges its volume more in an

exophytic fashion than a pontine tumor. The tumor tends

to compress one or some of the lower CMN ventrally,

thus the initial BSM before tumor resection may fail to

locate them. The surgeon should be prepared to repeat

BSM intermittently since the unmapped CMN can be

detected near the bottom of the tumor cavity. Once the

unmapped CMN is located, it is recommended to leave

the rest of the tumor in order to preserve the CMN

function. Interpretation of the result of BSM in a medul-

lary lesion is not simple compared with that of a pontine

lesion, because the functional integrity of the lower

CMN consists of both afferent and efferent pathways

which form a reflex circuit in the brain stem. Preserved

BSM does not mean the lower CMN function is pre-

served. It means the efferent pathway is preserved. Post-

operative dysphagia and dysarthria can develop despite

preserved EMG responses following BSM.

The cervicomedullary junction spinal cord tumor

(CMJ SCT) shows a different displacement pattern. A

CMJ SCT may extend into the fourth ventricle when it is

large [6]. It pushes the lower CMN rostrally. Direct

approach to the rostral end of the tumor through the floor

of the fourth ventricle can damage the lower CMN.

Undermining the floor of the fourth ventricle from the

caudal side enables the surgeon to avoid direct damage

to the lower CMN.

From surgical view point, it would be safe to say that

neurosurgeons should be aware of the risk of damaging

the CMN at the edge of pontine tumors, at the bottom of

Fig. 8. Schematic representation of the result of BSM. The facial nu-

cleus is not displaced in the floor of the fourth ventricle. The hypo-

glossal nuclei were localized ventral to the rostral end of the tumor

which extended into the fourth ventricle


medullary tumors, and at the rostral edge of the CMJ

SCT [14]. This idea will help neurosurgeons to design a

safe surgical approach to the brain stem from the floor of

the fourth ventricle (Fig. 4).

Case presentation

Case 1

This 35-year-old woman noticed right facial dysesthesia and dysar-

thria 2 years ago. Sensory disturbance of the upper extremities and

dysphagia followed. MRI revealed a tumor located at the dorsal medulla

to the upper cervical cord (Fig. 5). On admission, she showed right facial

hypalgesia, left vocal cord palsy and mild left hemiparesis. Tumor

resection with the use of BSM was scheduled. At surgery, the dorsal

medulla to the upper cervical cord showed marked swelling and a part of

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

colliculus near the normal anatomical position, suggesting that there was

no displacement of the upper half of the brain stem (Fig. 6). No EMG

response was recorded when the tumor exposed at the caudal end of the

fourth ventricle and the dorsal medulla was mapped with the stimulation

intensity of 2.0 mA. The tumor at the caudal end of the fourth ventricle

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


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BSM successfully located the hypoglossal nuclei bilaterally and the right

glossopharyngeal=vagus nuclei at and near the obex, which became

visible after tumor resection (Fig. 7). Because the pathological report

suggested the tumor as a germinoma, further resection was halted. The

patient awoke from surgery following 2 days of respiratory control.

Transient deterioration of dysphagia was observed but no other neuro-

logical deficit developed during the hospital stay. Figure 8 demonstrates

the relationship between the brain stem tumor and the CMN in this case

(Fig. 8).

Case 2

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

recurrence on the floor of the fourth ventricle was depicted on MRI

and surgical resection was scheduled 3 years after the first operation

(Fig. 9). Intra-operative neurophysiology for the surgery was BSM and

the MEP monitoring of the CMN which we called the corticobulbar tract

(CBT) monitoring [4]. After preparing for BSM and the CBT monitoring

the floor of the fourth ventricle was exposed. Recurrent exophytic

tumors were recognized together with a thin layer of recurrence which

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

a thin layer of the recurrent tumor (Fig. 10). It was decided to leave the

thin layer of the tumor and remove the exophytic part of the tumor. The

CBT monitoring was performed during the tumor resection (Fig. 11).

The girl woke up without any sign of the neurological deficit after

surgery.

Discussion

BSM is a neurophysiological technique to localize the

CMN on the floor of the fourth ventricle. Even if the

normal anatomy is distorted by a brain stem lesion and

no anatomical landmarks are discerned, it enables the

neurosurgeon to locate the CMN [12–14, 19, 20]. Neu-

rosurgeons can thus avoid direct damage to the CMN

when approaching the lesion across the floor of the

fourth ventricle. This is the advantage of BSM. How-

ever, BSM does have its limitations [12]. It is unable to

monitor the functional integrity of the CBT and the

reflex circuits of the lower CMN. Preserved EMG

responses following BSM does not always promise pre-

served function of the lower CMN. It is unable to moni-

tor the functional integrity of the CMN during tumor

resection. Attention should be paid to the fact that

BSM is a mapping technique and not a monitoring

one. In order to overcome the limitations, combination

with BSM and the CBT monitoring would be the one

future model of intra-operative neurophysiology for the

brain stem surgery.

Understanding typical patterns for the CMN displace-

ment by brain stem lesions will help planning the surgi-

cal strategy [13, 14]. Myelotomy or retraction of the

floor of the fourth ventricle, if required, should be direct-

ed away from the mapped CMN. Neurosugeons can

prepare for the risk of damaging the CMN at the caudal

end of the tumor cavity when initial BSM before start-

ing tumor resection failed to localize the CMN. Three-

dimensional anatomical relationship between the brain

stem lesion and the displaced CMN is the key for safe

brain stem surgery.

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

trochlear nuclei would be helpful for the midbrain and

pineal region surgery [18]. Mapping the corticospinal

tract using the MEP would be required for midbrain

lesions approached by the subtemporal route [3].

BSM is a relatively new neurophysiological procedure

but is getting a more and more indispensable tool for

safe brain stem surgery [5, 8, 12, 19]. Surgical anatomy

of the floor of the fourth ventricle is often distorted and

difficult to recognize even under microscopic observa-

tion. BSM can disclose the CMN by neurophysiological

means and transform the surgical anatomy into a func-

tional one. The silent area demonstrated by BSM is the

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.

References

1. Bricolo A, Turazzi S (1995) Surgery for gliomas and other mass

lesions of the brainstem. Adv Tech Stand Neurosurg 22: 261–341

2. Deletis V (1993) Intraoperative monitoring of the functional integ-

rity of the motor pathways. In: Devinsky O, Beric A, Dogali M (eds)

Electrical and magnetic stimulation of the brain and spinal cord.

Raven Press, New York, pp 201–214

3. Deletis V, Sala F, Morota N (2000) Intraoperative neurophysiolog-

ical monitoring and mapping during brainstem surgery. A modern

approach. Operative technique in Neurosurgery 3: 109–113

4. Dong CCJ, MacDonald DB, Akagawa R, Westerberg B, AlKhani A,

Kanaan I, Hassounah M (2005) Intraoperative facial motor evoked

potential monitoring with transcranial electrical stimulation during

skull base surgery. Clin Neurophysiol 116: 588–596

5. Eisner W, Schmid UD, Reulen HJ, Oeckler R, Olteanu-Nerbe V,

Call C, Kothbauer K (1995) The mapping and continuous monitor-

ing of the intrinsic motor nuclei during brain stem surgery.

Neurosurgery 37: 255–265

6. Epstein FJ, Farmer J-P (1993) Brain-stem glioma growth patterns.

J Neurosurg 78: 408–412

7. Epstein F, Constantini S (1996) Practical decisions in the treatment

of pediatric brain stem tumors. Pediatr Neurosurg 24: 24–34

8. Katsuta T, Morioka T, Fujii K, Fukui M (1993) Physiological

localization of the facial colliculus during direct surgery on an

intrinsic brain stem lesion. Neurosurgery 32: 861–863

9. Konovalov AN, Spallone A, Makhmudov UB, Kukhlajeva JA,

Ozerova VI (1990) Surgical management of hematomas of the

brain stem. J Neurosurg 73: 181–186

10. Kyoshima K, Kobayashi S, Gibo H, Kuroyanagi T (1993) A study of

safe entry zones via the floor of the fourth ventricle for brain-stem

lesions: report of three cases. J Neurosurg 78: 987–993


11. Lang J, Ohmachi N, Lang Sen J (1991) Anatomical landmarks of

the rhomboid fossa (floor of the 4th ventricle), its length and its

width. Acta Neurochir (Wien) 113: 84–90

12. Morota N, Deletis V, Epstein FJ, Kofler M, Abbott R, Lee M,

Ruskin K (1995) Brain stem mapping: neurophysiological lo-

calization of motor nuclei on the floor of the fourth ventricle.


13. Morota N, Deletis V, Lee M, Epstein FJ (1996) Functional anatomic

relationship between brain stem tumors and cranial motor nuclei.


14. Morota N, Deletis V, Epstein FJ (2002) Brainstem mapping.

In: Deletis V, Shils JL (eds) Neurophysiology in neurosurgery.

Academic Press, New York, pp 319–335

15. Pierre-Kahn A, Hirsh JF, Vinchon M, Payan C, Sainte-Rose C,

Renier D, Lelouch-Tubiana A, Fermanian J (1993) Surgical man-

agement of brain stem tumors in children: results and statistical

analysis of 75 cases. J Neurosurg 79: 845–852

16. Pollack IF, Hoffman HJ, Humphreys RP, Becker L (1993) The long-

term outcome after surgical treatment of dorsally exophytic brain

stem gliomas. J Neurosurg 78: 859–863

17. Porter RW, Detwiler PW, Spetzleer RF, Lawton MT, Baskin JJ,

Derksen PT, Zabramski JM (1999) Cavernous malformations

of the brainstem: experience with 100 patients. J Neurosurg 90:

50–58

18. Sekiya T, Hatayama T, Shimamura N, Suzuki S (2000) Intraopera-

tive electrophysiological monitoring of oculomotor nuclei and their

intramedullary tracts during midbrain tumor surgery. Neurosurgery

47: 1170–1177

19. Strauss C, Romstock J, Nimsky C, Fahlbusch R (1993) Intraopera-

tive identification of motor areas of the rhomboid fossa using direct

stimulation. J Neurosurg 79: 393–399

20. Strauss C, Romstock J, Fahlbusch R (1999) Pericollicular

approaches to the rhomboid fossa. Part II. Neurophysiological

basis. J Neurosurg 91: 768–775

21. Suzuki K, Matsumoto M, Ohta M, Sasaki T, Kodama N (1997)

Experimental study for identification of the facial colliculus using

electromyography and antidromic evoked potentials. Neurosurgery

41: 1130–1136

Comment

Brainstem mapping in brainstem surgery has been very important

since its introduction more than 15 years ago. One of the authors

(V. Deletis) is a worldwide authority. Significant improvements in sur-

gical results have been documented by several groups, e.g. in caverno-

mas and tumours, including our group.

I agree that MEP and AEP as well as SEP are not very helpful for this

kind of surgery. The next progress in this field could be expected from

the navigation of fiber tracts (f.i. motor pathways, by diffusion tensor

imaging), since mapping of the nuclei is not monitoring of its intact

network as emphasized by the authors also.

The value of this paper is mainly an educational one with the goal to

convince definitely those neurosurgeons dealing with brainstem surgery.

Surgical results can be optimal by performing brainstem mapping.

Rudolph Fahlbusch

Erlangen

Correspondence: Nobuhito Morota, Department of Neurosurgery,

National Children’s Medical Center, National Center for Child Health

and Development, 1-10-2 Okura, Setagaya-Ku, Tokyo, Japan 157-8535.

e-mail: [email protected]


brainstem maping

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