Transcranial magnetic stimulation excites the labyrinthine segment of the facial nerve: An intraoperative electrophysiological study in man

Neuroscience Letters, 124 (199l) 273-276 © 1991 ElsevierScientific Publishers Ireland Ltd. 0304-3940/91/$ 03.50 ADONIS 030439409100060K

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Transcranial magnetic stimulation excites the labyrinthine segment of the facial nerve: an intraoperative electrophysiological study in man U r s D. S c h m i d , A a g e R. M o l l e r a n d J u d i t h S c h m i d Department of Neurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213 (U.S.A.)

(Received 23 November 1990; Revisedversion received 2 January 1991; Accepted 2 January 199I) Key words: Facialnerve; Neurography; Transcranial magnetic stimulation; Electrical stimulation

The site where transcranial magnetic stimulation (magStim) depolarizes the facial nerve was investigated in 6 patients who underwent surgery of the cerebellopontineangle (CPA). The facial nerve was stimulated (1) magneticallyprior to craniotomy, (2) electricallynear the brainstem (elREZ), (3) at the exit from the CPA into the facial canal (elPorus), and (4) in the stylomastoid fossa (elStylo). The range of latency differences(zl) of compound muscle action potentials (CMAPs) recorded from the ipsilateral mentalis muscle were as follows: JelREZ-magStim: +0.5 to + 1.1 ms (P ~<0.03, Wilcoxon test); ,JelPorus-magStim: + 0.2 to + 0.5 ms (P ~<0.03); zlelStylo-magStim: + 0.8 to + 1.0 ms (P ~ 0.03). On the basis of anatomical data and a facial nerve conduction velocity of 33-46 m/s in these patients, it was concluded that transcranial magnetic stimuli depolarized the facial nerve at a location 10-15 mm distal to its entrance into the facial canal. This corresponds to the end of the labyrinthine segment of the facial nerve, i.e. the transit zone where the nerve ceases to be surrounded by cerebrospinal fluid (CSF) with its high electrical conductivity and enters the high-resistancetissue of the petrous bone.

A rapidly varying magnetic field generated by a brief current in a circular coil [1] applied over the parieto-occipital surface of the scalp excites the facial nerve intracranially [2, 9, 16, 17, 19, 21]. However, controversy exists about the exact site o f excitation of the facial nerve along its intracranial course [2, 9, 16, 17, 19, 21]. In view of the future applications o f this technique, the objective of the present study was to determine the site of magnetoelectrical excitation of the facial nerve by transcranial magnetic stimulation of the nerve intraoperatively in patients in w h o m the facial nerve could be stimulated electrically both intra- and extracranially under comparable physiological conditions. Six patients (2 men, 4 women, mean age 45 years, range 36-73 years) who were to undergo posterior fossa microvascular decompression (MVD) operations for hemifacial spasm (HFS) on the right (n = 5) or left (n = 1) side volunteered for this study. Except for the relief of HFS, facial nerve function was clinically the same before and after the operation. An anesthesia technique was used that had been designed especially for facilitating intraoperative m o t o r nerve studies [11-15, 20]. The method used in this study was approved by the InstituCorrespondence: U.D. Schmid, Department of Neurosurgery, University Hospital, CH-3010 Berne, Switzerland.

tional Review Board of the University of Pittsburgh School of Medicine, and the patients gave their informed consent to participation in this study. Transcranial magnetic stimulation was performed with a M A G S T I M 200 ( M A G S T I M C o m p a n y Ltd., Whitland Industrial Estate, Whitland, Dyfed, SA34 O H R , U.K.). A standard circular coil with a mean diameter of 9.0 cm was placed tangentially over the ipsilateral parieto-occipital scalp [2, 9, 16, 17, 19]. The stimulation intensity was increased stepwise until a supramaximal c o m p o u n d muscle action potential (CMAP) was obtained. The current direction in the coil (current flow from positive to negative) was anticlockwise as seen from above when side A of the coil was visible, inducing a clockwise stimulating current in the tissue (and vice versa when side B was visible). The coil orientation with the lowest threshold to excite the facial nerve was used; in accordance with the findings by Rrsler et al. [17], this corresponded to anticlockwise and clockwise current direction in the coil for the left and right facial nerves, respectively. The stylomastoid segment o f the facial nerve was stimulated electrically with a pair of 1-cm long platinum needle electrodes (Type E2, Grass Instruments Co., Quincy, MA); the interelectrode distance was 5--6 mm. The cisternal segment was stimulated with a hand-held m o n o p o l a r stimulation electrode that was insulated

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except for the tip (Grass Instrument Co.), with the return electrode placed subcutaneously near the skin incision [11]. Rectangular pulses of 0.15-ms duration were used at intensities of 25-50 V, and 0.5-1.0 V for supramaxireal stimulation of the stylomastoid and cisternal segments, respectively. CMAPs were recorded with a pair of needle electrodes (Type E2, Grass) placed into the ipsilateral mentalis muscle, with an interelectrode distance of 2-3 cm. Differential amplifiers (System 12, Grass) with filters set at 3 Hz and 3 kHz were used, and CMAPs were recorded on magnetic tape (4-channel FM recorder, Type B, A.R. Vetter Co, Rebersburg, PA) at a tape speed of 15 ips and printed out on a laser printer for offline analysis. Experimental procedure. Electrical stylomastoid and magnetic transcranial stimulations were carried out 2030 min after induction of anesthesia. For operation, the patient was placed in a lateral decubitus position, the head was fixed in a 3-pin headholder, and the CPA was opened by a suboccipital retromastoid approach. Under continuous neuromonitoring [14, 15] the cisternal segment of the facial nerve was microsurgically dissected and stimulated electrically near its root exit zone (REZ) from the brainstem and at the porus as the nerve entered the facial canal. Mean body temperature of the 6 patients, measured preoperatively and again intraoperatively, was 35.6°C; the individual differences in temperatures measured at the two times was between - 0.1 and + 0.4°C. After recordings had been completed, MVD of the facial nerve was performed [5, 6]. No additional neurological deficit was identified after the operation in any patient, and all patients had relief from HFS at the time of discharge from the hospital. Evaluation of the data. The CMAPs evaluation in this study were obtained to electrical or magnetic stimulation at intensities slightly above those needed to yield responses of maximal amplitudes. Baseline-to-peak amplitudes and onset latencies of CMAPs were measured, and arithmetic differences (A) were calculated between CMAP latencies to electrical stylomastoid (elStylo), intracranial proximal (elREZ), and distal facial nerve (elPorus) stimulation, and to magnetic stimulation (magStim). Statistical comparisons were performed using the Wilcoxon test for two matched samples. Mentalis CMAP amplitudes (mean+S.D.) were 2.6 +2.2 mV (magStim), 3.2+2.86 mV (elREZ), 2.6+2.0 mV (elPorus), and 2 . 4 _ 2.2 mV (elStylo), and the amplitude differences between the various stimulation modalities were not significant (P > 0.1, Wilcoxon test) (Fig. 1). CMAP latencies obtained in each individual are shown in Table I; they are comparable to the values obtained by others using transcranial magnetic [9, 17, 19] or elec-

trical stylomastoid [8, 9, 17, 19, 21] stimulation in normal individuals or electrical cisternal stimulation of the facial nerve in patients with HFS [12]. CMAP latencies recorded to transcranial magStim were significantly longer than to elStylo, and - - without exception - shorter than CMAP latencies recorded to any electrical stimulation of the facial nerve intracranially. The differences between latencies of CMAP to magnetic and stylomastoid stimulation (dmagStim-elStylo) were +0.8 to +1.0 ms (P~<0.03, Wilcoxon test), differences were +0.5 to + 1.1 ms (P~<0.03) between latencies of CMAP to magnetic and REZ stimulation (zlelREZ-magStim), and differences were +0.2 to +0.5 ms (P~<0.03) between latencies of CMAP to magnetic and porus stimulation (zJelPorus-magStim) (Table I). The results of the present study provide evidence that magnetic stimulation excites the facial nerve distal to the REZ, and close but distal to its entrance at the porus into the facial canal. In cadavers, the length of the intratemporal course of the facial nerve has been measured to be approximately 30 mm, with 7-16 mm comprising the labyrinthine segment, 8-11 mm the tympanic segment, and 9-11 mm the mastoid segment of the facial nerve [3, 7]. By adding 16 mm (10-21 mm) for the seg-

m,MENTALIS

elStylo

I

;

1.0mV

I

elREZ

elPorus Magstim 0.5mV

i

0.smv

I

I

0

4

6

]

I

I

I

I

I

I

8

10

12

14

16

18

20

ms

Fig. 1. Mentalis C M A P s recorded in response to stimulation of the facial nerve by transcranial magnetic (magStim) and direct electrical stimulation near the root exit zone (elREZ), the porus of the facial canal (elPorus), and the stylomastoid fossa (elStylo).

275 TABLE I LATENCIES AND LATENCY DIFFERENCES (ms) OF MENTALIS CMAPs TO MAGNETIC AND ELECTRICAL STIMULATION, NERVE CONDUCTION VELOCITIES (m/s), AND DISTANCES TO SITES OF EXCITATION BY MAGNETIC STIMULATION AS DETERMINED BY INTRA- AND EXTRACRANIAL ELECTRICAL STIMULATION (mm) OF THE HUMAN FACIAL NERVE Pt.

*Latency

magStim

elREZ

Latency Difference

elPorus

elStylo

zlmagStim- AelPoruselStylo magStim

zlelREZmagStim

NCV AelPoruselStylo

Porus to Stylo

Calculated Distance Porus to magStim

Stylo to magStim

1 2 3 4 5 6

5.4 4.6 4.4 4.3 4.9 5.5

6.5 5.1 5.2 4.9 5.8 6.1

5.8 5.0 4.8 4.5 5.4 5.8

4.5 3.7 3.4 3.5 3.9 4.5

+0.9 +0.9 +1.0 +0.8 +0.9 +1.0

+0.4 +0.4 +0.4 +0.2 +0.5 +0.3

+1.1 +0.5 +0.8 +0.6 +1.0 +0.6

+1.3 +1.3 +1.4 +1.0 +1.4 +1.3

34.3 35.4 33.6 46.0 32.6 35.4

14 14 13 10 15 I0

32 32 33 36 31 36

Mean S.D.

4.8 0.5

5.6 0.6

5.2 0.5

3.9 0.5

0.9 0.1

0.4 0.1

0.8 0.2

1.3 0.1

36.2 4.9

13 2

33 2

*Magnetic stimulation (magStim) and electrical stimulation of the facial nerve at the brainstem (elREZ), at the entrance into the facial canal (elPorus), and in the stylomastoid fossa (elStylo).

ment of the facial nerve between the stylomastoid foramen and the point where the tips of needle electrodes used for recording are placed [18], a length of 46 mm for the facial nerve from the porus to the stylomastoid fossa is obtained. Assuming that the facial nerve conduction velocity (NCV) is uniform between the porus of the facial canal and the stylomastoid fossa, the NCV is estimated to be 34-46 m/s in the 6 patients who participated in the present study, which is within the broad range of NCV reported by others who have studied large series of normal subjects [8, 21]. The information we obtained from each individual regarding facial NCV and latency differences between magStim and either electrical stimulation at the porus (delPorus-magStim) or in the stylomastoid fossa (AmagStim-elStylo) indicates that the magnetic magnetic stimuli excited the facial nerve in an anatomically welldefined area, 10-15 mm distal to the porus, or 31-36 mm proximal to the stylomastoid fossa (Table I). This corresponds to the end of the labyrinthine segment of the facial nerve, i.e., the transit zone where the nerve ceases to be surrounded by CSF with its high conductivity and enters the high-resistance tissue of the petrous bone [7] (Fig. 2). These results, on the one hand, confirm previous findings that transcranial magnetic stimuli applied over the parieto-occipital scalp excite the ipsilateral infranuclear and intracranial portions, rather than the supranuclear or extracranial neural elements, of the facial nerve [2, 9, 16, 17, 19, 21]. On the other hand, our conclusions and those of others [17] stand in contrast to those arrived at by Maccabee and Seki [9, 21] that the site of magnetic

stimulation of the facial nerve is in its REZ. These latter investigators, however, arrived at their conclusions by comparing latencies of CMAPs obtained to magStim with latencies obtained to elStylo, and this method leads to uncertainty in interpretation of results because the method does not involve direct electrical stimulation of the facial nerve at its REZ and at the porus of the facial canal. We conclude that it is n o t possible to study the most proximal part of the facial nerve, i.e., its cisternal segment, with transcranial magnetic stimulation, as would have been most desirable for clinical purposes; this finding is of practical importance because it confirms that slowed facial nerve conduction due to a focal pathology in the CPA will not reliably be detected with facial neurography by transcranial magnetic stimulation [17].

Facial nerve Stylomast

elREZ elPorus

magStim

T

elStylo

Fig. 2. A comparison of latencies of CMAPs (shown in Fig. I and Table I) revealed that magStim excites the facial nerve not in its intracranial or cist(ernal) but in its labyr(inthine) segment in the facial canal, where the nerve ceases to be surrounded by CSF, and proximal to the tymp(anic), mast(oid), and stylomast(oid) segments of the facial nerve.

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Furthermore, central motor conduction time [4] in the facial motor pathways, when determined by transcranial magnetic stimulation of the facial motor cortex and of the intracranial portion of the facial nerve [2, 10, 17], includes conduction time in a considerable segment - approximately 17-30 mm long [7] - - of peripheral nerve. That accounted for 0.5-1.1 ms (A elREZ-magStim, Table I) in the present study. We thank Drs. Jannetta and Jho for permission to study patients who were under their care. This study was supported by the Swiss National Science Foundation (Grant 3.884.1.86), the Swiss Society for Medical-Biological Grants, and the Swiss MS-Society (to U.D.S.), and a grant from the National Institutes of Health (Grant No. 2-R01-NS21378) (to A.R.M.). 1 Barker, A.T., Jalinous, R. and Freeston, I.L., Non-invasive magnetic stimulation of the human motor cortex, Lancet, i (1985) 11061107. 2 Benecke, R., Meyer, B.U., Sch6nle, P. and Conrad, B., Transcranial stimulation of the human brain: responses in muscles supplied by cranial nerves, Exp. Brain Res., 71 (I 988) 623~32. 3 Esslen, E., The Acute Facial Palsies, Springer, Berlin, 1977. 4 Hess, C.W., Mills, K.R. and Murray, N.M.F., Responses in small hand muscles from magnetic stimulation of the human brain, J. Physiol., 338 (1987) 397-419. 5 Jannetta, P.J., Microsurgical exploration and decompression of the facial nerve in hemifacial spasm, Curr. Top. Surg. Res., 2 (1970) 217-220. 6 Jannetta, P.J., In M. Samii and P.J. Jannetta (Eds.), The Cranial Nerves, Springer, Berlin, 1981. 7 Lang, J., Klinische Anatomie des Kopfes, Springer, Berlin, 1981, 386 pp. 8 Ma, D.M. and Liveson, J.A., Nerve Conduction Handbook, F.A. Davis, Philadelphia, 1983. 9 Maccabee, P.J., Amassian, V.E., Cracco, R.Q., Cracco, J.B., and

Anziska, B.J., Intracranial stimulation of the facial nerve in humans with the magnetic coil, Electroencephalogr. Clin. Neurophysiol., 70 (1988) 350-354. 10 Meyer, B.U., Britton, T.C. and Benecke, R., Investigation of unilateral facial weakness: magnetic stimulation of the proximal facial nerve and of the face-associated motor cortex, J. Neurol., 236 (1989) 102-107. 11 Moller, A.R., Evoked Potentials in Intraoperative Monitoring, Williams and Wilkins, Baltimore, 1988. 12 Moller, A.R. and Jannetta, P.J., Preservation of facial function during removal of acoustic neuromas. Use of monopolar constant voltage stimulation and EMG, J. Neurosurg., 61 (1984) 757-760. 13 Moiler, A.R. and Jannetta, P.J., Hemifacial spasm: results of electrophysiologic recording during microvascular decompression operations, Neurology, 35 (1985) 969 974. 14 M~ller, A.R. and Jannetta, P.J., Microvascular decompression in hemifacial spasm: intraoperative electrophysiological observations, Neurosurgery, 16 (1985): 612~18. 15 Moiler, A.R. and Jannetta, P.J., Monitoring facial EMG responses during microvascular decompression operations for hemifacial spasm, J. Neurosurg., 66 (1987) 681~85. 16 Murray, N.M.F., Hess, C.W., Mills, K.R., Schriefer, T.N. and Smith, S.J.M., Proximal facial nerve conduction using magnetic stimulation, Electroencephalogr. Clin. Neurophysiol., 66 (1987) 71. 17 R6sler, K.M., Hess, C.W. and Schmid, U.D., Investigation of facial motor pathways by electrical and magnetic stimulation: sites and mechanisms of excitation, J. Neurol. Neurosurg. Psychiatry, 52 (1989) 1149-1156. 18 Schmid, U.D., Sturzenegger, M., Ludin, H.P., Seiler, R.W. and Reulen, H.J., Orthodromic (intra/extracranial) neurography to monitor facial nerve function intraoperatively, Neurosurgery, 22 (1988), 945-950. 19 Schriefer, T.N., Mills, K.R., Murray, N.M.F. and Hess, C.W., Evaluation of proximal facial nerve conduction by transcranial magnetic stimulation, J. Neurol. Neurosurg. Psychiatry, 51 (1988) 60~6. 20 Sekhar, L.N. and M~ller, A.R., Operative management of tumors involving the cavernous sinus, J. Neurosurg., 64 (1986) 879-889. 21 Seki, Y., Krain, L., Yamada, T. and Kimura, J., Transcranial magnetic stimulation of the facial nerve: recording technique and estimation of the stimulation site, Neurosurgery, 26 (1990) 286-290.