Electroencephalography and clinical Neurophysiology, 85 (1992) 248-252 © 1992 Elsevier Scientific Publishers Ireland, Ltd. 0924-980X/92/$05.00

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Motor potentials of inferior orbicularis oculi muscle to transcranial magnetic stimulation. Comparison with responses to electrical peripheral stimulation of facial nerve A. Ghezzi, L. Callea, M. Zaffaroni and A. Zibetti Centro Studi Sclerosi Multipla, Ospedale di Gallarate, Uniuersit~ di Milano, 21013 Gallarate (Italy) (Accepted for publication: 24 February 1992)

Summary Magnetic stimulation at the vertex evoked a motor potential (MP) in the inferior orbicularis oculi muscle of 10 healthy subjects with an onset latency of 8-13 msec. Its amplitude increased and its latency decreased when the muscle was contracted: the latency measured 9.5 + 1.3 msec with an intensity of stimulation 10-15% above threshold in the contracted muscle. This MP is secondary to excitation of the motor cortex. With the coil placed over the occipital scalp and the same stimulation intensity, an MP was recorded with an onset latency at 4.5+0.6 msec. This response reflects the activation of the facial nerve root. The peripheral electrical stimulation of the facial nerve at the mandible angle elicited an MP with an onset latency at 3.5 + 0,4 msec. Most records showed the presence of late components at about 30 msec for all types of stimulation. Key words: Brain magnetic stimulation; Facial nerve

I n spite of the large number of studies concerning the recording of motor potentials (MPs) in limb muscles after electrical or magnetic stimulation (MS) of the brain, only a few studies have investigated the MPs in muscles supplied by cranial nerves such as the 5th, 10th, l l t h and 12th (Benecke et al. 1988; Cruccu et al. 1989; Ludlow et al. 1989). Facial nerve conduction has been investigated in animals (Estrem et al. 1990; Haghighi and Estrem 1990) and in human subjects to MS of the posterior or parietal-posterior scalp (Maccabee et al. 1988; Schriefer et al. 1988): an MP could be elicited in the orbicularis oris or inferior orbicularis oculi muscle (lOOM) with onset latency at 4-5 msec, because of activation of the facial nerve root. These studies failed to demonstrate the possibility to excite the cortico-bulbar pathway. On the contrary, motor cortex stimulation was obtained by Benecke et al. (1988), R6sler et al. (1989) and Cruccu et al. (1990) with a different coil position over the scalp, resulting in an MP at about 10 msec. A similar latency was recorded by Cohen and Hallett (1988) in lower facial muscles with transcranial electrical stimulation. As the position of the coil is relevant in exciting the facial nerve rather than the supra-nuclear fibres, our study was undertaken to evaluate the MP characteris-

Correspondence to: Angelo Ghezzi, Centro Studi Sclerosi Multipla, Via Pastori 4, Ospedale di Gallarate, 21013 Gallarate (Italy).

tics after MS, placing the coil over the vertex, the occipital and the parietal scalp. The effects of coil current direction and of muscle contraction were also evaluated. Results were finally compared with t h e MP latency to peripheral electrical stimulation of the facial nerve.

Subjects and methods Ten healthy subjects (6 females, 4 males) took part in the study. Their ages ranged from 18 to 45 years (mean 29.5). MPs were recorded from l O O M using a surface A g / A g C I electrode referred to the nasal bridge. MS was performed by a Novametrix Magstim 200 device, placing the centre of the coil (mean diameter 9 cm) tangentially over the vertex, over the occipital scalp (3 cm above inion) and over the parietal scalp (8 cm lateral and 3 posterior to Cz). The intensity started from 40% and was increased to 100% of the maximum output (1.5 Tesla at the centre of the coil). Bandpass: 1-2000 Hz. Responses were recorded in relaxed muscles, then subjects were asked to contract the lOOM. MS was performed with coil currents flowing both clockwise and counter-clockwise, by turning the coil. The effects of muscle contraction and of coil current direction were evaluated, setting the intensity at 1015% above motor threshold. At least 4 responses were

MP C H A R A C T E R I S T I C S A F T E R M A G N E T I C S T I M U L A T I O N

recorded and superimposed for each stimulation condition (site, intensity, muscular status and coil current direction). The facial nerve was electrically stimulated near the stylomastoid foramen: square wave supramaximal stimuli of 0.1 msec duration were delivered through bipolar surface electrodes 1.5 cm apart, the cathode being distal, below the ear and anterior to the mastoid process. Bandpass 20-5000 Hz.

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INTENSITY Results

Magnetic stimulation at the vertex elicited an MP (V-MP) with an onset latency of 8-13 msec. Amplitude and latency changed in relation to stimulation intensity and muscle contraction whereas current flow direction had no effect (Fig. 1 and Table I). In most records the V-MP was preceded by an early wave at 4.4 + 0.7 msec. It was hardly recognizable in some instances because of the small amplitude. Unlike V-MPs this wave was not modified by muscle contraction; its amplitude was increased by using clockwise coil current in the right l O O M (Fig. 1) and by reversing the coil in the left side. The V-MP was followed by a late potential starting at 30.5 + 3.3 msec and lasting 10-30 msec (Fig. 1). This component was barely modified by muscle contraction, intensity or coil current direction. With the coil over the occipital scalp and an intensity 10-15% above the motor threshold, we recorded a response at 4.5 + 0.6 msec. This wave was not modified by muscle contraction; its amplitude was increased both on the right side with coil currents flowing counter-clockwise (from 1.5 + 0.7 to 2.9 + 0.8 mV) and on the left side when the coil was reversed (Fig. 2a). A late component a p p e a r e d at 27.8 + 3.6 msec. By stimulating over the parietal scalp an MP was recorded with onset at 4.4 + 0.2 msec: in some records this component was preceded by a wave at 3-3.5 msec (Fig. 2b), in some others the latency decreased to 3-3.5 msec when

TABLE I Latency and amplitude of V-MP in relation to coil current direction (only for the right muscle), muscle contraction and stimulus intensity.

Coil current direction a Muscle a Stimulation intensity

Latency (msec)

Amplitude (mV)

clockwise counter-clockwise relied contracted

9.5±1.3 9.4±1.3" 11.2±1.6 9.5±1.3"*

1.5±0.6 1.5±0.7" 0.7±0.5 1.5±0.6"*

70% 100%

11.8±1.4 9.9±1.4"*

0.7±0.5 1.1±0.6"*

Fig. 1. Motor potentials to transcranial magnetic stimulation at vertex in relation to muscle contracting status, intensity of stimulation and direction of current in the coil. An early wave is recognizable in the first 5 msec. The circle indicates the V-MP onset. Late components are present in all records with onset at about 30 msec.

the centre of the coil was lowered towards the ear (Fig. 2c). The MP latency to electrical stimulation at the mandible angle was 3.5 + 0.4 msec. Responses were followed in ipsilateral and contralateral records by a late component with onset at 26.7 +2.1 msec and 27.1 + 2.5 msec respectively. An example is given in Fig. 2.

Discussion

Paired t test: * n.s.; ** P < 0.01. a Intensity > 10-15% threshold.

The MS of the cerebral cortex with the coil at the vertex elicited an MP in the inferior orbicularis oculi muscle, supplied by the facial nerve, with a latency of about 10 msec. The latency decreased and the amplitude increased when the intensity of stimulation was raised and facial muscles were contracted. The facilitation provoked by muscle contraction suggests that the

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Fig. 2. Motor potentials of the right l O O M to transcranial magnetic stimulation (left) and electrical stimulation of the facial nerve at the stylomastoid foramen (right). a: different amplitude of occipital MPs in relation to coil current direction, b: 2 different kinds of response to magnetic stimulation over the parietal scalp, with an early wave at 3.5 msec in the lower trace, c: further evidence of an MP at about 3.5 msec, with the coil moved toward the ear. d: MP to electrical stimulation of the facial nerve (top) and the late ipsi- and contralateral components (bottom).

V-MP is elicited by activation of the descending cortico-bulbar pathway (Merton et al. 1982). Our results confirm previous reports demonstrating the possibility of exciting the cortico-bulbar pathway (Benecke et al. 1988; R/Ssler et al. 1989; Cruccu et al. 1990) and emphasize the relevance of coil position to obtain it. Current flow direction (and consequently the stimulation of either hemisphere) did not modify latency and amplitude of the V-MP, according with the finding that upper facial motor neurones are supplied by bilateral cortico-bulbar projections. Similarly, bilateral and large responses were recorded by Cruccu et al. (1990) in the frontalis muscles to MS delivered by a Novametrix device. In the lower facial muscles, MPs were merely recorded following contralateral electrical stimulation of the temporal cortex (Cohen and Hallett 1989) whereas results to MS are controversial: with the coil 4 cm lateral to the vertex, both contralateral (Cruccu et al. 1990) and bilateral (Benecke et al. 1988) MPs have been recorded. On the contrary, R6sler et al. (1989) found that current flow direction rather than the positioning of the coil was critical, counter-clockwise stimuli being more effective in stimulating the right facial nerve and vice versa, though the effect of current flow direction was not systematically investigated in this study. From these data it is not clear whether lower facial motor neurones also receive an ipsilateral cortico-bulbar projection, as observed in the monkey

(Jenny and Saper 1987), unless a more focal cortical stimulation is performed (i.e., with a figure-8 coil). On the contrary, bilateral MPs have been recorded in muscles supplyed by cranial nerves other than the 7th (the masseter - - Benecke et al. 1988; Cruccu et al. 1989; the genioglossus and sternocleidomastoideus - Benecke et al. 1988; the thyroarytenoid and cricothyroid - - Ludlow et al. 1989) reflecting the presence of a bilateral cortico-bulbar projection to motor neurones. Results on facial muscle MPs do not confirm the finding of hemispheric dominance observed by Ludlow et al. (1989) in laryngeal muscles. The V-MP was preceded by an early small amplitude wave at 4.4 + 0.7 msec. This wave was better defined on the right side to clockwise stimuli and vice versa. We obtained a wave with a similar latency but a larger amplitude by placing the coil tangentially over the occipital scalp, with currents flowing counter-clockwise for the right l O O M and clockwise for the left side: a similar finding was observed by R6sler et al. (1989) and by Schriefer et al. (1988). The effect of coil current direction is well known when stimulation of spinal roots is performed using a stimulator with a monophasic configuration of the magnetic pulse instead of a polyphasic one (Cros et al. 1990). For this reason current direction did not modify MP characteristics in the study of Maccabee et al. (1988), who employed a Cadwell stimulator.

MP CHARACTERISTICS AVFER MAGNETIC STIMULATION

The occipital MP latency of our study is comparable with the value of 4.8 msec recorded by R6sler et al. (1989) in the nasalis muscle and of 5.1 msec recorded by Schriefer e t a l . (1988) in the orbicularis oris muscle, both with a similar coil position. It is unclear whether this wave follows activation of the facial nerve at its exit from brain-stem (Estrem et al. 1990) or at its entrance into the internal auditory meatus (Schriefer et al. 1988; R6sler et al. 1989). The MP obtained after stimulation of the parietal scalp presented the same latency as the occipital MP. However, it is of practical importance to observe that the onset of the parietal MP was sometimes less defined than that of the occipital one or masked by a more precocious wave at about 3.5 msec, particularly when the coil was lowered toward the ear. This component probably reflects the activation of the facial nerve at the stylomastoid foramen, taking into account that a similar latency was obtained with peripheral electrical stimulation of the facial nerve (3.5 + 0.4 msec), in agreement with other literature reports (Schriefer et al. 1987; Maccabee et al. 1988; R6sler et al. 1989; Cruccu et al. 1990). Assuming that MS over the occipital cortex activates the facial nerve root, it is possible to calculate the central motor conduction time, by subtracting the latency of occipital MPs from that of V-MPs, and the transosseal conduction time, by subtracting the latency of MPs evoked by peripheral electrical stimulation from that of occipital MPs. The former time measured 6.6 + 1.7 msec in the relaxed and 5.0 + 1.2 msec in the contracted muscles, the latter time measured 1.0 + 0.1 msec (1.3 in Schriefer's study, 1988, 1.2 msec in R6sler's, 1989). An identical central conduction time was found by R6sler et al. (1989) and by Cruccu et al. (1990): as observed by Cruccu et al. (1989), the central conduction time of fibres supplying trigeminal motor neurones is 1.5 msec shorter, probably because of their different threshold. This finding might also depend on the fact that ceils of the facial nucleus are supplied by a di- or polysynaptic pathway from the motor cortex (Tanaka 1976) or it might reflect the different arrangements of facial motor fibres within the brain-stem (Brodal 1981). A late and long-lasting component was recorded in most cases at about 25-30 msec. Maccabee et al. (1988) stated that this could represent a polysynaptic reflex induced by sensory activation or by a spindlemediated reflex response to contraction of muscles of mastication. The late components have a latency similar to the R2 latency of the blink reflex, so they could be elicited by stimulation of the sensory 5th root; moreover, it has been shown that the R2 component can be affected by lesions of the cortico-bulbar pathway, because of loss of control on the lateral reticular formation (Ongerboer de Visser and Kuypers 1978; Dengler et al. 1982). The late components could also

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reflect the activation of cortico-bulbar fibres, via the lateral reticular formation, at least for MS over the vertex. The results of our study may be of interest in clinical practice: it has been shown that it is possible to assess the motor conduction from cortex to l O O M , from facial nerve root and from stylomastoid foramen to l O O M : in this way it should be possible to assess the site of facial nerve lesions in pathological conditions.

Note

It has been recently demonstrated (Chiappa et al., Neurology, 1991, 41: 1155) that current direction of the Novametrix Magstim device is erroneously reported in the user's manual. To avoid possible problems of comparison with previous studies, we did not change the direction of current flow in the present study.

References Benecke, R., Meyer, B.U., Sch6nle, P. and Conrad, B. Transcranial magnetic stimulation of the human brain. Exp. Brain Res., 1988, 71: 623-632. Brodal, A. Neurological Anatomy in Relation to Clinical Medicine. Oxford University Press, Oxford, 1981. Cohen, L.G. and Hallett, M. Non-invasive mapping of human motor cortex. Neurology, 1988, 38: 904-909. Cros, D., Chiappa, K.H., Gominak, S., Fang, J., Santamaria, J., King, P.J. and Shahani, B.T. Cervical magnetic stimulation. Neurology, 1990, 40: 1751-1756. Cruccu, G., Berardelli, A., Inghilleri, M. and Manfredi, M. Functional organization of the trigeminal motor system in man. Brain, 1989, 112: 1333-1350. Cruccu, G., Berardelli, A., lnghilleri, M. and Manfredi, M. Corticobulbar projections to upper and lower facial motor neurones. A study by magnetic transcranial stimulation in man. Neurosci. Lett., 1990, 117: 68-73. Dengler, R., Kossev, A., Gippner, C. and Struppler, A. Quantitative analysis of blink reflexes in patients with hemiplegic disorders. Electroenceph. clin. Neurophysiol., 1982, 53: 513-524. Estrem, S.A., McCormack, T., Haghighi, S.S. and Potter, T. A comparison of magnetic and electrical stimulation of facial nerve at the cerebello-pontine angle in the dog. Electroenceph. clin. Neurophysiol., 1990, 75: 558-560. Haghighi, S.S. and Estrem, S.A. Estimation of facial central motor delay by electrical stimulation of the motor cortex of the dog. Electroenceph. clin. Neurophysiol., 1990, 75: 82-87. Jenny, A.B. and Saper, C.B. Organization of the facial nucleus and corticofacial projection in the monkey: a reconsideration of the upper motor neurone facial palsy. Neurology, 1987, 37: 930-939. Ludlow, C.B., Cohen, L.G., Hallett, M. and Sedory, S.E. Bilateral intrinsic laryngeal muscle response to transcranial magnetic stimulation with left hemisphere dominance. Neurology, 1989, 39 (Suppl.1): 376. Maccabee, P.J, Amassian, V.E., Cracco, R.Q., Cracco, J.B. and Anziska B. Intracranial stimulation of facial nerve in humans with the magnetic coil. Electroenceph. clin. Neurophysiol., 1988, 70: 350-354.

252 Merton, P.A., Morton, H.B., Hill, D.K. and Marsden, C.D; Scope and technique for electrical stimulation of human brain, spinal cord and muscle. Lancet, 1982, ii: 597-600. Ongerboer de Visser, B.W. and Kuypers, H.G.J.M. Late blink reflex changes in lateral medullary lesions. An electrophysiological and neuro-anatomical study of Wallenberg's syndrome. Brain, 1978, 101: 285-294. R6sler, K.M., Hess, C.W. and Schmid, U.D. Investigation of facial

A. GHEZZI ET AL. motor pathway by electrical and magnetic stimulation: sites and mechanism of excitation. J. Neurol. Neurosurg. Psychiat., 1989, 52: 1149-1156. 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. Psychiat., 1988, 51: 60-66. Tanaka, T. Pyramidal activation of the facial nucleus in the cat. Brain Res., 1976, 103: 389-393.

Motor potentials of inferior orbicularis oculi muscle to transcranial magnetic stimulation. Comparison with responses to electrical peripheral stimulation of facial nerve.

Magnetic stimulation at the vertex evoked a motor potential (MP) in the inferior orbicularis oculi muscle of 10 healthy subjects with an onset latency...
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