82
Electroencephalograpt~' and clmtcal Neuropt[;siology, 1990, 75:82 87
Elsevier Scientific Publishers Ireland. Ltd. EEG 89017
Estimation of facial central motor delay by electrical stimulation of the motor cortex of the dog Siavash S. Haghighi and Scott A. Estrcm
*
Divisions of Neurological Surge 0, and * Otolaryngologo;, University of Missouri-Columbia. Columbia. MO 65202 ( U. S.A,)
(Accepted for publication: 25 June 1989)
Summa 0' Central delay time (CD) has been estimated for activation of limb muscles by electrical or transcranial magnetic coil t.TMC) stimulation of motor cortex and ventral root outflow. In the present study, we used surface electrical stimulation of the motor cortex of the right hemisphere to produce evoked compound muscle action potentials (CMAP) from the contralateral orbicularis oris (o.r.), and orbicularis ~xzuli(o.c.), in dogs. Monopolar electrical stimulation of the facial nerve at the cerebel!o-pontine (CP) angle yielded CMAP activation of ipsilateral facial muscles. These latencies when subtracted from those obtained by direct cortical stimulation established CD for activation of the seventh cranial nerve. Preliminary data with single pulse magnetic stimulation at high outputs ~ > 80%) revealed CMAP with onset latencies similar to the direct facial nerve stimulation at the CP angle by electrical means. Key words: Facial nerve; Central delay time; Cortical stimulation: Compound muscle action potential: Transcranial magnetic
stimulation
The technique of p e r c u t a n e o u s electrical or magnetic stimulation of the motor cortex has provided clinicians with an o p p o r t u n i t y to objectively study the descending m o t o r tracts in awake hum a n subjects ( H a s s a n et al. 1985; Barker et al. 1986; R o b i n s o n et al. 1988). M e r t o n et al. (1982) described transcranial s t i m u l a t i o n of the motor cortex utilizing a high voltage single pulse electrical stimulus. This technique was later used in patients with clinically diagnosed multiple sclerosis ( C o w a n et al. 1984; Berardelli et al. 1988). They estimated the central delay time (CD) by s u b t r a c t i n g the peripheral c o n d u c t i o n time, estimated by s t i m u l a t i o n of the ventral roots of the cervical spine, and recording peripherally from the same muscle group. The clinical utility of the
Correspondence to: Siavash S. Haghighi, D.V.M., Ph.D., Division of Neurological Surgery, N 522-Surgery, University of Missouri-Columbia,One Hospital Drive, Columbia, MO 65202 (U.S.A.).
transcranial magnetic coil ( T M C ) s t i m u l a t i o n has been recently d e m o n s t r a t e d (Barker et al. 1986). Benecke et al. (1988) a n d Maccabee et al. (1988) reported i n t r a c r a n i a l s t i m u l a t i o n of the facial nerve in h u m a n s with the T M C stimulation. They postulated that the location of the n e u r o n a l activation was at the facial nerve outflow from the b r a i n stem. Other authors also evaluated facial nerve activation in m a n by the T M C stimulation. They presented evidence that the l a b y r i n t h i n e segment of the facial canal was the p r o b a b l e site of the nerve stimulation ( M u r r a y et al. 1987; Schriefer et al. 1988). The objectives of the present study were twofold. First, electrical s t i m u l a t i o n was p e r f o r m e d in order to m a p the facial representation of the motor cortex a n d to record the evoked c o m p o u n d muscle action potentials ( C M A P s ) from the facial musculature in dogs. The second goal was to determine the C D for the facial nerve p a t h w a y by electrical stimulation. A c o m p a r i s o n with magnetic stimulation will briefly be discussed.
0013-4649/90/$03.50 ~'~,1990 Elsevier Scientific Publishers Ireland, Ltd.
FACIAL CENTRAL MOTOR CONDUCTION TIME Materials and methods Six mongrel dogs, weighing from 21.5 to 24.5 kg and selected randomly for sex, were used for this study. Each dog was premedicated with atropine sulfate (0.02 m g / k g ) and Innovar Vet (0.09 ml/kg). Halothane and oxygen mask induction was used which allowed intubation and replacement by methoxyflurane, oxygen anesthesia. An intravenous catheter was inserted for infusion of fluids. For continuous blood pressure measurements and blood gas sampling, a catheter was placed in a femoral artery. Arterial blood gases were taken frequently and were maintained within the physiological range. Electrocardiogram and rectal temperature were monitored continuously. For the electrical stimulation, a midline fronto-occipital incision was made. A large portion of the right frontal and parietal areas was exposed with incision of the dura. The dural flap was reflected medially and sutured over the midline sagittal sinus in order to have ample access to the medial surface of the motor cortex. W a r m mineral oil was applied to keep the brain moist and to reduce electrical current spread during the motor cortex stimulation. A silver ball electrode (0.5 m m in diameter) was positioned directly on the motor areas of the brain overlying the facial representation. The cathodal disk electrode was placed subcutaneously on the midline plane, 4 - 5 cm anterior to the silver ball anodal lead. To stimulate electrically the motor cortex, a constant voltage stimulator was used in conjunction with a stimulus isolation unit (Models $88 and SIU 8T, Grass Instruments, Quincy, MA). Repetitive electrical pulses (20-30 Hz at 0.2 msec duration) of amplitude 10-20 V or single pulses (0.2 msec duration) of high voltage (30-50 V) were used on the cortical surface. The left facial nerve was exposed in the CP angle through a suboccipital craniotomy under microscopic observation. To stimulate the facial nerve at the CP angle, single 0.1-0.2 msec rectangular pulses at 2 - 5 V intensities were used. Graded electrical stimulation, from threshold to supramaximal levels, was performed for the facial nerve. Concentric bipolar electrodes (Teca Corporation, Pleasantville, NY) were inserted in the con-
83 tralateral left orbicularis oculi (o.c.), and orbicularis oris (o.r.) muscles. Insertional muscle activity insured proper placement of the recording needles. An evoked potential averager (Cadwell Instruments, Kennewick, WA) was used for recording purposes. The high and low cut-off filters were set at 10 kHz and 300 Hz, respectively. The far-field myogenic or neurogenic sources were minimized by using concentric bipolar electrodes which are reported to record signals generated predominantly by the closest muscle fibers (Nandedkar et al. 1988). The latencies of the muscle responses were calculated from the start of the electrical shock artifact to the onset of the evoked compound action potential. For measurement of the E M G latencies, several consecutive responses were recorded to insure the reproducibility of the responses. A representative trace was accepted for latency measurements and stored for further analysis. The T M C stimulation was performed using a neuromagnetic stimulator (Cadwell Instruments, Kennewick, WA). The coil had an outside diameter of 9.5 cm and 2.2 (max) Tesla output. The C M A P to magnetic pulses were recorded both before and after craniotomy. The T M C stimulation was performed using variable orientations of the stimulating coil to the underlying skull and different output intensities. Euthanasia was carried out with an overdose of pentobarbital sodium (i.v.) under deep anesthesia after termination of the experiments.
Results Threshold stimulation with repetitive pulsing allowed us to map the facial area of the motor cortex. This area appeared more medial (Fig. 1) than what has been depicted in canine textbooks (Redding 1978). The facial movements were restricted to anodal stimulation of the anterior and posterior sigmoid gyri. The threshold repetitive stimulation allowed discrete contralateral facial muscle movement related closely to the d e p t h of anesthesia. Movement of the ipsilateral facial musculature also occurred, being predominant at the deeper level of anesthesia. Comparison of
S.S. HAGHIGHI, S.A. ESTREM
84
I
=I
,ooo.vl
,
I L
500 IJV l _ _ 1
L 0
I 1
I 2
11 3
t 4
I 5
I 6
1 7
msec
I 8
I 9
I 10
Fig. 2. The evoked compound muscle action potential (CMAP) of the orbicularis oculi in response to the electrical stimulation of the facial motor cortex (upper trace) is compared with the CMAP elicited by the cerebello-pontine angle stimulation of the facial nerve (lower trace).
Fig. 1. Location of area (cross-hatched) in the cerebral cortex of the dog that produces facial movements when stimulated electrically. The facial representation in our study is located more medially (A) compared with previous reports (B). (Modified from Hoerlein, B.F., Canine Neurology. Saunders, Philadelphia, PA, 1978.)
500 pv l__
C M A P of the facial m u s c u l a t u r e to the electrical s t i m u l a t i o n of the facial m o t o r cortex a n d the single pulse s t i m u l a t i o n of the nerve at the C P angle depicted the delay for the facial nerve (Figs. 2 a n d 3). T h e CP angle electrical s t i m u l a t i o n of the facial nerve yielded C M A P s with latency a n d a m p l i t u d e similar to those o b t a i n e d by the single electrical shocks to the facial cortex at high intensities. This seemed to i m p l y that current spread activated the i n t r a c r a n i a l segment of the facial nerve at its exit from the b r a i n - s t e m preferentially over true cortical activation. Sectioning of the facial nerve at the C P angle or facial nerve block at the stylomastoid (SM) f o r a m e n abolished the evoked electromyographic responses following electrical stimulation
t
0
I 2
I 4
I 6
I
tl
8
10
I
I
12
14
I 16
I 18
I 20
Upper: direct cortical stimulation Lower: facial nerve stimulation Fig. 3. Comparison of the evoked CMAP of the orbicularis oris to the electrical stimulation of the facial motor area (upper trace) and the single pulse electrical stimulation of the facial nerve at the cerebello-pontine angle (lower trace).
FACIAL CENTRAL MOTOR CONDUCTION TIME
LEFT
L (C-P Angle)
sopv~ _ a ms~
orblcullrls ocull
L~v.~ f ~ / ~
A/'~,_."
TABLE I Electrical stimulation ......
Magnetic stimulation (100%)
orblculerls orls
i
~-
85
vll[jl/~vrll-,V~f~rvv-~.
Comparison of the evoked compound muscle action potential lateneies of orbicularis oculi (o.c.), and orbicularis ores (o.r.) to facial nerve stimulation at the cerebello-pontine angle and motor cortex electrical stimulation.
Electrical stimulation
Motor cortex
Magnetic stimulation
o.
(too~)
Fig. 4. Comparison of the evoked compound muscle action potential of the orbicularis oeuli, and orbicularis otis to high intensity transcranial magnetic stimulation and the single-pulse electrical stimulation of the facial nerve at the cerebello-pontine angle.
oculi 5 4 5.08 3.58 3.5 4
o.
of the motor cortex. However, after the complete facial nerve transection at the CP angle in one dog, facial CMAP could be elicited with the high intensity magnetic stimulation with the coil positioned over the occipito-temporal region. The TMC stimulation at high outputs ( > 80%) elicited CMAP from facial musculature which was similar in onset latency to that obtained by facial nerve stimulation at the CP angle, again suggesting facial nerve activation rather than facial cortical activation (Fig. 4). Interestingly, the TMC stimulation at the retromandibular region (that is, near the SM foramen), at high outputs ( > 80%), could evoke shorter latency muscle response compared with those evoked at the lower magnetic intensities. This presumably implied that the magnetic stimulation at high intensities activated more distal segments of the nerve by the stimulus current spread (Fig. 5).
LEFT LEFT Levator nasolabialis
CP angle
CD
3.41 3.5 4 3.08 2.8 3.5
1.59 0.5 1.08 0.5 0.7 0.5
6.3 5.16 5.4 6.4 2.9 9.66
0.91 1.16 1.4 1.3 1.7 1.84
ores
7.21 6.33 6.8 7.7 4.6 11.5
C D ~ central delay. Values axe in milliseconds.
Table I summarizes the onset CMAP latencies of the o.c. and o.r. to the intracranial stimulation of the facial nerve at the CP angle and the cortical facial motor latencies obtained by electrical stimulation. The CD, determined with electrical stimulation, ranged from 0.5 to 1.59 msec for o.c., and from' 0.91 to 1.84 msec for o.r. muscles. The magnetic stimulation revealed similar latencies of the facial musculature. Single-shock TMC stimulation produced consistent facial muscle activation with the onset latencies dependent upon the position of the magnetic coil with respect to the underlying skull and
St ylomalltoid foramen 50%
LEFT
~ J ,
I~ / V W ~ , ~ . - - . . , ~ . _
Levator naaolablalls
Midltne frontal Midllne OCCipital
40%
3O% Fig. 5. Evoked C M A P of the left levator n~selabialis muscle to the transcr~dal magnetic stimulation at different intensities. Magnetic coil is placed at the left retromandibular region. Higher magnetic intensity activa~s the distal segments of the facial nerve through stimulus spread.
~ ~ ~
Left styl . . . . told
Fig. 6. Evoked C M A P of the levator nasolabialis muscle to the transcranial magnetic stimulation. Onset latency and general configuration of the evoked response are dependent upon the position of the magnetic coil on the skull.
86
the intensity of the T M C stimulation (Fig. 6). The CMAPs recorded before and after craniotomy did not change with the magnetic stimulation. Tangential (flat) positioning of the magnetic coil over the occipital midline parallel to the atlanto-occipital (AO) axis, revealed higher amplitude CMAP. Orthogonal positioning of the coil at a 45 ° angle to the axis produced lower amplitude muscle response. Perpendicular positioning of the coil to the AO axis did not elicit any E M G response.
Discussion Using repetitive electrical stimulation of the facial motor cortex, we mapped out the facial representation within the motor cortex of the dog. Previous work on the motor cortex representation in dogs depicts the facial area on the precruciate sulcus (Redding 1978). The facial motor area appeared to be more medially located, toward the interhemispheric fissure, in our investigation (Fig. 1). This discrepancy may be due to the stimulation methodology. The anesthetic agent and depth of anesthesia also play important roles for motor mapping. It is widely believed that intravenous anesthetics such as barbiturates suppress neuronal activities at the synaptic level within the central nervous system (Stoelting and Miller 1984). We observed the same phenomenon with the methoxyflurane anesthesia. The contralateral CMAPs were more dominant at the lighter stage of anesthesia. The evoked facial E M G to electrical stimulation at the CP angle was similar to that obtained by high intensity single cortical stimulations. We postulate that the latter is the result of electrical current spread to the facial nerve proper without being conveyed through the central facial pathways. The CD for the descending pathways and its clinical significance for determining certain central nervous system disease have been described previously for the spinal cord (Cowan et al. 1984; Snooks and Swash 1985). The normative range for the C D of the long descending tracts has been
S.S. H A G H I G H I , S.A. ESTREM
reported (Cowan e t a [ . 1984; Hess et al. 1986: Berardelli et al. 1988). This central delay has been reported to be 4.3 msec for the upper limbs and 9.3 for the lower limbs (Hugon et al. 1988). The only study on the transcranial activation of the corticobulbar fibers by magnetic stimulation is given by Benecke et al. (1988). They reported 6 msec C D for the corticobulbar segment of the facial nerve in man using magnetic stimulation. Several experimental studies have also been attempted utilizing the retrograde activation of the corticobulbar fibers by intracortical microstimulation methods (Dubner and Sessle 1971: Sirisko and Sessle 1983). Our investigation revealed a wide range of conduction delay for the facial musculature. This range varied from 0.5 to 1.59 msec for o.c., and from 0.91 to 1.84 msec for o.r. muscles. Based on the retrograde activation of corticobulbar fibers in monkeys, Sirisko and Sessle (1983) described a similar wide range of the central delay for the facial nerve. The difference in the central delay of the o.c. and the o.r. muscles in our study is remarkable. We postulate that this is presumably due to the difference in the intracranial length of the corticobulbar fibers for the o.c. and o.r. muscles. In this investigation, we have had the advantage of direct access to the CP angle for electrical stimulation of the facial nerve. We have demonstrated that the C M A P recorded with the magnetic stimulation at high intensities is similar to that of the CP angle electrical stimulation in our experimental model. This implies that T M C stimulation activates the intracranial segment of the nerve similar to the single-shock electrical stimulation of the nerve at brain-stem. Using magnetic stimulation in humans, Maccabee et al. (1988) and Schriefer et al. (1988) have reached a similar conclusion. We have also shown that the high electrical intensities applied to the motor cortex can directly activate the peripheral component of the facial nerve as the result of electrical current spread to the brain-stem region. Magnetic stimulation seems to have advantages over the conventional electrical stimulation of the facial nerve since it evaluates the more proximal segments of the nerve. The T M C stimulation may also be helpful in localizing facial nerve injuries
FACIAL CENTRAL MOTOR CONDUCTION TIME
along its neural pathway based on latency differences. We would like to thank Prof. V.E. Amassian for his helpful comments. We also thank Bridget Crabtree, Janet Sapp, and Becky Roberts for preparation of the manuscript and Charlene Saunders for the illustrations.
References Barker, A.T., Freeston, I.L., Jalinous, R. and Jarratt, J.A. Clinical evaluation of conduction time measurements in central motor pathways using magnetic stimulation of human brain. Lancet, 1986, 2: 1325-1326. Benecke, R., Meyer, B.U., Schonle, P. and Conrad, B. Transcranial magnetic stimulation of the human brain: responses in muscles supplied by cranial nerves. Exp. Brain Res., 1988, 71: 623-632. Berardelli, A., Inghilleri, M., Cruccu, G., Fornarelli, M., Accornero, N. and Manfredi, M. Stimulation of motor tracts in multiple sclerosis. J. Neurol. Neurosurg. Psychiat., 1988, 51: 677-683. Cowan, J.M.A., Dick, J.P.R., Day, B.L., Rothwell, J.C., Thompson, P.D. and Marsden, C.D. Abnormalities in central motor pathways conduction in multiple sclerosis. Lancet, 1984, ii: 304-307. Dubner, R. and Sessle, B.J. Presynaptic excitability changes of primary afferent and corticofugal fibers projecting to trigeminal brainstem nuclei. Exp. Neurol., 1971, 30: 223-238. Hassan, N.F., Rossini, P.M., Cracco, R.Q. and Cracco, J.B. Unexposed motor cortex activation by low voltage stimuli. In: C. Morocutti and P.A. Rizzo (Eds.), Evoked Potentials. Elsevier Science Publ., Amsterdam, 1985: 107-113. Hess, C.W., Mills, K.R. and Murray, N.M.F. Measurement of central motor conduction in multiple sclerosis by magnetic brain stimulation. Lancet, 1986, i.i.: 355-358. Hugon, J., Lubeau, M., Tabaraud, F., Chazot, F., Vallat, J.M.
87 et Dumas, M. Potentiels 6voqu6s moteurs; technique, r6sultats chez le sujet normal. Rev. Neurol., 1988, 144: 91-95. Maccabee, P.J., Amassian, V.E., Craeco, R.Q., Cracco, J.B. and Anziska, B.J. Intracranial stimulation of facial nerve in humans with the magnetic coil. Electroenceph. clin. Neurophysiol., 1988, 70: 350-354. Merton, P.A., Morton, H.B., Hill, D.K. and Marsden, C.D. Scope of a technique for electrical stimulation of human brain, spinal cord, and muscle. Lancet, 1982, ii: 597-600. Murray, N.M.F., Hess, C.W., Mills, R.R., Schriefer, T. and Smith, S.J.M. Proximal facial nerve conduction using magnetic stimulation. Electroenceph. clin. Neurophysiol., 1987, 66: $71. Nandedkar, S.D., Sanders, D.B., StMberg, E.V. and Andreassen, S. Simulation of concentric needle EMG motor unit action potentials. Muscle Nerve, 1988, 11: 151-159. Redding, R.W. Anatomy and physiology. In: B.F. Hoerlein (Ed.), Canine Neurology. Saunders, Philadelphia, PA, 1978: 7-52. Robinson, L.R., Jantra, P. and Maclean, I.C. Central motor conduction times using transcranial stimulation and F wave latencies. Muscle Nerve, 1988, 11: 174-180. 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. Sirisko, M.A. and Scssle, B.J. Corticobulbar projections and orofacial and muscle afferent inputs of neurons in primate sensorimotor cerebral cortex. Exp. Neurol., 1983, 82: 716-720. Snooks, S.S. and Swash, M. Motor conduction velocity in the human spinal cord: slowed conduction in multiple sclerosis and radiation myelopathy. J. Neurol. Neurosurg. Psychiat., 1985, 48: 1135-1139. Stoelting, R.K. and Miller, R.D. Intravenous anesthetics. In: R.K. Stoelting and R.D. Miller (Eds.), Basics of Anaesthesia. Churchill Livingstone, Edinburgh, 1984: 67-72.
Electroencephalograpt~' and clmtcal Neuropt[;siology, 1990, 75:82 87
Elsevier Scientific Publishers Ireland. Ltd. EEG 89017
Estimation of facial central motor delay by electrical stimulation of the motor cortex of the dog Siavash S. Haghighi and Scott A. Estrcm
*
Divisions of Neurological Surge 0, and * Otolaryngologo;, University of Missouri-Columbia. Columbia. MO 65202 ( U. S.A,)
(Accepted for publication: 25 June 1989)
Summa 0' Central delay time (CD) has been estimated for activation of limb muscles by electrical or transcranial magnetic coil t.TMC) stimulation of motor cortex and ventral root outflow. In the present study, we used surface electrical stimulation of the motor cortex of the right hemisphere to produce evoked compound muscle action potentials (CMAP) from the contralateral orbicularis oris (o.r.), and orbicularis ~xzuli(o.c.), in dogs. Monopolar electrical stimulation of the facial nerve at the cerebel!o-pontine (CP) angle yielded CMAP activation of ipsilateral facial muscles. These latencies when subtracted from those obtained by direct cortical stimulation established CD for activation of the seventh cranial nerve. Preliminary data with single pulse magnetic stimulation at high outputs ~ > 80%) revealed CMAP with onset latencies similar to the direct facial nerve stimulation at the CP angle by electrical means. Key words: Facial nerve; Central delay time; Cortical stimulation: Compound muscle action potential: Transcranial magnetic
stimulation
The technique of p e r c u t a n e o u s electrical or magnetic stimulation of the motor cortex has provided clinicians with an o p p o r t u n i t y to objectively study the descending m o t o r tracts in awake hum a n subjects ( H a s s a n et al. 1985; Barker et al. 1986; R o b i n s o n et al. 1988). M e r t o n et al. (1982) described transcranial s t i m u l a t i o n of the motor cortex utilizing a high voltage single pulse electrical stimulus. This technique was later used in patients with clinically diagnosed multiple sclerosis ( C o w a n et al. 1984; Berardelli et al. 1988). They estimated the central delay time (CD) by s u b t r a c t i n g the peripheral c o n d u c t i o n time, estimated by s t i m u l a t i o n of the ventral roots of the cervical spine, and recording peripherally from the same muscle group. The clinical utility of the
Correspondence to: Siavash S. Haghighi, D.V.M., Ph.D., Division of Neurological Surgery, N 522-Surgery, University of Missouri-Columbia,One Hospital Drive, Columbia, MO 65202 (U.S.A.).
transcranial magnetic coil ( T M C ) s t i m u l a t i o n has been recently d e m o n s t r a t e d (Barker et al. 1986). Benecke et al. (1988) a n d Maccabee et al. (1988) reported i n t r a c r a n i a l s t i m u l a t i o n of the facial nerve in h u m a n s with the T M C stimulation. They postulated that the location of the n e u r o n a l activation was at the facial nerve outflow from the b r a i n stem. Other authors also evaluated facial nerve activation in m a n by the T M C stimulation. They presented evidence that the l a b y r i n t h i n e segment of the facial canal was the p r o b a b l e site of the nerve stimulation ( M u r r a y et al. 1987; Schriefer et al. 1988). The objectives of the present study were twofold. First, electrical s t i m u l a t i o n was p e r f o r m e d in order to m a p the facial representation of the motor cortex a n d to record the evoked c o m p o u n d muscle action potentials ( C M A P s ) from the facial musculature in dogs. The second goal was to determine the C D for the facial nerve p a t h w a y by electrical stimulation. A c o m p a r i s o n with magnetic stimulation will briefly be discussed.
0013-4649/90/$03.50 ~'~,1990 Elsevier Scientific Publishers Ireland, Ltd.
FACIAL CENTRAL MOTOR CONDUCTION TIME Materials and methods Six mongrel dogs, weighing from 21.5 to 24.5 kg and selected randomly for sex, were used for this study. Each dog was premedicated with atropine sulfate (0.02 m g / k g ) and Innovar Vet (0.09 ml/kg). Halothane and oxygen mask induction was used which allowed intubation and replacement by methoxyflurane, oxygen anesthesia. An intravenous catheter was inserted for infusion of fluids. For continuous blood pressure measurements and blood gas sampling, a catheter was placed in a femoral artery. Arterial blood gases were taken frequently and were maintained within the physiological range. Electrocardiogram and rectal temperature were monitored continuously. For the electrical stimulation, a midline fronto-occipital incision was made. A large portion of the right frontal and parietal areas was exposed with incision of the dura. The dural flap was reflected medially and sutured over the midline sagittal sinus in order to have ample access to the medial surface of the motor cortex. W a r m mineral oil was applied to keep the brain moist and to reduce electrical current spread during the motor cortex stimulation. A silver ball electrode (0.5 m m in diameter) was positioned directly on the motor areas of the brain overlying the facial representation. The cathodal disk electrode was placed subcutaneously on the midline plane, 4 - 5 cm anterior to the silver ball anodal lead. To stimulate electrically the motor cortex, a constant voltage stimulator was used in conjunction with a stimulus isolation unit (Models $88 and SIU 8T, Grass Instruments, Quincy, MA). Repetitive electrical pulses (20-30 Hz at 0.2 msec duration) of amplitude 10-20 V or single pulses (0.2 msec duration) of high voltage (30-50 V) were used on the cortical surface. The left facial nerve was exposed in the CP angle through a suboccipital craniotomy under microscopic observation. To stimulate the facial nerve at the CP angle, single 0.1-0.2 msec rectangular pulses at 2 - 5 V intensities were used. Graded electrical stimulation, from threshold to supramaximal levels, was performed for the facial nerve. Concentric bipolar electrodes (Teca Corporation, Pleasantville, NY) were inserted in the con-
83 tralateral left orbicularis oculi (o.c.), and orbicularis oris (o.r.) muscles. Insertional muscle activity insured proper placement of the recording needles. An evoked potential averager (Cadwell Instruments, Kennewick, WA) was used for recording purposes. The high and low cut-off filters were set at 10 kHz and 300 Hz, respectively. The far-field myogenic or neurogenic sources were minimized by using concentric bipolar electrodes which are reported to record signals generated predominantly by the closest muscle fibers (Nandedkar et al. 1988). The latencies of the muscle responses were calculated from the start of the electrical shock artifact to the onset of the evoked compound action potential. For measurement of the E M G latencies, several consecutive responses were recorded to insure the reproducibility of the responses. A representative trace was accepted for latency measurements and stored for further analysis. The T M C stimulation was performed using a neuromagnetic stimulator (Cadwell Instruments, Kennewick, WA). The coil had an outside diameter of 9.5 cm and 2.2 (max) Tesla output. The C M A P to magnetic pulses were recorded both before and after craniotomy. The T M C stimulation was performed using variable orientations of the stimulating coil to the underlying skull and different output intensities. Euthanasia was carried out with an overdose of pentobarbital sodium (i.v.) under deep anesthesia after termination of the experiments.
Results Threshold stimulation with repetitive pulsing allowed us to map the facial area of the motor cortex. This area appeared more medial (Fig. 1) than what has been depicted in canine textbooks (Redding 1978). The facial movements were restricted to anodal stimulation of the anterior and posterior sigmoid gyri. The threshold repetitive stimulation allowed discrete contralateral facial muscle movement related closely to the d e p t h of anesthesia. Movement of the ipsilateral facial musculature also occurred, being predominant at the deeper level of anesthesia. Comparison of
S.S. HAGHIGHI, S.A. ESTREM
84
I
=I
,ooo.vl
,
I L
500 IJV l _ _ 1
L 0
I 1
I 2
11 3
t 4
I 5
I 6
1 7
msec
I 8
I 9
I 10
Fig. 2. The evoked compound muscle action potential (CMAP) of the orbicularis oculi in response to the electrical stimulation of the facial motor cortex (upper trace) is compared with the CMAP elicited by the cerebello-pontine angle stimulation of the facial nerve (lower trace).
Fig. 1. Location of area (cross-hatched) in the cerebral cortex of the dog that produces facial movements when stimulated electrically. The facial representation in our study is located more medially (A) compared with previous reports (B). (Modified from Hoerlein, B.F., Canine Neurology. Saunders, Philadelphia, PA, 1978.)
500 pv l__
C M A P of the facial m u s c u l a t u r e to the electrical s t i m u l a t i o n of the facial m o t o r cortex a n d the single pulse s t i m u l a t i o n of the nerve at the C P angle depicted the delay for the facial nerve (Figs. 2 a n d 3). T h e CP angle electrical s t i m u l a t i o n of the facial nerve yielded C M A P s with latency a n d a m p l i t u d e similar to those o b t a i n e d by the single electrical shocks to the facial cortex at high intensities. This seemed to i m p l y that current spread activated the i n t r a c r a n i a l segment of the facial nerve at its exit from the b r a i n - s t e m preferentially over true cortical activation. Sectioning of the facial nerve at the C P angle or facial nerve block at the stylomastoid (SM) f o r a m e n abolished the evoked electromyographic responses following electrical stimulation
t
0
I 2
I 4
I 6
I
tl
8
10
I
I
12
14
I 16
I 18
I 20
Upper: direct cortical stimulation Lower: facial nerve stimulation Fig. 3. Comparison of the evoked CMAP of the orbicularis oris to the electrical stimulation of the facial motor area (upper trace) and the single pulse electrical stimulation of the facial nerve at the cerebello-pontine angle (lower trace).
FACIAL CENTRAL MOTOR CONDUCTION TIME
LEFT
L (C-P Angle)
sopv~ _ a ms~
orblcullrls ocull
L~v.~ f ~ / ~
A/'~,_."
TABLE I Electrical stimulation ......
Magnetic stimulation (100%)
orblculerls orls
i
~-
85
vll[jl/~vrll-,V~f~rvv-~.
Comparison of the evoked compound muscle action potential lateneies of orbicularis oculi (o.c.), and orbicularis ores (o.r.) to facial nerve stimulation at the cerebello-pontine angle and motor cortex electrical stimulation.
Electrical stimulation
Motor cortex
Magnetic stimulation
o.
(too~)
Fig. 4. Comparison of the evoked compound muscle action potential of the orbicularis oeuli, and orbicularis otis to high intensity transcranial magnetic stimulation and the single-pulse electrical stimulation of the facial nerve at the cerebello-pontine angle.
oculi 5 4 5.08 3.58 3.5 4
o.
of the motor cortex. However, after the complete facial nerve transection at the CP angle in one dog, facial CMAP could be elicited with the high intensity magnetic stimulation with the coil positioned over the occipito-temporal region. The TMC stimulation at high outputs ( > 80%) elicited CMAP from facial musculature which was similar in onset latency to that obtained by facial nerve stimulation at the CP angle, again suggesting facial nerve activation rather than facial cortical activation (Fig. 4). Interestingly, the TMC stimulation at the retromandibular region (that is, near the SM foramen), at high outputs ( > 80%), could evoke shorter latency muscle response compared with those evoked at the lower magnetic intensities. This presumably implied that the magnetic stimulation at high intensities activated more distal segments of the nerve by the stimulus current spread (Fig. 5).
LEFT LEFT Levator nasolabialis
CP angle
CD
3.41 3.5 4 3.08 2.8 3.5
1.59 0.5 1.08 0.5 0.7 0.5
6.3 5.16 5.4 6.4 2.9 9.66
0.91 1.16 1.4 1.3 1.7 1.84
ores
7.21 6.33 6.8 7.7 4.6 11.5
C D ~ central delay. Values axe in milliseconds.
Table I summarizes the onset CMAP latencies of the o.c. and o.r. to the intracranial stimulation of the facial nerve at the CP angle and the cortical facial motor latencies obtained by electrical stimulation. The CD, determined with electrical stimulation, ranged from 0.5 to 1.59 msec for o.c., and from' 0.91 to 1.84 msec for o.r. muscles. The magnetic stimulation revealed similar latencies of the facial musculature. Single-shock TMC stimulation produced consistent facial muscle activation with the onset latencies dependent upon the position of the magnetic coil with respect to the underlying skull and
St ylomalltoid foramen 50%
LEFT
~ J ,
I~ / V W ~ , ~ . - - . . , ~ . _
Levator naaolablalls
Midltne frontal Midllne OCCipital
40%
3O% Fig. 5. Evoked C M A P of the left levator n~selabialis muscle to the transcr~dal magnetic stimulation at different intensities. Magnetic coil is placed at the left retromandibular region. Higher magnetic intensity activa~s the distal segments of the facial nerve through stimulus spread.
~ ~ ~
Left styl . . . . told
Fig. 6. Evoked C M A P of the levator nasolabialis muscle to the transcranial magnetic stimulation. Onset latency and general configuration of the evoked response are dependent upon the position of the magnetic coil on the skull.
86
the intensity of the T M C stimulation (Fig. 6). The CMAPs recorded before and after craniotomy did not change with the magnetic stimulation. Tangential (flat) positioning of the magnetic coil over the occipital midline parallel to the atlanto-occipital (AO) axis, revealed higher amplitude CMAP. Orthogonal positioning of the coil at a 45 ° angle to the axis produced lower amplitude muscle response. Perpendicular positioning of the coil to the AO axis did not elicit any E M G response.
Discussion Using repetitive electrical stimulation of the facial motor cortex, we mapped out the facial representation within the motor cortex of the dog. Previous work on the motor cortex representation in dogs depicts the facial area on the precruciate sulcus (Redding 1978). The facial motor area appeared to be more medially located, toward the interhemispheric fissure, in our investigation (Fig. 1). This discrepancy may be due to the stimulation methodology. The anesthetic agent and depth of anesthesia also play important roles for motor mapping. It is widely believed that intravenous anesthetics such as barbiturates suppress neuronal activities at the synaptic level within the central nervous system (Stoelting and Miller 1984). We observed the same phenomenon with the methoxyflurane anesthesia. The contralateral CMAPs were more dominant at the lighter stage of anesthesia. The evoked facial E M G to electrical stimulation at the CP angle was similar to that obtained by high intensity single cortical stimulations. We postulate that the latter is the result of electrical current spread to the facial nerve proper without being conveyed through the central facial pathways. The CD for the descending pathways and its clinical significance for determining certain central nervous system disease have been described previously for the spinal cord (Cowan et al. 1984; Snooks and Swash 1985). The normative range for the C D of the long descending tracts has been
S.S. H A G H I G H I , S.A. ESTREM
reported (Cowan e t a [ . 1984; Hess et al. 1986: Berardelli et al. 1988). This central delay has been reported to be 4.3 msec for the upper limbs and 9.3 for the lower limbs (Hugon et al. 1988). The only study on the transcranial activation of the corticobulbar fibers by magnetic stimulation is given by Benecke et al. (1988). They reported 6 msec C D for the corticobulbar segment of the facial nerve in man using magnetic stimulation. Several experimental studies have also been attempted utilizing the retrograde activation of the corticobulbar fibers by intracortical microstimulation methods (Dubner and Sessle 1971: Sirisko and Sessle 1983). Our investigation revealed a wide range of conduction delay for the facial musculature. This range varied from 0.5 to 1.59 msec for o.c., and from 0.91 to 1.84 msec for o.r. muscles. Based on the retrograde activation of corticobulbar fibers in monkeys, Sirisko and Sessle (1983) described a similar wide range of the central delay for the facial nerve. The difference in the central delay of the o.c. and the o.r. muscles in our study is remarkable. We postulate that this is presumably due to the difference in the intracranial length of the corticobulbar fibers for the o.c. and o.r. muscles. In this investigation, we have had the advantage of direct access to the CP angle for electrical stimulation of the facial nerve. We have demonstrated that the C M A P recorded with the magnetic stimulation at high intensities is similar to that of the CP angle electrical stimulation in our experimental model. This implies that T M C stimulation activates the intracranial segment of the nerve similar to the single-shock electrical stimulation of the nerve at brain-stem. Using magnetic stimulation in humans, Maccabee et al. (1988) and Schriefer et al. (1988) have reached a similar conclusion. We have also shown that the high electrical intensities applied to the motor cortex can directly activate the peripheral component of the facial nerve as the result of electrical current spread to the brain-stem region. Magnetic stimulation seems to have advantages over the conventional electrical stimulation of the facial nerve since it evaluates the more proximal segments of the nerve. The T M C stimulation may also be helpful in localizing facial nerve injuries
FACIAL CENTRAL MOTOR CONDUCTION TIME
along its neural pathway based on latency differences. We would like to thank Prof. V.E. Amassian for his helpful comments. We also thank Bridget Crabtree, Janet Sapp, and Becky Roberts for preparation of the manuscript and Charlene Saunders for the illustrations.
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