Motor evoked potentials: a new method of controlled facilitation using quantitative surface EMG

Electroencephalography and clinical Neurophysiology, 85 (1992) 38-41 © 1992 Elsevier Scientific Publishers Ireland, Ltd. 0924-980X/92/$05.00

38

ELMOCO 90210

Motor evoked potentials: a new method of controlled facilitation u s i n g quantitative surface E M G C.L. Lim and C. Yiannikas Department of Neurophysiology, Westmead Hospital, Sydney, NSW (Australia) (Accepted for publication: 12 June 1991)

Summary A new method of assessing MEP facilitation using surface EMG under computer control is described. Transcranial magnetic stimulation with voluntary contraction at a value between 2 and 6% of maximal surface EMG activity produced responses with shortest latencies and largest amplitudes and power. No significant changes occurred when facilitation increased beyond this level. These results are similar to previously published studies using a force transducer, confirming the reliability of the system as an alternative method of monitoring voluntary contraction. The controlling system may potentially provide an easy, flexible, quantitative method of ensuring adequate, reproducible facilitation with minimum EMG interference for testing in a clinical setting.

Key words: Motor evoked potentials; Controlled facilitation; Voluntary contraction

Voluntary contraction (VC) of a muscle prior to transcranial stimulation (TCS) results in shortening of latency and an increase of amplitude of the motor evoked potential (MEP) (Rothwell et al. 1987a,b). It has been suggested that only small amounts of VC are required to produce maximal facilitation (Hess et al. 1986a,b), however, voluntary control of this is difficult. Inadequate VC may produce spuriously long latencies and excess VC may lead to distortion of the baseline causing uncertainty in onset measurements. Quantification of the amount of VC may therefore be useful and has been achieved by use of a force transducer, Inherently force transducers have a number of problems including requirement of an elaborate mechanical lever system for each muscle group which limits its use to certain accessible muscles. As muscle force and EMG are both related to muscle contraction, surface EMG may serve as an alternative of quantifying the amount of voluntary contraction. We hereby describe a new method of assessing MEP facilitation using surface EMG under computer control and report our preliminary clinical results obtained by the use of our hardware and software prototype interfaced to a magnetic stimulator and a conventional recording system,

Correspondence to: C.L. Lira, Department of Neurophysiology,

Westmead Hospital, Cnr Hawkesbury and D'Arcy Roads, Westmead, NSW 2145 (Australia).

Methods

A high gain, low noise, bandwidth limited, isolation differential amplifier was designed and built to the established standards (Guld et al. 1983; Standards Association of Australia 1986). The surface EMG signal was amplified and digitised by a 12-bit analog-digital converter sampling at 1100 Hz under an IBM AT computer control. Twenty-four sets of EMG during maximum voluntary effort were collected, squared, summed over 300 msec periods and displayed graphically. From these the averaged maximum muscle power (AMMP) was calculated. EMG following voluntary contraction of target muscle was continuously monitored and expressed as a percentage of AMMP and displayed on the monitor screen. When the level fell within the preset limits a trigger pulse was sent to synchronise a magnetic stimulator and an EMG recording system. Magnetic stimulation was achieved using a Cadwell MES-10 stimulator with the coil positioned over the vertex and orientated to reach resting threshold with the minimum intensity. CMAPs were recorded from surface disc electrodes placed over the belly of the abductor digiti minimi (ADM) muscle with reference to the base of the digit 5 and connected to a Medelec Mystro EMG system. MEPs were obtained from the ADM of 5 normal subjects at rest and with facilitation at > 0-2%, 2-4,

MEP FACILITATION USING QUANTITATIVE SURFACE EMG

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The MEPs showed a decrease in latency and an increase in amplitude with increasing levels of facilitation between 2 and 4% (Fig. 1). The response latencies, amplitudes and areas under curves of all the subjects are listed in Table I and shown graphically in Fig. 2A, B and C respectively. There was a m e a n reduction in latency of 3.3 msec and an 8-fold increase in amplitude between 4 and 6% facilitation and rest. Similar changes were seen in the area under the curve. All p a r a m e t e r s plateaued after 4 - 6 % .

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4-6, 8-10, 10-14, 18-22, 2 6 - 3 0 % of A M M P . At rest responses were recorded with a higher gain than those of facilitated tests. At each facilitation level, measurements w e r e m a d e on the average of at least 3 responses, displayed at higher sensitivities.

TABLE I Responses at various background EMG levels. Mean and standard deviation of latencies, amplitudes and areas under curve of motor evoked potentials to transcranial magnetic stimulations triggered by 8 levels of relative surface EMG power in 5 normal subjects, EMG power (%) 0 >0- 2 2- 4 4-6 6- 8 8-10 18-22 24-30

Latency Mean + S.D. (msec) 24.7 + 0 . 5 8 23.1+1.05 21.3±1.89 21.4±2.01 21.1 ± 1.92 21.0±2.00 20.6 5:1.69 20.8 + 1.61

Amplitude Mean + S.D. (mV) 0.55:0.20 1.6:t:1.97 3.45-1.32 4.25-0.57 4.3 5:1.65 4.3±1.34 4.3 ± 2.06 4.4 5:1.19

Area Mean ± S.D. (/zV) 1.2 5:0.86 1.6+ 1.27 15.15:13.60 14.35:11.58 15.5 ± 1 1 . 1 4 14.95:11.08 15.9 + 11.96 16.8 5:13.21

The observation that M E P latency decreased and amplitude increased when the target muscle was in slight contraction was first m a d e by Merton et al. (1982) and Marsden et al. (1983). This facilitation p h e n o m e n o n has been subsequently studied by o t h e r s (Cowan et al. 1984, 1986; Rossini et al. 1985, 1987; Hess et al. 1986a,b, 1987; Cracco 1987; Rothwell et al. 1987b; Chiappa et al. 1988; Starr et al. 1988; Amassian et al. 1989; Caramia et al. 1989; Day et al. 1989). The exact mechanism is still not clear although both spinal and cortical mechanisms have been implicated (Day et al. 1987; Hess et al. 1987; Cros et al. 1990). In view of the variation in amplitude and latency of M E P with facilitation there is a need to quantify the level of voluntary muscle activation to enhance the reproducibility of these studies. This has been done by means of force transducers (Hess et al. 1986a,b, 1987; Rossini et al. 1987) where a subject produces a contraction force against a transducer to match a preset level on a C R T display. Unfortunately, t h i s technique requires joint immobilisation, a lever system and force transducers which a r e cumbersome and limit the number of muscles that may be studied. As such it is difficult to use in the routine clinical setting. Another serious disadvantage is that the force transducer cannot distinguish isometric contraction from absence of contraction and may underestimate facilitation levels. Indeed, Rothwell et al. (1987b) c o m m e n t e d that in about 3% of their trials using force method the response latency in relaxed muscles was similar to that of active muscles, and they attributed this to failure of relaxation. For clinical use a simpler and easier control system would be more useful. A direct measure of voluntary muscle activation may be achieved more simply using surface E M G , since there is a high correlation between this and force m e a s u r e m e n t s (Philipson and Larsson 1988), This technique has been applied successfully by Chiappa et al. (1988), however, the assessment of the level of facilitation with E M G was retrospective and was not automat-

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which is a measure of power of muscle output, reflected similar facilitated effects. The latency results are similar to published data of facilitated responses determined with the aid of force measurements. Hess et al. (1987) reported in 10 subjects A D M onset latency of 20.9 ___1.12 msec at facilitation level of 5 - 1 0 % of maximum force, compared to our finding of 21.1 + 1.92 msec at a facilitation level of 6 - 8 % of AMMP. Comparable results were also seen at rest (24.1 ± 1.6 msec vs. 24.7 + 0.58 msec). The smaller standard deviation of latencies for relaxed muscles in this study may be due to the ability to detect even small amount of muscle contraction using this technique. The force method may have experienced some difficulties in differentiating isometric contraction from absence of muscular activity thereby increasing the variability in their resting results. This problem has been alluded to by others (Rothwell et al. 1987b). The amplitude variation seen beyond 4 - 6 % level in .2 subjects (Fig. 2B) may reflect variations in the excitability of the motor-neuronal pool. It is unlikely to be due to technical problems as the stimulus wand position was not significantly different at each facilition level. This system may potentially provide an easy, flexible, quantitative method of ensuring adequate, reproducible facilitation with minimum E M G interference for testing in a clinical setting.

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[2-41 [6-81 [18-22] BACKGROUND EMG % Fig. 2. Variation in latency (A), amplitude (B) and area under curve (C) with various trigger threshold levels. The data from each individual subject are shown in various shades of grey and their means, marked as "AVE," in black. The mean changes reach plateaued at 4-6% of AMMP.

ically time .locked to the stimulus. The system reported here incorporates the advantages of quantitative s u r face E M G with an integrated, software controlled automatic triggering mechanism. This allows the E M G threshold level for stimulation to be varied by a user to any level up to 1% accuracy. In addition, the prestimulation window may also be varied, allowing assessment of the optimal pre-stimulus epoch, It has been suggested that 5 - 1 0 % facilitation would give saturated responses for both MEP latency and amplitude (Rothwell et al. 1987b). In this study MEP latencies and amplitudes reached plateau with surface E M G levels at 4 - 6 % of maximal effort (Fig. 2 and Table I). Changes in area under the curve (Fig. 2C),

References

Amassian, V.E., Cracco, R.Q., Maccabee, P.J., Cracco, J.B., Rudell, A. and Eberle, L. Suppression of visual perception by magnetic coil stimulation of human occipital cortex. Electroenceph. clin. Neurophysioi., 1989, 74: 458-462. Caramia, M.D., Pardal, A.M., Zarola, F. and Rossini, P.M. Electric vs magnetic trans-craniai stimulation of the brain in healthy humans: a comparative study of central motor tracts "conductivity" and "excitability." Brain Res., 1989, 479: 98-104. Chiappa, K.H., Cros, D. and Santamaria, J. Magnetic stimulation of the human motor cortex: facilitation is not related to concentration on a visual motor task. J. Clin. Neurophysiol., 1988, 5:

370-371.

Cowan, J.M.A., Dick, J.P.R., Day, B.L., RothweU, J.C., Thompson, P.D. and Marsden, C.D. Abnormalities in central motor pathway

conduction in multiple sclerosis. Lancet, 1984, ii: 304-307. Cowan, J.M.A., Day, B.L., Marsden, C. and Rothwell, J.C. The

effect of percutaneous motor cortex stimulation on H reflexes in muscles of the arm and leg in intact man. J. Physiol. (Lond.), 1986, 377: 333-347.

Cracco,R.Q. Evaluation of conduction in central motor pathways: techniques, pathophysiology,and clinical interpretation. Neurosurgery, 1987, 20: 199-203. Eros, D., Fang, J., Shahani, B., Chiappa, K. and Day, B. Stimulation

of descending motor pathways in the spinal cord in humans: facilitation of motor responses by voluntary contraction. Neurology, 1990, 40 (Suppl. 1): 216.

Day, B.L., Maertens, A., Marsden, C.D., Nakashima, IC, Rothwell, J.C. and Thompson, P.D. Temporary interruption of brain pro-

MEP FACILITATION USING QUANTITATIVE SURFACE EMG

41

cessing by an electrical or magnetic cortical shock in man. J. Physiol. (Lond.), 1987, 390: 197P. Day, B.L., Rothwell, J.C. and Thompson, P.D. Delay in the execution of voluntary movement by electrical or magnetic brain stimulation in intact man. Brain, 1989, 112: 649-663. Guld, C., Rosenfalk, A. and Willison, R.G. Report of the Committee on EMG instrumentation. Technical factors in recording electrical activity of muscle and nerve in man. In: Recommendations for the Practice of Clinical Neurophysiology - International Federation of Societies for Electroencephalography and Clinical Neurophysiology (IFSECN). Elsevier, Amsterdam, 1983: 83-116. Hess, C.W., Mills, K.R. and Murray, N.M.F. Percutaneous stimulation of the human brain: a comparison of electrical and magnetic stimuli. J. Physiol. (Lond.), 1986a, 378: 35P. Hess, C.W., Mills, K.R. and Murray, N.M.F. Magnetic stimulation of the human brain: facilitation of motor responses by voluntary contraction of ipsilateral and contralateral muscles with additional observations on an amputee. Neurosci. Lett., 1986b, 71: 235-240. Hess, C.W., Mills, K.R. and Murray, N.M.F. Responses in small hand muscles from magnetic stimulator of the human brain. J. Physiol. (Lond.), 1987, 388: 397-419. Marsden, C.D., Merton, P.A. and Morton, H.B. Direct electrical stimulation of corticospinal pathways through the intact scalp in human subjects. In: J.E. Desmedt (Ed.), Motor Control Mechanisms in Health and Disease. Raven Press, New York, 1983: 387-391. "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. Philipson, L. and Larsson, P.G. The electromyographic signal as a measure of muscular force: a comparison of detection and quantification techniques. Electromyogr. Clin. Neurophysiol., 1988, 28: 141-150. Rossini, P.M., Di Stefano, E. and Stanzione, P. Nerve impulse propagation along central and peripheral fast conducting motor and sensory pathways in man. Electroenceph. clin. Neurophysiol., 1985, 60: 320-334. Rossini, P.M., Caramia, M.D. and Zarola, F. Mechanisms of nerve propagation along central motor pathways: noninvasive evaluation in health subjects and in patients with neurological disease. Neurosurgery, 1987, 20: 183-191. Rothwell, J.C., Thompson, P.D., Day, B.L., Dick, J.P.R., Kachi, T., Cowan, J.M.A. and Marsden, C.D. Motor cortex stimulation in intact man. Brain, 1987, 110: 1173-1190. Rothwell, J.C., Day, B.L., Thompson, P.D., Dick, J.P.R. and Marsden, C.D. Some experiences of techniques for stimulation of the human cecebral motor cortex through the scalp. Neurosurgery, 1987, 20: 156-163. Standards Association of Australia. Approval and Test Specifications of Electromedical Equipment: General Requirements, 3rd Edn. SAA, Sydney, 1986. Start, A., Caramia, M.D., Zarola, F. and Rossini, P.M. Enhancement of motor cortical excitability in human by non-invasive electrical stimulation appears prior to voluntary movement. Electroenceph. clin. Neurophysiol., 1988, 70: 26-32.