Electroencephalography and clinical Neui'ophysiology , 85 (1992) 158-160 © 1992 Elsevier Scientific Publishers Ireland, Ltd. 0924-980X/92/$05.00
158
ELMOCO 90689 Short communication
Silent period measurement revives as a valuable diagnostic tool with transcranial magnetic stimulation Bernhard A. Haug, Paul W. Sch6nle, Christian Knobloch and Martin K6hne Department of Clinical Neurophysiology, Georg August University, D-W-3400 G6ttingen (F.R.G.) (Accepted for publication: 12 November 1991)
Summary
Following magnetic transcranial stimulation (TCS) a post-excitatory pause can be observed in surface electromyographic (EMG) recordings from pre-innervated muscles. We studied the duration of this silent period (SP) in the abductor pollicis brevis muscle while varying the stimulus intensity (SI) and the amount of the voluntary tonic contraction in 23 normal adults aged 20-78 years. A multivariate linear regression analysis revealed a positive correlation of SP with SI and a slight negative correlation with age. In 11 hemiparetic patients a relative increase of the SP was found on the affected side despite normal central motor conduction time. A marked shortening of the SP in relation to controls was observed in 6 parkinsonian patients.
Key words: Electromyographic silent period; Post-excitatory inhibition; Magnetic transcranial stimulation; Pyramidal and extrapyramidal tract
Post-excitatory electromyographic (EMG) silence in muscles during voluntary contraction can be elicited in many ways. The phenomenon has first been observed with electric stimulation of peripheral nerves (Hoffmann 1920), where multiple factors may contribute to form the silent period (SP) (Merton 1951; Burg et al. 1973; Shahani and Young 1973), such as collision of the antidromic volley with descending motor nerve action potentials and a variety of reflex activities. Moreover, the SP is often partially interrupted by the F response. Many of these difficulties can be avoided by mechanical elicitation of the SP (Angel et al. 1965), but elaborate techniques (Higgins and Lieberman 1968) have hampered their introduction to clinical routine. With magnetic transcranial stimulation (TCS) a new method has been introduced that allows precise measurement of the EMG pause without ambiguity from peripheral stimulus artefacts. Using magnetic TCS we tried to re-evaluate SP measurement in normals and in hemiparetic or parkinsonian patients.
Methods The conventional Novametrix Magstim 200 was fitted with the flat concentric coil of 8.5 cm mean diameter and 20 loops, which was centered to the vertex. Either one or the other side of the coil was applied to induce maximum response of the left or right precentral hand area as in muscle evoked potential (MEP) elicitation (Hess et al. 1987). EMG activity was recorded from the respective abductor pollicis brevis (APB) muscle via surface electrodes placed on the belly and tendon. A T6nnies Myograph DA II served as a recording unit, using 0.5 mV/division for the sensitivity and 2 Hz respectively 10 kHz for the cut-off frequency filters. The patient or subject was seated comfortably on an armchair and was asked to maintain a
Correspondence to: Dr. Med. Bernhard Haug, Neurologische Universit~itsklinik, Robert-Koch-Strasse 40, D-W-3400 G6ttingen (F.R.G.), Tel.: (551) 39-8484 or 39-6691.
constant isometric contraction of the ipsilateral muscle. The magnetic impulse to the cortex was triggered 100 msec after starting a 500 msec storage sweep on the oscilloscope, so that pre- and poststimulus activity could be recorded satisfactorily from the screen storage. The direct muscle response was superimposed on the background myographic activity. With some delay (42-50 msec, mean 46 msec) and above a certain stimulus threshold an interval of complete absence of EMG activity followed, referred to as SP. The threshold of SP elicitation (ThrSP) was 25-45% of the maximum output (% MO) of the used stimulator and usually lower than the threshold of MEP elicitation in relaxed muscles. After having determined the individual ThrSP a stimulus intensity (SI) of + 10, + 20, + 30, + 40 and +50% MO above individual ThrSP has been applied. In the normal subjects at each SI the force of voluntary activity has also been varied to be 10, 25, 50, 75 and 100% of maximum force, the latter being defined as that which can be maintained for some 10 sec. To keep it at the desired level, it has been monitored under virtually isometric conditions by a vigorimeter and by visual judgment of the surface EMG interference pattern. In all patients we stuck to fixed values for pre-innervation (half maximum force) and SI ( + 30% MO above individual ThrSP), but measurements were reproduced 5 times on each side, and the arithmetic mean has been used for further calculations.
Results In 10 female and 13 male healthy adults aged 20-78 years we studied the influence of voluntary background activity, SI and age on the duration of the SP. Either of the first two parameters was varied independently in 5 steps as described above, so that 25 measurements have been acquired in each individual. ' Fig. 1 (top) illustrates the findings in a normal subject, when the SI is varied from + 10 to + 50% MO above the individual ThrSP. There is a near-linear increase of SP with SI, and a saturation cannot be achieved within the given limits. A set of 4 measurements at different voluntary activity levels but constant SI in the same subject is pictured in Fig. 1 (bottom). It demonstrates that the SP duration is
159
SILENT PERIOD WITH MAGNETIC STIMULATION Normal (constant
Subject
--
maximal
Stimulus force)
Stimulus Intensity ( + 3 0 * / . M O a b o v e Thr SP)
Normal S u b j e c t 50O/o m a x i m a l force)
Intensity
(~'IoMO a b o v e T h r SP)
s i l e n t period + 10°/. left APB +
20"/o
+ 40"/* right APB + 50 °/,
stimulus
at 1 0 0 m s
stimulus
1.0mV[
at lOOms
1.0
m[ V
i
50ms
i
50ms Normal S u b j e c t -Muscle A c t i v i t y (4-30 O/aM* a b o v e ThrSP) (*/. of m a x i m a l
Right Hemiparesis ( 5 0 " / o m a x i m a l force)
force)
--
Side C o m p a r i s o n ( + 3 0 * / . M O a b o v e Thr SP)
10 */* left APB
25°/.
50"/. right APB 100"/,
s t i m u l u s at 2 0 0 m s
1.0
V
0 * mss l s t i m atu l1 u
, 50ms
Fig. 1. Surface EMG recordings from APB muscle of an individual, who exerts maximal force while the SI is varied (top) and, vice versa, constant Sis are applied while he is varying the voluntary muscle activity (bottom). For the print-outs a Nihon-Kohden Neuropack 4 Mini was used with a sampling rate of 1024/sec, four 500 msec sweeps were recorded and displayed at a reduced sensitivity of 1.0 mV/division, cut-off frequencies 2 Hz and 10 kHz.
1.0 m V [
i
50ms
Fig. 2. Surface EMG recordings from left and right APB muscles of a normal subject (top) and of a patient with right hemiparesis (bottom), showing 2 consecutive peristimulus sweeps on either side. Note the reproducible SP duration and the marked prolongation on the affected side in the patient (bottom 2 tracings). silent period [ms]
200
150
not influenced as long as sufficient EMG activity allows to determine its exact beginning and end. All the measurements in normal subjects have been analyzed by backward stepwise multiple linear regression. It showed that the variable of pre-innervation could be removed without compromise. An approximation of the SP in the APB muscle of normal adults was calculated from 23 healthy individuals with independent values of SI and age. With age there is a slight decrease of SP, illustrated in Fig. 3. Throughout the clinical studies a voluntary muscle contraction of half maximal force and an SI of + 30% MO above individual ThrSP was used. The ThrSP has been found to be equal on both sides in each individual of this sample, so we could apply the same SI for both sides, thereby avoiding ambiguities when comparing side to side. We examined 11 patients aged 49-83 years just prior to dismissal, when they had nearly fully recovered from a small cortical or subcortical infarct. At this time there was hardly any weakness or
100
50
0
iil~ 40
,llll,,lll~ll,ll,Jll~Jl~,Jr, 50
J,,~,,~,lllll
60
70
80
age [ y r s ] potklnsonlsm [~
regression - 2 SD
m m
h e m l / n o , m a l side
[~
heml/po#h, side
regression normols
[~
regression +
2 SO
Fig. 3. Silent period from APB muscle following magnetic TCS. Age-dependent regression curve of 23 healthy controls for intensity +30% MO above individual ThrSP. Individual measurements of patients with hemiparesis (pathological versus normal side) and of parkinsonians (one side only).
B.A. HAUG ET AL.
160 reflex pathology on the affected side, and central motor conduction time CMCT = C M L -
to established neurophysiological methods, especially if they fail to clearly detect assumed pyramidal or extrapyramidal tract pathology.
(F+ D M L ) / 2 ,
calculated from central motor latency (CML), minimal F wave latency (F) and distal motor latency (DML) was normal and equal on both sides. However, the SP measurement often disclosed a prolongation on the affected side, which is more conspicuous with intraindividual side comparison. The findings of a normal individual (Fig. 2, top) and of a patient with slight hemiparesis on the right side (Fig. 2, bottom) clarify the high event-to-event stability in consecutive recordings. Similarly 6 parkinsonian patients aged 46-71 years were studied during adjustment of drug therapy, two of them with unilateral symptoms only. Here a marked shortening of the SP was revealed, in hemiparkinsonism restricted to the affected side. All findings of the clinical study are shown in a bar graph (Fig. 3), allowing comparison to the normal range.
Discussion
In agreement with former studies on the SP following electric peripheral nerve stimulation (Herman 1969; Dietrichson 1971) and TCS (Rossini 1990) we did not find a relationship between SP duration and amount of voluntary muscle activity or contraction force. The positive correlation between cortical SI and SP duration may be explained from different viewpoints. Mills (1988) and Brouwer et al. (1989) have shown that magnetic TCS elicits excitatory and inhibitory cortical inputs to spinal motoneurons. The latter outlast the former for as much as 80 msec and may contribute to the SP according to the SI. Another viewpoint takes proprioceptive reflexes into consideration, which may play a role for the generation of later parts of the SP. Being disinhibited on the affected side in patients with pyramidal tract injury (Burke 1988; Katz and Rymer 1989), they could explain the interside difference of the SP in cerebral infarcts. Side-to-side differences of SP may also reflect an interhemispheric asymmetry of cortical motor thresholds in spastic hemiparesis (Caramia et al. 1991), although in our cases such asymmetry was too small for detection. Thus, prolongation of the SP on the affected side seems to be a very sensitive indicator of ischemic central motor deficits, even if MEPs and CMCTs are normal. In parkinsonism a deficit of basal ganglia inhibition to long-latency responses accounts for a predominance of excitatory inputs to spinal motoneurons (Rothwell et al. 1983), resulting in the typical rigidity (Berardelli et al. 1983; Mortimer and Webster 1983). Rossini states a general lack of sensorimotor integration in a subgroup of parkinsonians, where conditioning stimulation of the median nerve fails to affect the excitability threshold in TCS (personal communication 1991). Recent work on magnetic TCS in parkinsonian patients has also shown that the amplitudes of their MEPs are larger compared to normals (Kandler et al. 1990). Inhibitory inputs following TCS may therefore be less effective and the SP may be shortened or even sometimes interrupted by bursts of activity. The negative correlation of SP duration with age may be seen as an expression of a natural process of aging leading to a physiological state of hypokinesia and relative rigidity, thus parallelling the changes in parkinsonism. Partly it can be explained by the tendency for a higher ThrSP in older people. Further studies may clarify the physiological aspects of the SP elicited by TCS, particularly in bow much it depends on excitatory and inhibitory cortical inputs to motoneurons. Diseases which impair the delicate balance of these pathways may hence be detected and quantified by SP examination. We propose the measurement of the SP elicited by magnetic TCS as a useful and easy-to-perform adjunct
References
Angel, R.W., Eppler, W. and Iannone, A. Silent period produced by unloading of muscle during voluntary contraction. J. Physiol. (Lond.), 1965, 180: 864-870. Berardelli, A., Sabra, A.F. and Hallett, M. Physiological mechanisms of rigidity in Parkinson's disease. J. Neurol. Neurosurg. Psychiat., 1983, 46: 45-53. Brouwer, B., Ashby, P. and Midroni, G. Excitability of corticospinal neurons during tonic muscle contraction in man. Exp. Brain Res., 1989, 74: 649-652. Burg, D., Szumski, A.T. and Struppler, A. Afferent and efferent activation of human muscle receptors involved in reflex and zcoluntary contraction. Exp. Neurol., 1973, 41: 754-768. Burke, D. Spasticity as an adaptation to pyramidal tract injury. Adv. Neurol., 1988, 47: 401-423. Caramia, M.D., Cicinelli, P,, Paradiso, C., Mariorenzi, R., Zarola, F., Bernardi, G. and Rossini, P.M. 'Excitability' changes of muscular responses to magnetic brain stimulation in patients with central motor disorders. Electroenceph. clin. Neurophysiol., 1991, 8l: 243-250. Dietrichson, P. The silent period in spastic, rigid, and normal subjects during isotonic and isometric muscle contractions. Acta Neurol. Scand., 1971, 47: 183-193. Herman, R. Silent period during isometric and isotonic contraction. Arch. Phys. Med. Rehab., 1969, 50: 642-646. 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. (Lond.), 1987, 388: 397-419. Higgins, D.C. and Lieberman, J.S. The muscle silent period: variability in normal man. Electroenceph. clin. Neurophysiol., 1968, 24: 176-182. Hoffmann, P. Demonstration eines Hemmungsreflexes im menschlichen RiJckenmark. Z. Biol., 1920, 70: 515-524. Kandler, R.H., Jarratt, J.A., Sagar, HJ., Gumpert, E.J.W., Venables, G.S., Davies-Jones, G.A.B. and Jordan, N. Abnormalities of central motor conduction in Parkinson's disease. J. Neurol. Sci., 1990, 100: 94-97. Katz, R.T. and Rymer, W.Z. Spastic hypertonia: mechanisms and measurement. Arch. Phys. Med. Rehab., 1989, 70: 144-155. Merton, P.A. The silent period in a muscle of the human hand. J. Physiol. (Lond.), 1951, 114: 183-198. Mills, K.R. Excitatory and inhibitory effects on human spinal motoneurons from magnetic brain stimulation. Neurosci. Lett., 1988, 94: 297-302. Mortimer, J.A. and Webster, D.D. Evidence for a quantitative association between EMG stretch responses and parkinsonian rigidity. Brain Res., 1983, 162: 169-173. Rossini, P.M. Methodological and physiological aspects of motor evoked potentials. In: P.M. Rossini and F. Maugui~re (Eds.), New Trends and Advanced Techniques in Clinical Neurophysiology (EEG Suppl. 41). Elsevier Science Publishers, Amsterdam, 1990: 124-133. Rothwell, J.C., Obeso, J.A., Traub, M.M. and Marsden, C.D. The behaviour o f the long-latency stretch reflex in patients with Parkinson's disease. J. Neurol. Neurosurg. Psychiat., 1983, 46: 35-44. Shahani, B.T. and Young, R.R. Studies of the normal silent period. In: J.E. Desmedt (Ed.), New Developments in Electromyography and Clinical Neurology. Karger, Basel, 1973: 589-602.
158
ELMOCO 90689 Short communication
Silent period measurement revives as a valuable diagnostic tool with transcranial magnetic stimulation Bernhard A. Haug, Paul W. Sch6nle, Christian Knobloch and Martin K6hne Department of Clinical Neurophysiology, Georg August University, D-W-3400 G6ttingen (F.R.G.) (Accepted for publication: 12 November 1991)
Summary
Following magnetic transcranial stimulation (TCS) a post-excitatory pause can be observed in surface electromyographic (EMG) recordings from pre-innervated muscles. We studied the duration of this silent period (SP) in the abductor pollicis brevis muscle while varying the stimulus intensity (SI) and the amount of the voluntary tonic contraction in 23 normal adults aged 20-78 years. A multivariate linear regression analysis revealed a positive correlation of SP with SI and a slight negative correlation with age. In 11 hemiparetic patients a relative increase of the SP was found on the affected side despite normal central motor conduction time. A marked shortening of the SP in relation to controls was observed in 6 parkinsonian patients.
Key words: Electromyographic silent period; Post-excitatory inhibition; Magnetic transcranial stimulation; Pyramidal and extrapyramidal tract
Post-excitatory electromyographic (EMG) silence in muscles during voluntary contraction can be elicited in many ways. The phenomenon has first been observed with electric stimulation of peripheral nerves (Hoffmann 1920), where multiple factors may contribute to form the silent period (SP) (Merton 1951; Burg et al. 1973; Shahani and Young 1973), such as collision of the antidromic volley with descending motor nerve action potentials and a variety of reflex activities. Moreover, the SP is often partially interrupted by the F response. Many of these difficulties can be avoided by mechanical elicitation of the SP (Angel et al. 1965), but elaborate techniques (Higgins and Lieberman 1968) have hampered their introduction to clinical routine. With magnetic transcranial stimulation (TCS) a new method has been introduced that allows precise measurement of the EMG pause without ambiguity from peripheral stimulus artefacts. Using magnetic TCS we tried to re-evaluate SP measurement in normals and in hemiparetic or parkinsonian patients.
Methods The conventional Novametrix Magstim 200 was fitted with the flat concentric coil of 8.5 cm mean diameter and 20 loops, which was centered to the vertex. Either one or the other side of the coil was applied to induce maximum response of the left or right precentral hand area as in muscle evoked potential (MEP) elicitation (Hess et al. 1987). EMG activity was recorded from the respective abductor pollicis brevis (APB) muscle via surface electrodes placed on the belly and tendon. A T6nnies Myograph DA II served as a recording unit, using 0.5 mV/division for the sensitivity and 2 Hz respectively 10 kHz for the cut-off frequency filters. The patient or subject was seated comfortably on an armchair and was asked to maintain a
Correspondence to: Dr. Med. Bernhard Haug, Neurologische Universit~itsklinik, Robert-Koch-Strasse 40, D-W-3400 G6ttingen (F.R.G.), Tel.: (551) 39-8484 or 39-6691.
constant isometric contraction of the ipsilateral muscle. The magnetic impulse to the cortex was triggered 100 msec after starting a 500 msec storage sweep on the oscilloscope, so that pre- and poststimulus activity could be recorded satisfactorily from the screen storage. The direct muscle response was superimposed on the background myographic activity. With some delay (42-50 msec, mean 46 msec) and above a certain stimulus threshold an interval of complete absence of EMG activity followed, referred to as SP. The threshold of SP elicitation (ThrSP) was 25-45% of the maximum output (% MO) of the used stimulator and usually lower than the threshold of MEP elicitation in relaxed muscles. After having determined the individual ThrSP a stimulus intensity (SI) of + 10, + 20, + 30, + 40 and +50% MO above individual ThrSP has been applied. In the normal subjects at each SI the force of voluntary activity has also been varied to be 10, 25, 50, 75 and 100% of maximum force, the latter being defined as that which can be maintained for some 10 sec. To keep it at the desired level, it has been monitored under virtually isometric conditions by a vigorimeter and by visual judgment of the surface EMG interference pattern. In all patients we stuck to fixed values for pre-innervation (half maximum force) and SI ( + 30% MO above individual ThrSP), but measurements were reproduced 5 times on each side, and the arithmetic mean has been used for further calculations.
Results In 10 female and 13 male healthy adults aged 20-78 years we studied the influence of voluntary background activity, SI and age on the duration of the SP. Either of the first two parameters was varied independently in 5 steps as described above, so that 25 measurements have been acquired in each individual. ' Fig. 1 (top) illustrates the findings in a normal subject, when the SI is varied from + 10 to + 50% MO above the individual ThrSP. There is a near-linear increase of SP with SI, and a saturation cannot be achieved within the given limits. A set of 4 measurements at different voluntary activity levels but constant SI in the same subject is pictured in Fig. 1 (bottom). It demonstrates that the SP duration is
159
SILENT PERIOD WITH MAGNETIC STIMULATION Normal (constant
Subject
--
maximal
Stimulus force)
Stimulus Intensity ( + 3 0 * / . M O a b o v e Thr SP)
Normal S u b j e c t 50O/o m a x i m a l force)
Intensity
(~'IoMO a b o v e T h r SP)
s i l e n t period + 10°/. left APB +
20"/o
+ 40"/* right APB + 50 °/,
stimulus
at 1 0 0 m s
stimulus
1.0mV[
at lOOms
1.0
m[ V
i
50ms
i
50ms Normal S u b j e c t -Muscle A c t i v i t y (4-30 O/aM* a b o v e ThrSP) (*/. of m a x i m a l
Right Hemiparesis ( 5 0 " / o m a x i m a l force)
force)
--
Side C o m p a r i s o n ( + 3 0 * / . M O a b o v e Thr SP)
10 */* left APB
25°/.
50"/. right APB 100"/,
s t i m u l u s at 2 0 0 m s
1.0
V
0 * mss l s t i m atu l1 u
, 50ms
Fig. 1. Surface EMG recordings from APB muscle of an individual, who exerts maximal force while the SI is varied (top) and, vice versa, constant Sis are applied while he is varying the voluntary muscle activity (bottom). For the print-outs a Nihon-Kohden Neuropack 4 Mini was used with a sampling rate of 1024/sec, four 500 msec sweeps were recorded and displayed at a reduced sensitivity of 1.0 mV/division, cut-off frequencies 2 Hz and 10 kHz.
1.0 m V [
i
50ms
Fig. 2. Surface EMG recordings from left and right APB muscles of a normal subject (top) and of a patient with right hemiparesis (bottom), showing 2 consecutive peristimulus sweeps on either side. Note the reproducible SP duration and the marked prolongation on the affected side in the patient (bottom 2 tracings). silent period [ms]
200
150
not influenced as long as sufficient EMG activity allows to determine its exact beginning and end. All the measurements in normal subjects have been analyzed by backward stepwise multiple linear regression. It showed that the variable of pre-innervation could be removed without compromise. An approximation of the SP in the APB muscle of normal adults was calculated from 23 healthy individuals with independent values of SI and age. With age there is a slight decrease of SP, illustrated in Fig. 3. Throughout the clinical studies a voluntary muscle contraction of half maximal force and an SI of + 30% MO above individual ThrSP was used. The ThrSP has been found to be equal on both sides in each individual of this sample, so we could apply the same SI for both sides, thereby avoiding ambiguities when comparing side to side. We examined 11 patients aged 49-83 years just prior to dismissal, when they had nearly fully recovered from a small cortical or subcortical infarct. At this time there was hardly any weakness or
100
50
0
iil~ 40
,llll,,lll~ll,ll,Jll~Jl~,Jr, 50
J,,~,,~,lllll
60
70
80
age [ y r s ] potklnsonlsm [~
regression - 2 SD
m m
h e m l / n o , m a l side
[~
heml/po#h, side
regression normols
[~
regression +
2 SO
Fig. 3. Silent period from APB muscle following magnetic TCS. Age-dependent regression curve of 23 healthy controls for intensity +30% MO above individual ThrSP. Individual measurements of patients with hemiparesis (pathological versus normal side) and of parkinsonians (one side only).
B.A. HAUG ET AL.
160 reflex pathology on the affected side, and central motor conduction time CMCT = C M L -
to established neurophysiological methods, especially if they fail to clearly detect assumed pyramidal or extrapyramidal tract pathology.
(F+ D M L ) / 2 ,
calculated from central motor latency (CML), minimal F wave latency (F) and distal motor latency (DML) was normal and equal on both sides. However, the SP measurement often disclosed a prolongation on the affected side, which is more conspicuous with intraindividual side comparison. The findings of a normal individual (Fig. 2, top) and of a patient with slight hemiparesis on the right side (Fig. 2, bottom) clarify the high event-to-event stability in consecutive recordings. Similarly 6 parkinsonian patients aged 46-71 years were studied during adjustment of drug therapy, two of them with unilateral symptoms only. Here a marked shortening of the SP was revealed, in hemiparkinsonism restricted to the affected side. All findings of the clinical study are shown in a bar graph (Fig. 3), allowing comparison to the normal range.
Discussion
In agreement with former studies on the SP following electric peripheral nerve stimulation (Herman 1969; Dietrichson 1971) and TCS (Rossini 1990) we did not find a relationship between SP duration and amount of voluntary muscle activity or contraction force. The positive correlation between cortical SI and SP duration may be explained from different viewpoints. Mills (1988) and Brouwer et al. (1989) have shown that magnetic TCS elicits excitatory and inhibitory cortical inputs to spinal motoneurons. The latter outlast the former for as much as 80 msec and may contribute to the SP according to the SI. Another viewpoint takes proprioceptive reflexes into consideration, which may play a role for the generation of later parts of the SP. Being disinhibited on the affected side in patients with pyramidal tract injury (Burke 1988; Katz and Rymer 1989), they could explain the interside difference of the SP in cerebral infarcts. Side-to-side differences of SP may also reflect an interhemispheric asymmetry of cortical motor thresholds in spastic hemiparesis (Caramia et al. 1991), although in our cases such asymmetry was too small for detection. Thus, prolongation of the SP on the affected side seems to be a very sensitive indicator of ischemic central motor deficits, even if MEPs and CMCTs are normal. In parkinsonism a deficit of basal ganglia inhibition to long-latency responses accounts for a predominance of excitatory inputs to spinal motoneurons (Rothwell et al. 1983), resulting in the typical rigidity (Berardelli et al. 1983; Mortimer and Webster 1983). Rossini states a general lack of sensorimotor integration in a subgroup of parkinsonians, where conditioning stimulation of the median nerve fails to affect the excitability threshold in TCS (personal communication 1991). Recent work on magnetic TCS in parkinsonian patients has also shown that the amplitudes of their MEPs are larger compared to normals (Kandler et al. 1990). Inhibitory inputs following TCS may therefore be less effective and the SP may be shortened or even sometimes interrupted by bursts of activity. The negative correlation of SP duration with age may be seen as an expression of a natural process of aging leading to a physiological state of hypokinesia and relative rigidity, thus parallelling the changes in parkinsonism. Partly it can be explained by the tendency for a higher ThrSP in older people. Further studies may clarify the physiological aspects of the SP elicited by TCS, particularly in bow much it depends on excitatory and inhibitory cortical inputs to motoneurons. Diseases which impair the delicate balance of these pathways may hence be detected and quantified by SP examination. We propose the measurement of the SP elicited by magnetic TCS as a useful and easy-to-perform adjunct
References
Angel, R.W., Eppler, W. and Iannone, A. Silent period produced by unloading of muscle during voluntary contraction. J. Physiol. (Lond.), 1965, 180: 864-870. Berardelli, A., Sabra, A.F. and Hallett, M. Physiological mechanisms of rigidity in Parkinson's disease. J. Neurol. Neurosurg. Psychiat., 1983, 46: 45-53. Brouwer, B., Ashby, P. and Midroni, G. Excitability of corticospinal neurons during tonic muscle contraction in man. Exp. Brain Res., 1989, 74: 649-652. Burg, D., Szumski, A.T. and Struppler, A. Afferent and efferent activation of human muscle receptors involved in reflex and zcoluntary contraction. Exp. Neurol., 1973, 41: 754-768. Burke, D. Spasticity as an adaptation to pyramidal tract injury. Adv. Neurol., 1988, 47: 401-423. Caramia, M.D., Cicinelli, P,, Paradiso, C., Mariorenzi, R., Zarola, F., Bernardi, G. and Rossini, P.M. 'Excitability' changes of muscular responses to magnetic brain stimulation in patients with central motor disorders. Electroenceph. clin. Neurophysiol., 1991, 8l: 243-250. Dietrichson, P. The silent period in spastic, rigid, and normal subjects during isotonic and isometric muscle contractions. Acta Neurol. Scand., 1971, 47: 183-193. Herman, R. Silent period during isometric and isotonic contraction. Arch. Phys. Med. Rehab., 1969, 50: 642-646. 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. (Lond.), 1987, 388: 397-419. Higgins, D.C. and Lieberman, J.S. The muscle silent period: variability in normal man. Electroenceph. clin. Neurophysiol., 1968, 24: 176-182. Hoffmann, P. Demonstration eines Hemmungsreflexes im menschlichen RiJckenmark. Z. Biol., 1920, 70: 515-524. Kandler, R.H., Jarratt, J.A., Sagar, HJ., Gumpert, E.J.W., Venables, G.S., Davies-Jones, G.A.B. and Jordan, N. Abnormalities of central motor conduction in Parkinson's disease. J. Neurol. Sci., 1990, 100: 94-97. Katz, R.T. and Rymer, W.Z. Spastic hypertonia: mechanisms and measurement. Arch. Phys. Med. Rehab., 1989, 70: 144-155. Merton, P.A. The silent period in a muscle of the human hand. J. Physiol. (Lond.), 1951, 114: 183-198. Mills, K.R. Excitatory and inhibitory effects on human spinal motoneurons from magnetic brain stimulation. Neurosci. Lett., 1988, 94: 297-302. Mortimer, J.A. and Webster, D.D. Evidence for a quantitative association between EMG stretch responses and parkinsonian rigidity. Brain Res., 1983, 162: 169-173. Rossini, P.M. Methodological and physiological aspects of motor evoked potentials. In: P.M. Rossini and F. Maugui~re (Eds.), New Trends and Advanced Techniques in Clinical Neurophysiology (EEG Suppl. 41). Elsevier Science Publishers, Amsterdam, 1990: 124-133. Rothwell, J.C., Obeso, J.A., Traub, M.M. and Marsden, C.D. The behaviour o f the long-latency stretch reflex in patients with Parkinson's disease. J. Neurol. Neurosurg. Psychiat., 1983, 46: 35-44. Shahani, B.T. and Young, R.R. Studies of the normal silent period. In: J.E. Desmedt (Ed.), New Developments in Electromyography and Clinical Neurology. Karger, Basel, 1973: 589-602.
