The electromyographic silent period (SP) produced by electrical stimulation of the median and ulnar nerve, before and after lidocaine block of the ulnar nerve at the elbow, was recorded in the voluntarily contracting abductor pollicis brevis (APB) muscle of 4 normal subjects. Prior to block, stimulation of the corresponding segment in either nerve (e.g., wrist and elbow) elicited SPs with similar end points. With more proximal stimulation, the SPs consistently ended earlier. Following the block, ulnar nerve stimulation below the elbow failed to elicit a SP in any subject, despite a mechanical twitch caused by the antagonistic contraction of adductor pollicis muscle. Ulnar nerve stimulation above the block elicited a SP in all subjects similar to the preblock SP. In all 4 subjects, submaximal median nerve stimulation at the wrist produced an H-reflex, followed by a SP in the absence of the direct M-response. This SP, due to selective activation of sensory fibers, lacked a collision component, but, was otherwise similar to the SP elicited by supramaximal wrist stimulation. These findings indicate that the ascending volley following electrical stimulation of a mixed peripheral nerve produces the SP without apparent contribution from the descending motor volley. Key words: silent period electromyogram peripheral nerve H-reflex muscle spindle MUSCLE 81 NERVE 14:1202-1208 1991
THE SILENT PERIOD PRODUCED BY ELECTRICAL STIMULATION OF MIXED PERIPHERAL NERVES A. ARTURO LEIS, MD, MARK A. ROSS, MD, TAKUMI EMORI, MD, YOSHlHlKO MATSUE, MD, and TAKANORI SAITO, MD
Axons within the mixed peripheral nerve that are directly activated by an electrical stimulus carry two volleys of impulses, one which ascends to the spinal cord and the other which descends to produce the direct muscle r e s p o n ~ e . ~The ~ ' ~ascending volley consists of orthodromic sensory or antidromic motor impulses, while the descending volley contains orthodromic motor or antidromic sensory impulses. It has been generally accepted that the SP produced by electrical stimulation of a
From the Division of Restorative Neurology and Human Neurobiology, Baylor College of Medicine, Houston, Texas (Dr Leis), and Department of Neurology, University of Iowa Hospitals and Clinics, Iowa City, Iowa (Drs. Ross, Emori, Matsue, and Saito). Acknowledgment: We thank Sheila Mennen and Sandra Knowlson for their assistance in the manuscript preparation. AAEM Young Investigator Award Winner. Presented at the 37th Annual Scientific Meeting of the American Association of Electrodiagnostic Medicine (AAEM) Chicago, Illinois, September 7-8, 1990. Address reprint requests to A. Arturo Leis, MD, Division of Restorative Neurology and Human Neurobiology, One Baylor Plaza, Room S815, Texas Medical Center, Houston, TX 77030. Accepted for publication December 24, 1990. CCC 0148-639X/91/01201202-07 $04.00 0 1991 John Wiley & Sons, Inc.
1202
The Silent Period
mixed peripheral nerve is largely dependent on the descending volley and the mechanical changes created by the superimposed direct muscle twitch. Matthews' (1931) showed that a mechanical twitch of an isolated frog muscle modified the discharges from muscle spindles, and postulated that a "spindle pause" could be responsible for the SP in humans. Mertong (1951) concluded that the SP resulted from the descending motor volley and that the ascending volley was not even partially responsible for the SP. Higgins and Lieberman* (1968) also attributed the SP to a pause in spindle discharges and considered the burst of EMG activity which terminates the SP to result from spindle excitation during stretch of the muscle in the falling phase of the twitch. Shahani and Young13 (1970) contended that much of the second half of the SP was related to changes produced in spindle discharges by the superimposed twitch, but also stressed the importance of hitherto ignored cutaneous mechanisms. Miles et a1.l' (1989) likewise concluded that a late component of the SP was dependent on timing of the twitch evoked by the stimulus. Few investigators have attributed the development of
MUSCLE & NERVE
December 1991
the SP exclusively to the ascending volley. McLellan (1973),' however, found no correlation between the degree of muscle shortening during the twitch contraction and the duration of the SP. He concluded that the end point of the SP was determined by the ascending volley via an inhibitory spinal reflex, with no indication that changes in spindle activity contributed to the SP. T h e purpose of the present study was to establish the role of the descending and ascending action potential volleys, following electrical stimulation of a mixed peripheral nerve, in the genesis of the SP. MATERIALS AND METHODS
Four healthy men, ages 32 to 42 years, voluntarily participated in 3 experiments designed to assess descending and ascending volley contribution to the SP. Experiment 1-Isolation of the Descending and Ascending Volley. We studied the SP evoked by
electrical stimulation of the ulnar nerve while subjects maintained constant isometric abduction of the thumb. T h e SP was recorded with the active surface electrode (Gl) placed over the belly of the APB muscle, and the reference electrode (G2) over the tendon. Single shocks were delivered to the ulnar nerve, sequentially, at the wrist and elbow. Stimuli were square waves 0.1 to 0.4 ms in duration. Stimulus intensity was 25% above supramaximal for the direct M-response recorded from the abductor digiti minimi (ADM) muscle. Consecutive SP responses from each site were displayed with a stepwise vertical shift of the baseline on the storage oscilloscope. Filter settings ranged from 20 Hz to 10 kHz. The sweep was 20 ms/cm. A relative or absolute decrease in the voluntary EMG activity identified the SP. The ulnar nerve was then blocked at the elbow, using sterile technique, by injecting 2 to 3 cc of 2% lidocaine. A complete conduction block was documented electrophysiologically. Following the block, the ulnar nerve was again stimulated while subjects maintained thumb abduction. The cathode was positioned distal to the anode when stimulating below the block and proximally when stimulating above the block. Stimulation below the block evoked only descending volley influence, because the ascending impulses were blocked at the elbow. The descending volley produced brief adduction in the previously abducted thumb, due to the synchronous contraction of ulnar-innervated hand muscles, in-
The Silent Period
cluding the antagonistic adductor pollicis muscle. Stimulation above the block isolated the ascending volley by preventing passage of descending impulses. Using this method, we were able to electrophysiologically isolate the descending and ascending volleys, and to study the independent contribution of each volley to the SP elicited in a nonhomonymous muscle (e.g., a muscle not innervated by the nerve that is stimulated). Experiment 2-Selective bers. This portion of
Activation of Sensory Fi-
Experiment 3-Movement
of the Site of Stimulation.
the study assessed the effects of selective activation of median nerve sensory fibers on the voluntary EMG activity in the homonymous APB muscle. We accomplished selective sensory fiber activation by delivery of a stimulus that was subthreshold for motor fibers, yet evoked an H-reflex r e ~ p o n s e .The ~ H-reflex was recorded with G1 placed over the APB and G2 over the tendon. Subjects maintained steady abduction of the thumb under isometric and isotonic conditions. T h e latter condition was achieved by placing the thumb in a metal loop attached to a 1-kg weight via a pully device. The adductor pollicis muscle remained completely relaxed to palpation during thumb abduction. T h e cathode was positioned proximal to the anode, and placed directly over the median nerve at the wrist. Shock intensity was carefully adjusted until consecutive H-reflex responses were elicited without any direct M-responses. No mechanical twitch was observed following the shocks. Stimulus duration was 1.0 ms. Using this technique, we looked for changes in the EMG activity of the ABP muscle. In addition, we tested the effect of pure cutaneous sensory fiber activation on the EMG activity of the APB muscle. This was accomplished by delivering single shocks to the digital nerve of each digit with the cathode positioned on the fingertip proximal to the anode. Recording technique was as previously described.
The third part of the study assessed the change in SP end-point latencies with distal and proximal stimulation. Belly-tendon recordings were made from the APB muscle under isometric and isotonic conditions. Each subject received 8 consecutive electrical shocks, with the cathode placed directly over the mixed nerve and the anode away from the nerve, at several sites in the upper extremity; for the median nerve, the cathode was placed at the wrist, elbow, and upper arm, and, for the ulnar nerve, at the wrist and above elbow.
MUSCLE &
NERVE
December 1991
1203
The distance between each site was measured. Consecutive responses from each site were recorded, and the EMG activity in the APB muscle was displayed with a stepwise vertical shift of the baseline on the oscilloscope. Shocks were 0.2 to 0.4 ms in duration with stimulus intensity 25% above supramaximal for the M-response at all sites. Surface electrode recordings from the ADM muscle ensured maximum M-response amplitudes following ulnar nerve stimulation. The sweep was 20 ms/cm. Periods of EMG silence, and their end points following stimulation at the different sites, were identified and measured. The SP end point was taken as the return of uninterrupted voluntary EMG activity.
nerve at the elbow, stimulation below the block, which isolated the descending volley, produced no periods of silence or potentiation in the EMG activity of the APB muscle in any of the 4 subjects (Fig. 2). The mechanical twitch of ulnar innervated hand muscles altered the position of the abducted thumb, but did not influence the EMG activity of the APB muscle. Stimulation above the block, which isolated the ascending volley, readily reproduced the complete SP seen prior to the block in all 4 subjects (Fig. 3). No significant change in the onset or end point of the SP occurred, before or after block, with stimulation above the elbow.
RESULTS
dian nerve at the wrist, during isometric and isotonic abduction of the thumb, generated H-reflex potentials and a SP in the APB muscle in all 4 subjects (Fig. 4).Stimuli were subthreshold for the direct M-response, and no muscle twitch occurred.
Experiment 1-Isolation of the Descending and Ascending Volley. Stimulation of the ulnar nerve at
the wrist and elbow elicited an SP in the median nerve innervated APB muscle in all 4 subjects (Fig. 1). Following lidocaine block of the ulnar
Experiment 2-Selective Activation of Sensory Fibers. Delivery of submaximal stimuli to the me-
Ulnar Nerve
Ulnar Nerve Site of stimulation
Site of stimulation
Wrist Wrist
Wrist Elbow
CT
(1V
The Silent Period
L
V
2 0 ms
20 ms
FIGURE 1. Silent period in the APE muscle after stimulation (open arrow) of the ulnar nerve at the wrist (top 3 tracings) and elbow (bottom 3 tracings).
1204
CT
FIGURE 2. Silent period in the APE muscle after stimulation (open arrow) of the ulner nerve at the wrist (top 3 tracings). Stimulation at the same site after lidocaine block of the ulnar nerve at the elbow did not produce the silent period (bottom 3 tracings).
MUSCLE & NERVE
December 1991
Ulnar Nerve
Median N e r v e Site of stimul at ion
Site of stimulation
H
Elbow
Wrist
Elbow
U
L
V
20 ms
FIGURE 3. Silent period in the APE muscle after stimulation (open arrow) of the ulnar nerve at the elbow (top 3 tracings). Stimulation at the same site after lidocaine block of the ulnar nerve at the elbow reproduced the silent period (bottom 3 tracings).
The SP in any one individual was similar under isotonic or isometric recording conditions. The onset of the SP in all subjects occurred immediately following the H-reflex response, and had a mean latency of 40 ms. Because motor fibers were not electrically activated, the contribution to the early portion of the SP from collision of antidromic motor with volitional orthodromic motor impulses was avoided. The duration of the SP was 60 to 65 ms with the end point at 100 ms (range 92 to 114 ms). A brief burst of EMG activity often interrupted the SP at about 15 ms after its onset, otherwise, the SP elicited by selective sensory fiber activation was surprisingly similar to the SP elicited by supramaximal stimulation (Fig. 4). I n all subjects, the digital nerve stimulation produced a complete SP in the voluntary EMG activity of the APB muscle, irrespective of the digit that was stimulated (Fig. 5 ) . This cutaneous SP lasted about 50 ms, with an onset and end point of roughly 70 ms and 120 ms, respectively, and
The Silent Period
L5mV 1Oms FIGURE 4. H-reflex (H) followed by the silent period in the APE muscle under isotonic conditions after stimulation of the median nerve at the wrist (top tracings). Stimuli were subthreshold for the direct M-response. Supramaximal stimulation at the same site (bottom tracings) produced the direct M-response, F-wave (F), and the silent period. Note similarity of the silent periods elicited by selective activation of sensory fibers (top) and supramaximal stimulation (bottom).
showed only slight variation in latency from digit to digit. Experiment 3-Movement
of the Site of Stimulation.
In all subjects, the SP produced by supramaximal stimulation of the median or ulnar nerve at a proximal site consistently ended earlier than the SP elicited by more distal stimulation, despite the increased latency of the twitch response (Fig. 6). The mean difference in the SP end point between wrist and elbow sites was 18 ms for median nerve, and 21 ms for ulnar nerve stimulation. Table 1 summarizes the data from the 4 subjects (numbers 1 through 4) following consecutive stimuli to the mixed nerve at distal and proximal sites under isotonic conditions. Similar results were obtained during isometric contraction.
MUSCLE & NERVE
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1205
~~
Table 1. Silent periods recorded in the abductor pollicis brevis muscle under isotonic conditions
1 Site of stimulation
2
Median Nerve Wrist
Rt 3 A
Elbow
Arm
FIGURE 5. Cutaneous silent periods recorded from the APB muscle after stimulation (open arrow) of the distal index finger (top tracing), middle finger (second tracing), ring finger (third tracing), and little finger (bottom tracing). Note the reproducible and complete silent period irrespective of the digit stimulated.
Ulnar Nerve Wrist
Elbow
Median Nerve Site of stirnulation
Subject
Individual mean SP end point (ms)
Individual range SP end point (ms)
1 2 3 4
116 104 120 116
112-124 98-108 114-126 108- 120
1 2 3 4
99 86 100 98
94-108 84-90 96- 106 90-104
1 2 3 4
88
80-94
84 92
80-88 90-96
1 2 3 4
110 102 112 106
98-114 97-106 108-116 102-1 10
1 2 3 4
94 84 86 86
86-98 82-88 82-90 80-90
Group mean (ms)
114
96
88
108
87
'Data missing.
Wrist
DISCUSSION
Elbow
E5mV lOms FIGURE 6. The direct M-response, F-wave (F), and silent period in the APB muscle under isotonic conditions after stimulation of the median nerve at the wrist (top 4 tracings). Stimulation at the elbow (bottom 4 tracings) produced a silent period that ended 15 to 20 ms earlier.
1206
The Silent Period
This study shows that the SP following electrical stimulation of a mixed peripheral nerve results from the effects of the ascending action potential volley. This ascending volley consists of orthodromic sensory and antidromic motor impulses directly activated by the electrical The first experiment provides direct evidence that the ascending volley produces a complete SP in a nonhomonymous muscle. Following the ulnar nerve block at the elbow, generation of the ascending volley, by stimulating above the block, elicited the SP in the non-homonymous APB muscle in all subjects (Fig. 3). Stimulation below the block, which generated only the descending volley, produced neither silence nor potentiation in the EMG activity of the APB muscle, despite an adduction twitch that briefly altered the position of the abducted thumb (Fig. 2). This mechanical twitch, due to the synchronous contraction of ulnar innervated hand muscles, including the antagonistic adductor pollicis muscle, presumably modified discharges from spindles in the APB muscle, since APB muscle
MUSCLE & NERVE
December 1991
length changed slightly. Experiments with unloading of muscle during voluntary contractions suggest that even slight muscle length changes (0.28 cm in biceps brachii) can modify spindle discharges.' In spite of this, we found no evidence that the descending volley influenced the EMG activity in the APB muscle. Results from the second experiment indicate that an SP following submaximal mixed nerve stimulation can be produced in the homonymous muscle in the absence of recordable motor fiber activation. Delivery of a stimulus subthreshold for alpha motor fibers is unlikely to activate the smaller, less excitable gamma motor axons innervating intrafusal muscle fibers.37' Under these conditions, orthodromic sensory impulses in the ascending volley likely generate the SP. Following selective sensory fiber activation in the mixed nerve, the usual collision of antidromic with volitional orthodromic motor impulses cannot occur, and no EMG silence is seen during the first 30 ms following the stimulus (Fig. 4). The brief burst of EMG activity, which occasionally interrupts the SP about 15 ms after its onset, may be a consequence of the weak stimulus that fails to generate the antidromic motor impulses needed to fully activate Renshaw cell i n h i b i t i ~ n . 'Studies ~ in the cat have shown greater Renshaw cell activity following antidromic rather than orthodromic activation of the motor neuron ~ 0 0 1 . 'Except ~ for this collision effect and the occasional voluntary potentials that interrupt the SP, selective activation of sensory impulses produces a SP similar to the SP elicited by supramaximal stimulation. Clearly, the superimposed mechanical twitch following mixed nerve stimulation is not necessary to produce this SP. Additionally, we demonstrated, as have oththat activation of cutaneous sensory fibers following digital nerve stimulation can produce a complete SP. T h e same afferent fibers that originate in the fingertips are presumably activated during more proximal electrical stimulation of the mixed nerve. In light of such observations, it is difficult to understand how some investigators concluded that the SP resulted primarily from the superimposed mechanical and that the ascending volley was not even partially responsible for the SP.9 The results of the third experiment, dealing with movement of the site of stimulation, confirm McLellan's findings' and indicate that the end point of the SP is determined by the ascending volley and independent of the superimposed
'
The Silent Period
twitch. In all subjects, the SP end point produced in a homonymous and a non-homonymous muscle by stimulation at a proximal site, was consistently shorter than that produced by distal stimulation (Table 1). This indicates that the impulses destined to produce this portion of the SP, like the impulses that generate the F-wave (Fig. 6), first travel away from the recording electrodes toward the spinal cord. If the descending volley contributed to this portion of the SP, then proximal stimulation, which generates an M-response and muscle twitch of increased latency, should have produced a SP that ended later. This was never observed in multiple trials. Our findings lead us to conclude that the ascending volley, following electrical stimulation of a mixed peripheral nerve, produces the SP, without apparent contribution from the descending volley. The first 30 ms of the SP produced by supramaximal stimulation results from the collision of antidromic with orthodromic motor The next portion of the SP can best be seen by using submaximal stimulation, and corresponds to the segment from the H-reflex response (30 ms) to the end of the voluntary potentials that interrupt the SP (60 ms). This segment of the SP occurs too soon to be explicable on the basis of either cutaneous or possible descending volley e f f e c t ~ ,and ' ~ seems to be dependent on the ability of the antidromic motor volley to maximally activate Renshaw cell inhibition. The latter half of the SP can be attributed entirely to cutaneous afferent impulses which, in isolation, produce a complete SP between 70 and 120 ms after digital stimulation. With more proximal stimulation, these same cutaneous fibers are activated within the mixed nerve. Our calculations, and those of McClellan,' suggest that these afferent impulses are carried by slowly conducting fibers at a rate of 10 to 15 m/s. This explains the much greater latency shift of the SP end point with movement of the site of stimulation compared with the F-wave o r H-reflex response, which also result from the effects of the ascending volley, but are generated by impulses carried in faster conducting fibers. Previous theories implicating the superimposed electrically induced twitch and muscle spindle pause in the genesis of the SP must take into account that a SP can be elicited in the homonymous muscle from mixed nerve stimulation in absence of mechanical twitch. Furthermore, a complete SP can be obtained in the non-homonymous muscle in absence of the descending volley. Finally,
MUSCLE & NERVE
December 1991
1207
nally, only the ascending volley theory adequately explains the contribution to the SP from cutaneous
effects, and the unequivocal shortening in the SP end point seen with more proximal stimulation.
REFERENCES
1. Angel RW, Eppler W, Iannone A: Silent period produced by unloading of muscle during voluntary contraction. J Physiol 1965;180:864-870. 2. Caccia MR, McComas AJ, Upton ARM, Blogg T: Cutaneous reflexes in small muscles of the hand. J Neurol Neurosurg Psychiatly 1973;36:960- 977. 3. Erlanger J, Gasser HS: The compound nature of the action current of nerve as disclosed by the cathode ray oscillograph. Am J Physiol 1924;70:624-666. 4. Higgins DC, Lieberman JS: The muscle silent period and spindle function in man. Electroenceph Clin Neurophysiol 1968;25:238-243. 5. Kimura J: H, T, masseter, and other reflexes, in Electrodiagnosis in Diseases of Nerue and Muscle: Principles and Practice, 2 ed. Philadelphia, FA Davis, 1989, pp 356-374. 6. Kranz H, Adorjani C, Baumgartner G: The effect of nociceptive cutaneous stimuli on human motoneurons. Brain 1973;96:57 1-590. 7. Matthews BHC: The response of a muscle spindle during active contraction of a muscle. J Physiol 1931;72:153- 174.
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The Silent Period
8. McLellan DL: The electromyographic silent period produced by supramaximal electrical stimulation in normal man. J Neurol Neurosurg Psychiatry 1973;36:334-341. 9. Merton PA: The silent period in a muscle of the human hand. JPhysiol 1951;114:183-198. 10. Miles TS, Le T H , Turker KS: Biphasic inhibitory responses and their IPSPs evoked by tibia1 nerve stimulation in human soleus motor neurones. Exp Brain Res 1989; 77~637-645. 1 1 . Ruffini A: On the minute anatomy of the neuromuscvlar spindles of the cat, and on their physiological significance. J Physiol 1898;23:190-208. 12. Ryall RW, Piercey MF, Polosa C, Goldfarb J: Excitation of Renshaw cells in relation to orthodromic and anti-dromic excitation of motorneurons. J Neurophysiol 1972;35:137148. 13. Shahani BT, Young RR: Studies of the normal human silent period, in Desmedt JE (ed): New Developments in Electromyography and Clinical Neurophysiology. Karger, Basel, 1973, vol 3, pp 589-602.
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THE SILENT PERIOD PRODUCED BY ELECTRICAL STIMULATION OF MIXED PERIPHERAL NERVES A. ARTURO LEIS, MD, MARK A. ROSS, MD, TAKUMI EMORI, MD, YOSHlHlKO MATSUE, MD, and TAKANORI SAITO, MD
Axons within the mixed peripheral nerve that are directly activated by an electrical stimulus carry two volleys of impulses, one which ascends to the spinal cord and the other which descends to produce the direct muscle r e s p o n ~ e . ~The ~ ' ~ascending volley consists of orthodromic sensory or antidromic motor impulses, while the descending volley contains orthodromic motor or antidromic sensory impulses. It has been generally accepted that the SP produced by electrical stimulation of a
From the Division of Restorative Neurology and Human Neurobiology, Baylor College of Medicine, Houston, Texas (Dr Leis), and Department of Neurology, University of Iowa Hospitals and Clinics, Iowa City, Iowa (Drs. Ross, Emori, Matsue, and Saito). Acknowledgment: We thank Sheila Mennen and Sandra Knowlson for their assistance in the manuscript preparation. AAEM Young Investigator Award Winner. Presented at the 37th Annual Scientific Meeting of the American Association of Electrodiagnostic Medicine (AAEM) Chicago, Illinois, September 7-8, 1990. Address reprint requests to A. Arturo Leis, MD, Division of Restorative Neurology and Human Neurobiology, One Baylor Plaza, Room S815, Texas Medical Center, Houston, TX 77030. Accepted for publication December 24, 1990. CCC 0148-639X/91/01201202-07 $04.00 0 1991 John Wiley & Sons, Inc.
1202
The Silent Period
mixed peripheral nerve is largely dependent on the descending volley and the mechanical changes created by the superimposed direct muscle twitch. Matthews' (1931) showed that a mechanical twitch of an isolated frog muscle modified the discharges from muscle spindles, and postulated that a "spindle pause" could be responsible for the SP in humans. Mertong (1951) concluded that the SP resulted from the descending motor volley and that the ascending volley was not even partially responsible for the SP. Higgins and Lieberman* (1968) also attributed the SP to a pause in spindle discharges and considered the burst of EMG activity which terminates the SP to result from spindle excitation during stretch of the muscle in the falling phase of the twitch. Shahani and Young13 (1970) contended that much of the second half of the SP was related to changes produced in spindle discharges by the superimposed twitch, but also stressed the importance of hitherto ignored cutaneous mechanisms. Miles et a1.l' (1989) likewise concluded that a late component of the SP was dependent on timing of the twitch evoked by the stimulus. Few investigators have attributed the development of
MUSCLE & NERVE
December 1991
the SP exclusively to the ascending volley. McLellan (1973),' however, found no correlation between the degree of muscle shortening during the twitch contraction and the duration of the SP. He concluded that the end point of the SP was determined by the ascending volley via an inhibitory spinal reflex, with no indication that changes in spindle activity contributed to the SP. T h e purpose of the present study was to establish the role of the descending and ascending action potential volleys, following electrical stimulation of a mixed peripheral nerve, in the genesis of the SP. MATERIALS AND METHODS
Four healthy men, ages 32 to 42 years, voluntarily participated in 3 experiments designed to assess descending and ascending volley contribution to the SP. Experiment 1-Isolation of the Descending and Ascending Volley. We studied the SP evoked by
electrical stimulation of the ulnar nerve while subjects maintained constant isometric abduction of the thumb. T h e SP was recorded with the active surface electrode (Gl) placed over the belly of the APB muscle, and the reference electrode (G2) over the tendon. Single shocks were delivered to the ulnar nerve, sequentially, at the wrist and elbow. Stimuli were square waves 0.1 to 0.4 ms in duration. Stimulus intensity was 25% above supramaximal for the direct M-response recorded from the abductor digiti minimi (ADM) muscle. Consecutive SP responses from each site were displayed with a stepwise vertical shift of the baseline on the storage oscilloscope. Filter settings ranged from 20 Hz to 10 kHz. The sweep was 20 ms/cm. A relative or absolute decrease in the voluntary EMG activity identified the SP. The ulnar nerve was then blocked at the elbow, using sterile technique, by injecting 2 to 3 cc of 2% lidocaine. A complete conduction block was documented electrophysiologically. Following the block, the ulnar nerve was again stimulated while subjects maintained thumb abduction. The cathode was positioned distal to the anode when stimulating below the block and proximally when stimulating above the block. Stimulation below the block evoked only descending volley influence, because the ascending impulses were blocked at the elbow. The descending volley produced brief adduction in the previously abducted thumb, due to the synchronous contraction of ulnar-innervated hand muscles, in-
The Silent Period
cluding the antagonistic adductor pollicis muscle. Stimulation above the block isolated the ascending volley by preventing passage of descending impulses. Using this method, we were able to electrophysiologically isolate the descending and ascending volleys, and to study the independent contribution of each volley to the SP elicited in a nonhomonymous muscle (e.g., a muscle not innervated by the nerve that is stimulated). Experiment 2-Selective bers. This portion of
Activation of Sensory Fi-
Experiment 3-Movement
of the Site of Stimulation.
the study assessed the effects of selective activation of median nerve sensory fibers on the voluntary EMG activity in the homonymous APB muscle. We accomplished selective sensory fiber activation by delivery of a stimulus that was subthreshold for motor fibers, yet evoked an H-reflex r e ~ p o n s e .The ~ H-reflex was recorded with G1 placed over the APB and G2 over the tendon. Subjects maintained steady abduction of the thumb under isometric and isotonic conditions. T h e latter condition was achieved by placing the thumb in a metal loop attached to a 1-kg weight via a pully device. The adductor pollicis muscle remained completely relaxed to palpation during thumb abduction. T h e cathode was positioned proximal to the anode, and placed directly over the median nerve at the wrist. Shock intensity was carefully adjusted until consecutive H-reflex responses were elicited without any direct M-responses. No mechanical twitch was observed following the shocks. Stimulus duration was 1.0 ms. Using this technique, we looked for changes in the EMG activity of the ABP muscle. In addition, we tested the effect of pure cutaneous sensory fiber activation on the EMG activity of the APB muscle. This was accomplished by delivering single shocks to the digital nerve of each digit with the cathode positioned on the fingertip proximal to the anode. Recording technique was as previously described.
The third part of the study assessed the change in SP end-point latencies with distal and proximal stimulation. Belly-tendon recordings were made from the APB muscle under isometric and isotonic conditions. Each subject received 8 consecutive electrical shocks, with the cathode placed directly over the mixed nerve and the anode away from the nerve, at several sites in the upper extremity; for the median nerve, the cathode was placed at the wrist, elbow, and upper arm, and, for the ulnar nerve, at the wrist and above elbow.
MUSCLE &
NERVE
December 1991
1203
The distance between each site was measured. Consecutive responses from each site were recorded, and the EMG activity in the APB muscle was displayed with a stepwise vertical shift of the baseline on the oscilloscope. Shocks were 0.2 to 0.4 ms in duration with stimulus intensity 25% above supramaximal for the M-response at all sites. Surface electrode recordings from the ADM muscle ensured maximum M-response amplitudes following ulnar nerve stimulation. The sweep was 20 ms/cm. Periods of EMG silence, and their end points following stimulation at the different sites, were identified and measured. The SP end point was taken as the return of uninterrupted voluntary EMG activity.
nerve at the elbow, stimulation below the block, which isolated the descending volley, produced no periods of silence or potentiation in the EMG activity of the APB muscle in any of the 4 subjects (Fig. 2). The mechanical twitch of ulnar innervated hand muscles altered the position of the abducted thumb, but did not influence the EMG activity of the APB muscle. Stimulation above the block, which isolated the ascending volley, readily reproduced the complete SP seen prior to the block in all 4 subjects (Fig. 3). No significant change in the onset or end point of the SP occurred, before or after block, with stimulation above the elbow.
RESULTS
dian nerve at the wrist, during isometric and isotonic abduction of the thumb, generated H-reflex potentials and a SP in the APB muscle in all 4 subjects (Fig. 4).Stimuli were subthreshold for the direct M-response, and no muscle twitch occurred.
Experiment 1-Isolation of the Descending and Ascending Volley. Stimulation of the ulnar nerve at
the wrist and elbow elicited an SP in the median nerve innervated APB muscle in all 4 subjects (Fig. 1). Following lidocaine block of the ulnar
Experiment 2-Selective Activation of Sensory Fibers. Delivery of submaximal stimuli to the me-
Ulnar Nerve
Ulnar Nerve Site of stimulation
Site of stimulation
Wrist Wrist
Wrist Elbow
CT
(1V
The Silent Period
L
V
2 0 ms
20 ms
FIGURE 1. Silent period in the APE muscle after stimulation (open arrow) of the ulnar nerve at the wrist (top 3 tracings) and elbow (bottom 3 tracings).
1204
CT
FIGURE 2. Silent period in the APE muscle after stimulation (open arrow) of the ulner nerve at the wrist (top 3 tracings). Stimulation at the same site after lidocaine block of the ulnar nerve at the elbow did not produce the silent period (bottom 3 tracings).
MUSCLE & NERVE
December 1991
Ulnar Nerve
Median N e r v e Site of stimul at ion
Site of stimulation
H
Elbow
Wrist
Elbow
U
L
V
20 ms
FIGURE 3. Silent period in the APE muscle after stimulation (open arrow) of the ulnar nerve at the elbow (top 3 tracings). Stimulation at the same site after lidocaine block of the ulnar nerve at the elbow reproduced the silent period (bottom 3 tracings).
The SP in any one individual was similar under isotonic or isometric recording conditions. The onset of the SP in all subjects occurred immediately following the H-reflex response, and had a mean latency of 40 ms. Because motor fibers were not electrically activated, the contribution to the early portion of the SP from collision of antidromic motor with volitional orthodromic motor impulses was avoided. The duration of the SP was 60 to 65 ms with the end point at 100 ms (range 92 to 114 ms). A brief burst of EMG activity often interrupted the SP at about 15 ms after its onset, otherwise, the SP elicited by selective sensory fiber activation was surprisingly similar to the SP elicited by supramaximal stimulation (Fig. 4). I n all subjects, the digital nerve stimulation produced a complete SP in the voluntary EMG activity of the APB muscle, irrespective of the digit that was stimulated (Fig. 5 ) . This cutaneous SP lasted about 50 ms, with an onset and end point of roughly 70 ms and 120 ms, respectively, and
The Silent Period
L5mV 1Oms FIGURE 4. H-reflex (H) followed by the silent period in the APE muscle under isotonic conditions after stimulation of the median nerve at the wrist (top tracings). Stimuli were subthreshold for the direct M-response. Supramaximal stimulation at the same site (bottom tracings) produced the direct M-response, F-wave (F), and the silent period. Note similarity of the silent periods elicited by selective activation of sensory fibers (top) and supramaximal stimulation (bottom).
showed only slight variation in latency from digit to digit. Experiment 3-Movement
of the Site of Stimulation.
In all subjects, the SP produced by supramaximal stimulation of the median or ulnar nerve at a proximal site consistently ended earlier than the SP elicited by more distal stimulation, despite the increased latency of the twitch response (Fig. 6). The mean difference in the SP end point between wrist and elbow sites was 18 ms for median nerve, and 21 ms for ulnar nerve stimulation. Table 1 summarizes the data from the 4 subjects (numbers 1 through 4) following consecutive stimuli to the mixed nerve at distal and proximal sites under isotonic conditions. Similar results were obtained during isometric contraction.
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~~
Table 1. Silent periods recorded in the abductor pollicis brevis muscle under isotonic conditions
1 Site of stimulation
2
Median Nerve Wrist
Rt 3 A
Elbow
Arm
FIGURE 5. Cutaneous silent periods recorded from the APB muscle after stimulation (open arrow) of the distal index finger (top tracing), middle finger (second tracing), ring finger (third tracing), and little finger (bottom tracing). Note the reproducible and complete silent period irrespective of the digit stimulated.
Ulnar Nerve Wrist
Elbow
Median Nerve Site of stirnulation
Subject
Individual mean SP end point (ms)
Individual range SP end point (ms)
1 2 3 4
116 104 120 116
112-124 98-108 114-126 108- 120
1 2 3 4
99 86 100 98
94-108 84-90 96- 106 90-104
1 2 3 4
88
80-94
84 92
80-88 90-96
1 2 3 4
110 102 112 106
98-114 97-106 108-116 102-1 10
1 2 3 4
94 84 86 86
86-98 82-88 82-90 80-90
Group mean (ms)
114
96
88
108
87
'Data missing.
Wrist
DISCUSSION
Elbow
E5mV lOms FIGURE 6. The direct M-response, F-wave (F), and silent period in the APB muscle under isotonic conditions after stimulation of the median nerve at the wrist (top 4 tracings). Stimulation at the elbow (bottom 4 tracings) produced a silent period that ended 15 to 20 ms earlier.
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The Silent Period
This study shows that the SP following electrical stimulation of a mixed peripheral nerve results from the effects of the ascending action potential volley. This ascending volley consists of orthodromic sensory and antidromic motor impulses directly activated by the electrical The first experiment provides direct evidence that the ascending volley produces a complete SP in a nonhomonymous muscle. Following the ulnar nerve block at the elbow, generation of the ascending volley, by stimulating above the block, elicited the SP in the non-homonymous APB muscle in all subjects (Fig. 3). Stimulation below the block, which generated only the descending volley, produced neither silence nor potentiation in the EMG activity of the APB muscle, despite an adduction twitch that briefly altered the position of the abducted thumb (Fig. 2). This mechanical twitch, due to the synchronous contraction of ulnar innervated hand muscles, including the antagonistic adductor pollicis muscle, presumably modified discharges from spindles in the APB muscle, since APB muscle
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December 1991
length changed slightly. Experiments with unloading of muscle during voluntary contractions suggest that even slight muscle length changes (0.28 cm in biceps brachii) can modify spindle discharges.' In spite of this, we found no evidence that the descending volley influenced the EMG activity in the APB muscle. Results from the second experiment indicate that an SP following submaximal mixed nerve stimulation can be produced in the homonymous muscle in the absence of recordable motor fiber activation. Delivery of a stimulus subthreshold for alpha motor fibers is unlikely to activate the smaller, less excitable gamma motor axons innervating intrafusal muscle fibers.37' Under these conditions, orthodromic sensory impulses in the ascending volley likely generate the SP. Following selective sensory fiber activation in the mixed nerve, the usual collision of antidromic with volitional orthodromic motor impulses cannot occur, and no EMG silence is seen during the first 30 ms following the stimulus (Fig. 4). The brief burst of EMG activity, which occasionally interrupts the SP about 15 ms after its onset, may be a consequence of the weak stimulus that fails to generate the antidromic motor impulses needed to fully activate Renshaw cell i n h i b i t i ~ n . 'Studies ~ in the cat have shown greater Renshaw cell activity following antidromic rather than orthodromic activation of the motor neuron ~ 0 0 1 . 'Except ~ for this collision effect and the occasional voluntary potentials that interrupt the SP, selective activation of sensory impulses produces a SP similar to the SP elicited by supramaximal stimulation. Clearly, the superimposed mechanical twitch following mixed nerve stimulation is not necessary to produce this SP. Additionally, we demonstrated, as have oththat activation of cutaneous sensory fibers following digital nerve stimulation can produce a complete SP. T h e same afferent fibers that originate in the fingertips are presumably activated during more proximal electrical stimulation of the mixed nerve. In light of such observations, it is difficult to understand how some investigators concluded that the SP resulted primarily from the superimposed mechanical and that the ascending volley was not even partially responsible for the SP.9 The results of the third experiment, dealing with movement of the site of stimulation, confirm McLellan's findings' and indicate that the end point of the SP is determined by the ascending volley and independent of the superimposed
'
The Silent Period
twitch. In all subjects, the SP end point produced in a homonymous and a non-homonymous muscle by stimulation at a proximal site, was consistently shorter than that produced by distal stimulation (Table 1). This indicates that the impulses destined to produce this portion of the SP, like the impulses that generate the F-wave (Fig. 6), first travel away from the recording electrodes toward the spinal cord. If the descending volley contributed to this portion of the SP, then proximal stimulation, which generates an M-response and muscle twitch of increased latency, should have produced a SP that ended later. This was never observed in multiple trials. Our findings lead us to conclude that the ascending volley, following electrical stimulation of a mixed peripheral nerve, produces the SP, without apparent contribution from the descending volley. The first 30 ms of the SP produced by supramaximal stimulation results from the collision of antidromic with orthodromic motor The next portion of the SP can best be seen by using submaximal stimulation, and corresponds to the segment from the H-reflex response (30 ms) to the end of the voluntary potentials that interrupt the SP (60 ms). This segment of the SP occurs too soon to be explicable on the basis of either cutaneous or possible descending volley e f f e c t ~ ,and ' ~ seems to be dependent on the ability of the antidromic motor volley to maximally activate Renshaw cell inhibition. The latter half of the SP can be attributed entirely to cutaneous afferent impulses which, in isolation, produce a complete SP between 70 and 120 ms after digital stimulation. With more proximal stimulation, these same cutaneous fibers are activated within the mixed nerve. Our calculations, and those of McClellan,' suggest that these afferent impulses are carried by slowly conducting fibers at a rate of 10 to 15 m/s. This explains the much greater latency shift of the SP end point with movement of the site of stimulation compared with the F-wave o r H-reflex response, which also result from the effects of the ascending volley, but are generated by impulses carried in faster conducting fibers. Previous theories implicating the superimposed electrically induced twitch and muscle spindle pause in the genesis of the SP must take into account that a SP can be elicited in the homonymous muscle from mixed nerve stimulation in absence of mechanical twitch. Furthermore, a complete SP can be obtained in the non-homonymous muscle in absence of the descending volley. Finally,
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nally, only the ascending volley theory adequately explains the contribution to the SP from cutaneous
effects, and the unequivocal shortening in the SP end point seen with more proximal stimulation.
REFERENCES
1. Angel RW, Eppler W, Iannone A: Silent period produced by unloading of muscle during voluntary contraction. J Physiol 1965;180:864-870. 2. Caccia MR, McComas AJ, Upton ARM, Blogg T: Cutaneous reflexes in small muscles of the hand. J Neurol Neurosurg Psychiatly 1973;36:960- 977. 3. Erlanger J, Gasser HS: The compound nature of the action current of nerve as disclosed by the cathode ray oscillograph. Am J Physiol 1924;70:624-666. 4. Higgins DC, Lieberman JS: The muscle silent period and spindle function in man. Electroenceph Clin Neurophysiol 1968;25:238-243. 5. Kimura J: H, T, masseter, and other reflexes, in Electrodiagnosis in Diseases of Nerue and Muscle: Principles and Practice, 2 ed. Philadelphia, FA Davis, 1989, pp 356-374. 6. Kranz H, Adorjani C, Baumgartner G: The effect of nociceptive cutaneous stimuli on human motoneurons. Brain 1973;96:57 1-590. 7. Matthews BHC: The response of a muscle spindle during active contraction of a muscle. J Physiol 1931;72:153- 174.
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The Silent Period
8. McLellan DL: The electromyographic silent period produced by supramaximal electrical stimulation in normal man. J Neurol Neurosurg Psychiatry 1973;36:334-341. 9. Merton PA: The silent period in a muscle of the human hand. JPhysiol 1951;114:183-198. 10. Miles TS, Le T H , Turker KS: Biphasic inhibitory responses and their IPSPs evoked by tibia1 nerve stimulation in human soleus motor neurones. Exp Brain Res 1989; 77~637-645. 1 1 . Ruffini A: On the minute anatomy of the neuromuscvlar spindles of the cat, and on their physiological significance. J Physiol 1898;23:190-208. 12. Ryall RW, Piercey MF, Polosa C, Goldfarb J: Excitation of Renshaw cells in relation to orthodromic and anti-dromic excitation of motorneurons. J Neurophysiol 1972;35:137148. 13. Shahani BT, Young RR: Studies of the normal human silent period, in Desmedt JE (ed): New Developments in Electromyography and Clinical Neurophysiology. Karger, Basel, 1973, vol 3, pp 589-602.
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