Electroencephalography and Clinical Neurophysiology, 1978, 4 5 : 3 3 1 - - 3 4 0
331
© Elsevier/North-Holland Scientific Publishers, Ltd.
EVOKED SPINAL CORD AND N E R V E R O O T POTENTIALS IN HUMANS USING A NON-INVASIVE R E C O R D I N G T E C H N I Q U E M.R. DIMITRIJEVIC 1, L.E. LARSSON 2, D. LEHMKUHL 3 and A. SHERWOOD 3
I Institute of Clinical Neurophysiology, University Hospital, Ljubljana (Yugoslavia); 2 Department of Clinical Neurophysiology, University Hospital, LinklJping (Sweden); 3 Department of Clinical Neurophysiology, TIRR and Department of Rehabilitation, Baylor College of Medicine, Houston, Texas (U.S.A.) (Accepted for publication: January 31, 1978)
In the quest to describe the functional status of the nervous system in conscious human subjects with non-invasive techniques, we recorded evoked potentials over the thoracic and l u m b a r spine using surface electrodes. We found that it is possible to distinguish responses in spinal roots from those generated in cord structures as readily as was done in earlier studies which used invasive techniques. Recordings of action potentials from the thoracolumbar subdural space evoked b y stimulation of the tibial nerve in humans were described b y Magladery et al. (1951a,b). They found propagated nerve action potentials from dorsal as well as ventral roots and, in addition, described a biphasic negativepositive potential which was recorded over the dorsal surface of the spinal cord. Other reports of successful recordings o f evoked spinal potentials in man include Ertekin (1973, 1976a,b), who used subdural recording techniques, Shimoji et al. (1971, 1972, 1973) and Caccia et al. (1976), w h o used epi. dural recording techniques, and Liberson et al. {1963, 1966), Cracco (1973) and Cracco et al. (1975), who used surface recording techniques. Delbeke et al. (1978) added to surface recording techniques the monitoring of H-reflex and direct m o t o r responses of triceps surae. We have used similar techniques to correlate reflex and direct muscle responses with corresponding spinal potentials and to
determine neurophysiological characteristics of evoked potentials recorded from lumbosacral portions of the spine.
Material and methods
Subjects Eighteen sets of measurements were collected from 13 subjects, 10 men and 3 women, ranging in age from 21 to 53 years. The measurements were made with the subjects lying in a supine position on a comfortable couch. They were asked to relax completely and, if possible, to go to sleep. Non-invasive procedures were used which presented little or no risk of injury to the subject. Electrical stimulation of peripheral nerves with surface electrodes caused little discomfort to most subjects and it was never necessary to discontinue stimulation during an experiment because of a complaint by a subject.
Recording Recording electrodes in the form of 4 cm × 0 . 5 c m chlorided (fine) silver strips were placed transversely over the spinous processes at the T~, T~2, L2, L4, and $1 vertebral levels and taped to the skin. When recording from the back with several distant reference electrode locations, little or no electrical activity was recorded at T6 as compared to other
332 spinal locations. Thus, T6 was used as the reference electrode, providing 'monopolar' signals from the other electrode positions. These signals were amplified 2 or 3 X 104 times using the negative potential-upward deflection EEG convention via an ElemaSchonander Mingograf. The bandwidth was initially adjusted for 6--2000 c/sec in the earlier experiments, and 60--2000 c/sec in the later experiments. Lead plate ground straps, 4 cm X 25 cm, were placed at mid thigh on each leg above the stimulating electrodes to reduce the stimulus artefact in the evoked potentials. Beckman recessed silver-silver chloride electrodes were placed over the triceps surae muscles to monitor the reflex electrical activity. Using Astrodata amplifiers with a bandwidth of 10--3000 c/sec, the activity was amplified from 100 to 1000 times. A total of 64 responses on 8 channels were averaged simultaneously, 4 each on an HP signal averager and on an Anops special purpose computer. The HP averager was set for 250 points per channel, sampled at 200/~sec per point, for a sweep time of 50 msec. The Anops, with twice the m e m o r y , was arranged to provide 500 points per channel, sampled at 80 psec intervals, for a sweep time of 40 msec. Using a special arithmetic function on the Anops, different sets of data could be compared by adding and subtracting the averaged responses. The display gain on both averagers was in the range of 1--32. The single evoked responses, together with timing and stimulus control signals, were recorded on a 14-channel FM magnetic tape recorder for subsequent processing.
Stimulation The tibial nerves were stimulated on one or both sides. The cathode was a lead disc (2 cm diameter) placed over the tibial nerve trunk in the popliteal fossa and the anode was a lead plate (8 cm X 8 cm) placed over the patella. A constant voltage stimulator, with stimulus isolation units, provided stimulus pulses of 1 msec to 100 ttsec duration. The stimulator, triggered externally, was operated so as to
M.R. DIMITRIJEVIC ET AL. deliver single pulses, simultaneous pulses in both channels, simultaneous pulse pairs in each channel (or pulse pairs in one channel), or an adjustable delay between the pulses from each channel. The stimulus was delivered during the quiescent phase of the ECG by delaying the ECG-derived trigger signal 300--900 msec after the QRS complex. Care was taken to insure that changes in the heart rate did not cause the P-wave to overlap the response averaging window. Repeated control trials with the stimulus off showed that there was no averaged activity related to the cardiac cycle present in the output.
Results
Description o f evoked responses An example of the evoked electrical potentials recorded over the spine at lower thoracic and lumbosacral levels is shown in Fig. 1. This recording was produced by unilateral (Fig. 1A right; Fig. 1B left), then by bilateral (Fig. 1C), stimulation of the tibial nerve(s) with sufficient intensity to elicit a maximum direct muscle response (M-wave) as recorded by surface EMG electrodes placed over the triceps surae muscles on both sides. The responses obtained in Fig. 1C after bilateral stimulation are equal to the sum of both unilateral responses. Thus, there is little or no interference between those processes which generate the unilateral responses separately. Using the bilateral nerve stimulation method, the peak-to-peak amplitude ranged from 1 to 10 #V. Two distinctive types of responses were found. At the TL2 level, the responses are smooth, predominantly negative waves, each ending with a long lasting positive deflection. Using Magladery's terminology, this wave has been labeled S (spinal cord response). At the L4 and S~ levels, the responses are double peaked with a d o m i n a n t early negative wave. In conformity with Magladery et al. (1951a), the early wave has been labeled R (dorsal root response) and the late negative deflec-
EVOKED SPINAL CORD AND NERVE ROOT POTENTIALS IN HUMANS
>
A
,
333
B ,
Fig. 1. Surface recording of evoked activity over the spine at T12, L2, L4 and 81 vertebral levels. This figure shows the evoked spinal responses to right (A), left (B) and bilateral (C) tibial nerve stimulation at the popliteal fossae. The S, R and A waves are identified in part C. On the right is a diagram o f the lower spine and pelvis. The shaded areas indicate the location of recording electrodes. The stimulus strength was adjusted to elicit a maximal direct motor response in each triceps surae muscle as recorded by surface EMG electrodes. All traces are the average of 64 responses.
tion labeled A (anterior root response). We found the present technique suitable for eliciting demonstrable spinal responses in each subject tested, and the responses were reproducible when performing repeated trials on the same subject. There were minor variations in shape of the evoked potentials between different subjects; the main variation was that the transition from the double peak response to the single peak occurred at slightly different levels of the spine. The diagram included in Fig. 1 illustrates the relationships between the various structures in the spinal canal and the electrical activity obtained in our recordings; the S-wave is recorded over the lower end of the spinal cord while the R- and A-waves are recorded over the cauda equina. The average latency for the early negative wave at the S~ vertebral level was 8.8 + 1.0 msec. This gives a c o m p u t e d conduction velocity for the fastest afferent fibers of 64 + 6 m/sec. A summary of the latencies is presented in Table I. In the table it is seen that the onset latencies are prolonged with more rostral recording.
Increasing stimulus strength The traces in Fig. 2 illustrate the effects of bilateral tibial nerve stimulation at gradually increasing stimulus strength. The H-reflex and direct m o t o r responses to stimulation are shown in the EMG traces from the triceps surae muscles to the right in the figure. When the stimulus is at the threshold for the H-reflex (Fig. 2A) a slight S-wave is seen at the T12 level. Increasing the strength of the stimulus further (Fig. 2B and C) produced a distinct M-response in the EMG recording and a well-defined R-wave in the spinal recording {Fig. 2C). These responses both grew larger when the stimulus was increased even more {Fig. 2D). Note t h a t when such a strong stimulus is applied the H-reflex and spinal A wave responses are abolished. It can also be seen in Fig. 2 t h a t with increasing stimulus strength a response (S-wave) appeared first in leads over the spinal cord. Further increases in stimulus strength elicited an R-wave in leads over the cauda equina. Plotting the relationship between the amplitude of the R-wave and
334
M.R. DIMITRIJEVIC ET AL.
TABLE I Average latencies of the spinal evoked responses following bilateral tibial nerve stimulation at the popliteal fossa (in msec) (8 subjects). The duration of the positive phase of the S-wave is approximately double that of the negative.
RA 4~
Vertebrae
R onset
R peak
A onset
A peak
A end
S1 L4 L2 **
8.8 ± 1.0 * 9.4 ± 0.9 9.9 ± 1.0
10.7 ± 0.9 11.4 ± 0.9 12.0 ± 1.2
12.7 ± 1.1 13.0 ± 1.2 13.2 ± 1.1
14.7 ± 0.9 14.6 ~ 1.2 14.5 ± 1.2
16.7 ± 0.7 17.1 -+ 1.0 17.6 ± 1.3
S
Vertebrae
S onset
S peak
End of negative phase
T12
10.8 ± 1.1
14.4 -+ 1.3
18.0 ± 1.5
* Mean ± S.D. ** Data for the A-wave at L2 were compiled for only 7 subjects. t h a t o f t h e S - w a v e as a f u n c t i o n o f s t i m u l u s s t r e n g t h r e v e a l e d t h a t t h i s r e l a t i o n s h i p is n o t linear (Fig, 3A). On the other hand, the r e l a t i o n s h i p b e t w e e n t h e a m p l i t u d e s o f t h e Ma n d t h e R - w a v e s was f o u n d t o be l i n e a r ( F i g . 3B).
The relationship between the S-wave and the H-reflex response
C
Fig. 2. Spinal responses (left) and EMG responses (right) to increasing stimulus strength. Stimuli were applied to the tibial nerve bilaterally at the popliteal fossae. The increasing strength is indicated by the
T h e e x p e r i m e n t o f Fig. 2 i n d i c a t e s a possible r e l a t i o n s h i p b e t w e e n the S-wave a n d the H-reflex since they appear at the same stimul u s s t r e n g t h . T h i s r e l a t i o n is s h o w n i n t h e d i a g r a m o f Fig. 4. W h e n t h e p o i n t s o b t a i n e d a t m a x i m a l s t i m u l u s s t r e n g t h are e x c l u d e d , t h e d a t a c a n b e f i t t e d w i t h a s t r a i g h t l i n e , suggesting a direct relationship between the two r e s p o n s e s . T h e H - r e f l e x is a n i n d e x o f m o t o EMG responses from the triceps surae muscles in the right column. The H-reflex response appears as the late wave and the direct muscle response (M:wave) appears early in the EMG traces. Due to the high amplification the H-wave is distorted in C and the M-wave in D.
335
EVOKED SPINAL CORD AND NERVE ROOT POTENTIALS IN HUMANS
H
S,
A
?
100
100
50
50
iJ
B
100'
o
go
loo
Fig. 4. H- and S-wave amplitude relationship. The graph shows the normalized relationship between the evoked spinal S-wave amplitude and the EMG H-reflex response. Varying strengths of stimulation were applied simultaneously to the tibial nerves (bilaterally) at the popliteal fossae. The H-reflex amplitude is the average of amplitudes from the two legs.
Influence o f conditioning stimuli on S- and R-wave responses
o
s'o
10o
Fig. 3. Amplitude relations at increasing stimulus strength. The graph shows the relationship of the normalized amplitudes of (A) the R- and S-waves of the spinal responses and (B) the R-wave of the spinal response and the EMG M-wave response of the triceps surae muscles. Varying strengths of stimulation were applied simultaneously to the tibial nerves (bilaterally) at the popliteal fossae. The S-wave was measured on the ascending phase. The M-wave amplitude is the average of the amplitudes from the two legs. n e u r o n a c t i v i t y as l o n g as it is n o t o c c l u d e d by antidromic activity associated with the direct motor response. Thus the relationship b e t w e e n t h e s e S-wave a n d H - r e f l e x r e s p o n s e s is m e a n i n g f u l o n l y to t h e p o i n t t h a t t h e H-reflex r e s p o n s e is o c c l u d e d . T h e a m p l i t u d e o f the S-wave does, h o w e v e r , c o n t i n u e to increase w i t h increased s t i m u l u s s t r e n g t h a f t e r occlusion of the H-reflex response.
H a v i n g f o u n d e v i d e n c e t h a t t h e S-wave m a y r e p r e s e n t activity u n d e r s y n a p t i c i n f l u e n c e (e.g., t h e linear r e l a t i o n b e t w e e n t h e H-reflex a n d t h e S-wave a n d t h e n o n - l i n e a r r e l a t i o n b e t w e e n t h e R- a n d S-waves), we t e s t e d t h e effects on the responses of supramaximal d o u b l e s t i m u l a t i o n t o t h e tibial nerves (Fig. 5). T h e s e c o n d s t i m u l u s was a p p l i e d a t successively longer intervals a f t e r t h e condit i o n i n g stimulus, w i t h i n t e r s t i m u l u s intervals ranging b e t w e e n 1 a n d 20 m s e c . T h e c o n t r o l r e s p o n s e s t o single stimuli are s h o w n at t h e top above the net responses to the second stimulus. T h e s e n e t r e s p o n s e s w e r e o b t a i n e d by subtracting the control responses from the c o m p o s i t e r e s p o n s e s t o t h e d o u b l e stimulat i o n . I t is seen t h a t an S-wave r e s p o n s e to t h e s e c o n d s t i m u l u s was elicited at an i n t e r - s t i m u lus interval o f 3 m s e c a n d t h e n r e m a i n e d c o m p a r a t i v e l y c o n s t a n t . In o t h e r e x p e r i m e n t s t h e d e p r e s s i o n lasted a p p r o x i m a t e l y 5 m s e c . A
336
M.R. DIMITRIJEVIC ET AL.
S
-,-.~./~
~,......~/~
~
R
CONTROL ~ , , ~
~'~
2mS
8mS lOmS 15mS T12
20mS
Fig. 5. R- and S-wave recovery from conditioning stimulation. Double stimuli were delivered at the interval indicated in the center of the figure: .The responses shown are obtained by subtracting the control responses to single stimuli (shown at the top) from the responses to the double stimuli.
faint R-wave appeared as early as 1 msec and appeared to be facilitated after 3 msec. T h e A - w a v e responses T h e second wave of the double peaked response recorded at $1 and L4 levels of the spine is called the A-wave. The latency of the peak of this response appr oxi m at el y corresponds to the latency of the peak of the S-wave {Figs. 1 and 2), but its amplitude tends to be smaller than that of the S-wave. Fig. 2B illustrates that the second of the two peaks (A-wave) appeared alone at the L4 level when the stimulus intensity was adjusted to elicit a well
331
© Elsevier/North-Holland Scientific Publishers, Ltd.
EVOKED SPINAL CORD AND N E R V E R O O T POTENTIALS IN HUMANS USING A NON-INVASIVE R E C O R D I N G T E C H N I Q U E M.R. DIMITRIJEVIC 1, L.E. LARSSON 2, D. LEHMKUHL 3 and A. SHERWOOD 3
I Institute of Clinical Neurophysiology, University Hospital, Ljubljana (Yugoslavia); 2 Department of Clinical Neurophysiology, University Hospital, LinklJping (Sweden); 3 Department of Clinical Neurophysiology, TIRR and Department of Rehabilitation, Baylor College of Medicine, Houston, Texas (U.S.A.) (Accepted for publication: January 31, 1978)
In the quest to describe the functional status of the nervous system in conscious human subjects with non-invasive techniques, we recorded evoked potentials over the thoracic and l u m b a r spine using surface electrodes. We found that it is possible to distinguish responses in spinal roots from those generated in cord structures as readily as was done in earlier studies which used invasive techniques. Recordings of action potentials from the thoracolumbar subdural space evoked b y stimulation of the tibial nerve in humans were described b y Magladery et al. (1951a,b). They found propagated nerve action potentials from dorsal as well as ventral roots and, in addition, described a biphasic negativepositive potential which was recorded over the dorsal surface of the spinal cord. Other reports of successful recordings o f evoked spinal potentials in man include Ertekin (1973, 1976a,b), who used subdural recording techniques, Shimoji et al. (1971, 1972, 1973) and Caccia et al. (1976), w h o used epi. dural recording techniques, and Liberson et al. {1963, 1966), Cracco (1973) and Cracco et al. (1975), who used surface recording techniques. Delbeke et al. (1978) added to surface recording techniques the monitoring of H-reflex and direct m o t o r responses of triceps surae. We have used similar techniques to correlate reflex and direct muscle responses with corresponding spinal potentials and to
determine neurophysiological characteristics of evoked potentials recorded from lumbosacral portions of the spine.
Material and methods
Subjects Eighteen sets of measurements were collected from 13 subjects, 10 men and 3 women, ranging in age from 21 to 53 years. The measurements were made with the subjects lying in a supine position on a comfortable couch. They were asked to relax completely and, if possible, to go to sleep. Non-invasive procedures were used which presented little or no risk of injury to the subject. Electrical stimulation of peripheral nerves with surface electrodes caused little discomfort to most subjects and it was never necessary to discontinue stimulation during an experiment because of a complaint by a subject.
Recording Recording electrodes in the form of 4 cm × 0 . 5 c m chlorided (fine) silver strips were placed transversely over the spinous processes at the T~, T~2, L2, L4, and $1 vertebral levels and taped to the skin. When recording from the back with several distant reference electrode locations, little or no electrical activity was recorded at T6 as compared to other
332 spinal locations. Thus, T6 was used as the reference electrode, providing 'monopolar' signals from the other electrode positions. These signals were amplified 2 or 3 X 104 times using the negative potential-upward deflection EEG convention via an ElemaSchonander Mingograf. The bandwidth was initially adjusted for 6--2000 c/sec in the earlier experiments, and 60--2000 c/sec in the later experiments. Lead plate ground straps, 4 cm X 25 cm, were placed at mid thigh on each leg above the stimulating electrodes to reduce the stimulus artefact in the evoked potentials. Beckman recessed silver-silver chloride electrodes were placed over the triceps surae muscles to monitor the reflex electrical activity. Using Astrodata amplifiers with a bandwidth of 10--3000 c/sec, the activity was amplified from 100 to 1000 times. A total of 64 responses on 8 channels were averaged simultaneously, 4 each on an HP signal averager and on an Anops special purpose computer. The HP averager was set for 250 points per channel, sampled at 200/~sec per point, for a sweep time of 50 msec. The Anops, with twice the m e m o r y , was arranged to provide 500 points per channel, sampled at 80 psec intervals, for a sweep time of 40 msec. Using a special arithmetic function on the Anops, different sets of data could be compared by adding and subtracting the averaged responses. The display gain on both averagers was in the range of 1--32. The single evoked responses, together with timing and stimulus control signals, were recorded on a 14-channel FM magnetic tape recorder for subsequent processing.
Stimulation The tibial nerves were stimulated on one or both sides. The cathode was a lead disc (2 cm diameter) placed over the tibial nerve trunk in the popliteal fossa and the anode was a lead plate (8 cm X 8 cm) placed over the patella. A constant voltage stimulator, with stimulus isolation units, provided stimulus pulses of 1 msec to 100 ttsec duration. The stimulator, triggered externally, was operated so as to
M.R. DIMITRIJEVIC ET AL. deliver single pulses, simultaneous pulses in both channels, simultaneous pulse pairs in each channel (or pulse pairs in one channel), or an adjustable delay between the pulses from each channel. The stimulus was delivered during the quiescent phase of the ECG by delaying the ECG-derived trigger signal 300--900 msec after the QRS complex. Care was taken to insure that changes in the heart rate did not cause the P-wave to overlap the response averaging window. Repeated control trials with the stimulus off showed that there was no averaged activity related to the cardiac cycle present in the output.
Results
Description o f evoked responses An example of the evoked electrical potentials recorded over the spine at lower thoracic and lumbosacral levels is shown in Fig. 1. This recording was produced by unilateral (Fig. 1A right; Fig. 1B left), then by bilateral (Fig. 1C), stimulation of the tibial nerve(s) with sufficient intensity to elicit a maximum direct muscle response (M-wave) as recorded by surface EMG electrodes placed over the triceps surae muscles on both sides. The responses obtained in Fig. 1C after bilateral stimulation are equal to the sum of both unilateral responses. Thus, there is little or no interference between those processes which generate the unilateral responses separately. Using the bilateral nerve stimulation method, the peak-to-peak amplitude ranged from 1 to 10 #V. Two distinctive types of responses were found. At the TL2 level, the responses are smooth, predominantly negative waves, each ending with a long lasting positive deflection. Using Magladery's terminology, this wave has been labeled S (spinal cord response). At the L4 and S~ levels, the responses are double peaked with a d o m i n a n t early negative wave. In conformity with Magladery et al. (1951a), the early wave has been labeled R (dorsal root response) and the late negative deflec-
EVOKED SPINAL CORD AND NERVE ROOT POTENTIALS IN HUMANS
>
A
,
333
B ,
Fig. 1. Surface recording of evoked activity over the spine at T12, L2, L4 and 81 vertebral levels. This figure shows the evoked spinal responses to right (A), left (B) and bilateral (C) tibial nerve stimulation at the popliteal fossae. The S, R and A waves are identified in part C. On the right is a diagram o f the lower spine and pelvis. The shaded areas indicate the location of recording electrodes. The stimulus strength was adjusted to elicit a maximal direct motor response in each triceps surae muscle as recorded by surface EMG electrodes. All traces are the average of 64 responses.
tion labeled A (anterior root response). We found the present technique suitable for eliciting demonstrable spinal responses in each subject tested, and the responses were reproducible when performing repeated trials on the same subject. There were minor variations in shape of the evoked potentials between different subjects; the main variation was that the transition from the double peak response to the single peak occurred at slightly different levels of the spine. The diagram included in Fig. 1 illustrates the relationships between the various structures in the spinal canal and the electrical activity obtained in our recordings; the S-wave is recorded over the lower end of the spinal cord while the R- and A-waves are recorded over the cauda equina. The average latency for the early negative wave at the S~ vertebral level was 8.8 + 1.0 msec. This gives a c o m p u t e d conduction velocity for the fastest afferent fibers of 64 + 6 m/sec. A summary of the latencies is presented in Table I. In the table it is seen that the onset latencies are prolonged with more rostral recording.
Increasing stimulus strength The traces in Fig. 2 illustrate the effects of bilateral tibial nerve stimulation at gradually increasing stimulus strength. The H-reflex and direct m o t o r responses to stimulation are shown in the EMG traces from the triceps surae muscles to the right in the figure. When the stimulus is at the threshold for the H-reflex (Fig. 2A) a slight S-wave is seen at the T12 level. Increasing the strength of the stimulus further (Fig. 2B and C) produced a distinct M-response in the EMG recording and a well-defined R-wave in the spinal recording {Fig. 2C). These responses both grew larger when the stimulus was increased even more {Fig. 2D). Note t h a t when such a strong stimulus is applied the H-reflex and spinal A wave responses are abolished. It can also be seen in Fig. 2 t h a t with increasing stimulus strength a response (S-wave) appeared first in leads over the spinal cord. Further increases in stimulus strength elicited an R-wave in leads over the cauda equina. Plotting the relationship between the amplitude of the R-wave and
334
M.R. DIMITRIJEVIC ET AL.
TABLE I Average latencies of the spinal evoked responses following bilateral tibial nerve stimulation at the popliteal fossa (in msec) (8 subjects). The duration of the positive phase of the S-wave is approximately double that of the negative.
RA 4~
Vertebrae
R onset
R peak
A onset
A peak
A end
S1 L4 L2 **
8.8 ± 1.0 * 9.4 ± 0.9 9.9 ± 1.0
10.7 ± 0.9 11.4 ± 0.9 12.0 ± 1.2
12.7 ± 1.1 13.0 ± 1.2 13.2 ± 1.1
14.7 ± 0.9 14.6 ~ 1.2 14.5 ± 1.2
16.7 ± 0.7 17.1 -+ 1.0 17.6 ± 1.3
S
Vertebrae
S onset
S peak
End of negative phase
T12
10.8 ± 1.1
14.4 -+ 1.3
18.0 ± 1.5
* Mean ± S.D. ** Data for the A-wave at L2 were compiled for only 7 subjects. t h a t o f t h e S - w a v e as a f u n c t i o n o f s t i m u l u s s t r e n g t h r e v e a l e d t h a t t h i s r e l a t i o n s h i p is n o t linear (Fig, 3A). On the other hand, the r e l a t i o n s h i p b e t w e e n t h e a m p l i t u d e s o f t h e Ma n d t h e R - w a v e s was f o u n d t o be l i n e a r ( F i g . 3B).
The relationship between the S-wave and the H-reflex response
C
Fig. 2. Spinal responses (left) and EMG responses (right) to increasing stimulus strength. Stimuli were applied to the tibial nerve bilaterally at the popliteal fossae. The increasing strength is indicated by the
T h e e x p e r i m e n t o f Fig. 2 i n d i c a t e s a possible r e l a t i o n s h i p b e t w e e n the S-wave a n d the H-reflex since they appear at the same stimul u s s t r e n g t h . T h i s r e l a t i o n is s h o w n i n t h e d i a g r a m o f Fig. 4. W h e n t h e p o i n t s o b t a i n e d a t m a x i m a l s t i m u l u s s t r e n g t h are e x c l u d e d , t h e d a t a c a n b e f i t t e d w i t h a s t r a i g h t l i n e , suggesting a direct relationship between the two r e s p o n s e s . T h e H - r e f l e x is a n i n d e x o f m o t o EMG responses from the triceps surae muscles in the right column. The H-reflex response appears as the late wave and the direct muscle response (M:wave) appears early in the EMG traces. Due to the high amplification the H-wave is distorted in C and the M-wave in D.
335
EVOKED SPINAL CORD AND NERVE ROOT POTENTIALS IN HUMANS
H
S,
A
?
100
100
50
50
iJ
B
100'
o
go
loo
Fig. 4. H- and S-wave amplitude relationship. The graph shows the normalized relationship between the evoked spinal S-wave amplitude and the EMG H-reflex response. Varying strengths of stimulation were applied simultaneously to the tibial nerves (bilaterally) at the popliteal fossae. The H-reflex amplitude is the average of amplitudes from the two legs.
Influence o f conditioning stimuli on S- and R-wave responses
o
s'o
10o
Fig. 3. Amplitude relations at increasing stimulus strength. The graph shows the relationship of the normalized amplitudes of (A) the R- and S-waves of the spinal responses and (B) the R-wave of the spinal response and the EMG M-wave response of the triceps surae muscles. Varying strengths of stimulation were applied simultaneously to the tibial nerves (bilaterally) at the popliteal fossae. The S-wave was measured on the ascending phase. The M-wave amplitude is the average of the amplitudes from the two legs. n e u r o n a c t i v i t y as l o n g as it is n o t o c c l u d e d by antidromic activity associated with the direct motor response. Thus the relationship b e t w e e n t h e s e S-wave a n d H - r e f l e x r e s p o n s e s is m e a n i n g f u l o n l y to t h e p o i n t t h a t t h e H-reflex r e s p o n s e is o c c l u d e d . T h e a m p l i t u d e o f the S-wave does, h o w e v e r , c o n t i n u e to increase w i t h increased s t i m u l u s s t r e n g t h a f t e r occlusion of the H-reflex response.
H a v i n g f o u n d e v i d e n c e t h a t t h e S-wave m a y r e p r e s e n t activity u n d e r s y n a p t i c i n f l u e n c e (e.g., t h e linear r e l a t i o n b e t w e e n t h e H-reflex a n d t h e S-wave a n d t h e n o n - l i n e a r r e l a t i o n b e t w e e n t h e R- a n d S-waves), we t e s t e d t h e effects on the responses of supramaximal d o u b l e s t i m u l a t i o n t o t h e tibial nerves (Fig. 5). T h e s e c o n d s t i m u l u s was a p p l i e d a t successively longer intervals a f t e r t h e condit i o n i n g stimulus, w i t h i n t e r s t i m u l u s intervals ranging b e t w e e n 1 a n d 20 m s e c . T h e c o n t r o l r e s p o n s e s t o single stimuli are s h o w n at t h e top above the net responses to the second stimulus. T h e s e n e t r e s p o n s e s w e r e o b t a i n e d by subtracting the control responses from the c o m p o s i t e r e s p o n s e s t o t h e d o u b l e stimulat i o n . I t is seen t h a t an S-wave r e s p o n s e to t h e s e c o n d s t i m u l u s was elicited at an i n t e r - s t i m u lus interval o f 3 m s e c a n d t h e n r e m a i n e d c o m p a r a t i v e l y c o n s t a n t . In o t h e r e x p e r i m e n t s t h e d e p r e s s i o n lasted a p p r o x i m a t e l y 5 m s e c . A
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Fig. 5. R- and S-wave recovery from conditioning stimulation. Double stimuli were delivered at the interval indicated in the center of the figure: .The responses shown are obtained by subtracting the control responses to single stimuli (shown at the top) from the responses to the double stimuli.
faint R-wave appeared as early as 1 msec and appeared to be facilitated after 3 msec. T h e A - w a v e responses T h e second wave of the double peaked response recorded at $1 and L4 levels of the spine is called the A-wave. The latency of the peak of this response appr oxi m at el y corresponds to the latency of the peak of the S-wave {Figs. 1 and 2), but its amplitude tends to be smaller than that of the S-wave. Fig. 2B illustrates that the second of the two peaks (A-wave) appeared alone at the L4 level when the stimulus intensity was adjusted to elicit a well
