Nerve conduction studies are of great clinical value in diagnosing nerve pathology and injury. In most neurophysiological laboratories nerve conduction recordings are routinely made with surface bipolar electrodes. More rarely, needle electrodes are used. A bipolarly recorded nerve action potential (NAP) is the difference between 2 unipolar NAPs recorded from each pole of a bipolar electrode and a remote reference. The delay between the 2 separated unipolar NAPs depends on the distance between the poles and the conduction velocity (CV). When the delay between the unipolar NAPs was increased (partly through simulation), the following changes of the bipolar NAP occurred: (1) total amplitude was maximal at a certain delay but decreased if the delay was shorter or longer, (2) latencies of the first positive and the first negative peaks increased slightly until their amplitudes reached maximal values, (3) a second negative peak of increasing latency appeared with longer delays, (4) latencies of later peaks increased linearly, and (5) total area increased nonlinearly. All parameters of the bipolarly recorded NAP (except the onset of the first positive phase) changed with increasing delay. The significance of this is that if NAPs are recorded with a bipolar electrode, standard values obtained for each nerve cannot be transferred between laboratories if different interelectrode (interpolar) distances are used. Furthermore, the assumption that a fixed interelectrode distance allows comparisons between reference values and patient data is incorrect. Key words: nerve action potentials neurography bipolar recording unipolar recording phase cancellation MUSCLE 81 NERVE 14:133-141 1991
UNI= AND BIPOLAR SURFACE RECORDING OF HUMAN NERVE RESPONSES TOMAS WINKLER, MD, ERIK STALBERG, MD, PhD, and LINDSAY F. HAAS, MB, ChB, BMedSc, FRACP
Nerve conduction studies are of major importance in diagnosing focal and generalized diseases of nerves. For motor nerves, measurements of the muscle response latency and amplitude are usually used. For sensory and mixed nerve studies the nerve action potential (NAP) is recorded. Latency, amplitude, duration, and shape of the NAPS are measured to calculate nerve conduction velocity (CV), and indicate number of conducting axons,
From the Department of Clinical Neurophysiology. University Hospital, Uppsala, Sweden. Acknowledgment: This study was in part supported by the Swedish Medical Research Council (Grant 135, ES). Presented in part at the Forty-Sixth Annual Meeting of the Swedish Society of Clinical Neurophysiology, Stockholm, Sweden, December 1988. Address reprint requests to T Winkler. Department of Clinical Neurophysiology, University Hospital, S-751 85 Uppsala. Sweden. Accepted January 20, 1990 CCC 0148-639X/91/020133-09 $04.00 0 1991 John Wiley & Sons, Inc.
Uni- and Bipolar Recording
and their temporal dispersion. In most neurophysiological laboratories NAPS are recorded with bipolar surface electrodes placed along the nerve trunk. This method is noninvasive, easy to perform, and relatively free from artifacts. Less commonly, needle electrodes are used. T o interpret the factors determining the shape of the NAP, the factors contributing to it must be known. Major factors discussed in literature are: number of axons, axon diameter^,'^ density of axons in the nerve, distribution of axonal conduction v e l ~ c i t i e s , distance ~’~ between recording electrode and n e r ~ e , ~ ” stimulus ~’” strength, temperature of tissue and nerve,”12 polarity of stimulating electrodes, 14,15 filter settings in the recording equipment, and configuration of the recording electrode. The last factor has been carefully investigated by Buchthal and Rosenfalck.‘ They recorded the sensory NAPS from the median nerve at wrist and elbow with needle electrodes following digital stimulation. With bipolar recordings their main findings were:
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1. The bipolar NAP is the difference between 2 unipolarly recorded NAPs, slightly displaced in time. 2. Amplitude, duration, and shape of the bipolar NAP depend on distance between the poles of the recording electrode and CV. 3. Maximal amplitude is obtained when the time interval between the unipolar NAPs is such that the negative peak of the earlier unipolar NAP coincide with the positive peak of the latter. 4. The latency to the onset of the initial positive phase is determined by the unipolar NAP recorded by the electrode pole closest to the stimulus site. The importance of the distance between the poles of the recording bipolar electrode is often overlooked, and if ring or silver cup electrodes are used without any corrections for variations of interelectrode distances, errors will result. The aim of this study is to further investigate the effect on the bipolar NAP of different time delays (ie, the time taken for the NAP to travel between the two poles of the recording bipolar electrode) and variations of the shape of the corresponding unipolar NAPs.
METHODS
These were performed on 4 healthy volunteers aged 25 to 5 1 years. ‘Their median nerves were stimulated supramaximally at the wrist with short square pulses (duration 0.1 msec) at a frequency of 1 Hz. Bipolar recordings were made with a standard surface felt pad electrode (Dantec 9013 L, interpole distance 23 mm) placed over the nerve proximal to the elbow. Unipolar NAPs from one or the other of the pads of the bipolar electrode were obtained using a felt pad electrode (diameter 8 mm) as reference, placed on the lateral side of the arm at the same level as the bipolar electrode. The distance to the reference electrode was large enough to prevent signals from the nerve to be recorded by the reference. Recordings were made on a routine EMG equipment (Medelec MS 90, Mystro) with filter settings 2 Hz to 10 kHz. Sixty responses were averaged for each trace. Measurements of NAPs were made after manual setting of cursors. Amplitudes were measured between maximal positive and maximal negative peaks. Durations of bipolar NAPs were measured between the first and last positive peak, and total area from the onset of the Median Nerve Recordings.
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first positive to the end of the last positive or negative phase.
A unipolar NAP recorded between the distal pad of the bipolar electrode and the reference was stored in the computer as template for simulation of bipolar recordings. This template was kept at a constant latency, then a succession of identical templates were delayed relative to the first in increasing steps of 0.1 msec from 0.1 to 2.4 msec. By subtracting each successive delayed template from the first a series of simulated bipolar NAPs with increasing delays between the corresponding unipolar NAPs were obtained.
Simulation.
In another series, the technique was used to simulate bipolar NAPs in different clinical situations. This was performed by changing the delay between the templates, and/or amplitude of and/or rise-time of the templates (rise-time defined as latency between positive and negative peaks of the template). For each of 4 conditions bipolar NAPs obtained with 2 different electrodes with interelectrode distances 17 and 45 mm (Fig. 1) were simulated, respectively. The conditions to be simulated are normality (Fig. lA), primary sensory axonal degeneration (Fig. 1B), nerve entrapment (Fig. IC), and polyneuropathy (Fig. ID). Figure 1(A). “Normal” delay (calculated for the two interelectrode distances) is 0.3 msec and 0.8 msec resp. if CV = 56 m/s. If this delay is 100% for the 17-mm electrode, the delay for the 45-mm electrode will be 265%; the “normal” amplitude is set to 100% and “normal” rise-time is also set to 100% of the templates. Figure I(B). Doubled delay (200% and 5304 for the 17- and 45-mm electrodes respectively, CV = 28 mis), decreased amplitude (84%), and normal rise-time (100%) of the templates. Figure I(C). Normal delay (ie, 100% and 265% respectively, CV = 56 m/s), normal amplitude (loo%), and doubled rise-time (200%) of the templates. Figure I(D). Doubled delay (ie, 200 and 530% respectively, CV = 28 m/s), decreased amplitude (84%), and doubled rise-time (200%) of the templates.
Simulation of Clinical Situations.
To validate the simulations, the median nerves in 2 volunteers were stimulated at the wrist. Bipolar recordings were obtained
Clinical Comparison.
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A
B
C
D
FIGURE 1. Bipolar recordings may be altered in different clinical situations. Bipolar recorded NAPs are simulated with interelectrode distances of 17 (trace 3) and 45 mm (trace 6). The corresponding unipolar NAPs are shown above each bipolar NAP respectively (trace 1-2 = 3 and trace 4-5 = 6). (A) Normal conditions. Delay between unipolar NAPs, duration of bipolar NAP for the 17-mm electrode, amplitude and rise-time of unipolar NAPs are all set to 100% and later used as references. Delay for the 45-mm electrode is here 265% and amplitudes of bipolar NAPs are 106% and 156%, respectively. (6)Primary axonal degeneration of sensory fibers may give a loss of fast axons = decrease of CV = increased delay (200% and 530%, respectively, are used). A decrease of the unipolar amplitude is also simulated (amplitude of unipolar NAPs is here 84%). Due to favorable or unfavorable summation effects, the amplitude of the bipolar NAPs is increased for 17 mm (129%) but decreased and biphasic for 45 mm (112%), respectively,compared with (A) (106% and 156%, respectively).(C) Local entrapment between stimulating and recording electrodes may give a dispersion of action potentials [rise-timeof unipolar NAP is here 200% compared with (A)] while CV (delay) and amplitude of unipolar NAPs are unchanged. The amplitudes of the bipolar NAPs are decreased (59% and 129%, respectively) compared with (A) (106% and 156%, respectively). Thus, the decrease of bipolar amplitudes does not reflect any loss of axons. If a decrease of amplitude of unipolar NAPs is also simulated (not shown here) amplitudes of bipolar NAPs would be even smaller. (D) An axonal and demyelinating neuropathy gives decrease of CV = increase in delay (here 200% and 530%, respectively),dispersion = increase in rise-time (here 200%) and a loss of axons = drop in amplitude of unipolar NAP (here 84%). Due to various summation effects the amplitudes of the bipolar NAPs (91% and 135%, respectively) are slightly decreased compared to (A) (106% and 156%, respectively).Compared to (C) (59% and 129%, respectively) they are increased and unchanged respectively. The durations of the bipolar NAPs show an increase from (A) to (D): loo%, 113%, 200%, and 206% for the 17-mm interelectrode separation and 31%, 194%, 206%, and 256% for the 45-mm electrode separation, respectively.
with ring electrodes at increasing interelectrode distances at the third digit.
3. RESULTS
When two recorded unipolar NAPs were subtracted, the constructed bipolar NAP was identical to the directly recorded bipolar NAP (Fig. 2) showing that the simulations were valid. Relation Between Uni- and Bipolar NAPs.
4.
Simulation of Bipolar NAPs With Increasing Delay Between Its Two Templates. As the delay be-
tween the two templates increased, the configuration of the constructed bipolar NAP showed the following characteristics (Figs. 3, 4 and 5 ) : 1. The latency to the onset of the first positive peak was unchanged. 2. The latency of the first positive peak increased slightly until its amplitude reached the maximal
Uni- and Bipolar Recording
5.
6.
value (equal to the maximal positive amplitude of the first template). The latency of the negative peak first increased. After a certain delay the peak was divided into two peaks. Following this only the second peak showed any major changes in latency. The amplitude of the negative peak increased until the peak divided. After this, the amplitudes of the 2 negative peaks decreased to minimum levels that were equal to the maximal negative amplitude of the first template and the maximal positive amplitude of the second template respectively. The amplitude of the last positive peak increased to a maximal value which was equal to the maximal negative amplitude of the second template. The total amplitude increased rapidly to a
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A dist
prox
FIGURE 2. Recordings (A) and recording setups (B) showing various combinations of signal derivations. Numbers in A and B correspond. Distal unipolar NAP ( l ) , proximal unipolar NAP (2), and bipolar NAP (3) from a median nerve recorded between each of the poles and a remote reference (1, 2) or between the poles (3) of a bipolar electrode placed at the elbow. Wrist stimulation. Trace (4) shows the subtraction of (2) from (1). This difference is equal to the recorded bipolar response (3); (3) and (4) are superimposed in (5). Differences in peak latencies and amplitudes between uni- and bipolarly recorded NAPs are demonstrated in (6).
maximum when the negative peak of the first and the positive peak of the second template coincided (here for a delay of 0.8 msec). 7 The duration between the first and last positive peaks increased only slightly for short delays (here for delays less than 0.5 msec) but linearly for longer delays (here for delays exceeding 0.8 msec; Fig. 4B). 8. The total area increased nonlinearly.
Recording of Bipolar NAPs With Increasing Interelec. trode Distance. The variation of bipolarly re-
corded NAPS when using various distances between the recording ring electrodes (Fig. 6), followed the same pattern as in the simulations already described. When the distance was increased from 8 mm to 56 mm (corresponding to a delay of 0.14 and 1.0 ms respectively for a CV of 56 m/s), the amplitude first increased and then decreased, the negative peak broadened and the duration increased. A second negative peak was not seen because the normal CV was too high (hence, the delay too short) to give sufficiently long delays
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between 2 unipolar NAPs with the interelectrode distances used. Simulation of Bipolar NAPs With Various Combinations of Delay, Unipolar Amplitude, and Unipolar Rise-time. In the following presentation of re-
sults from simulations, the resulting bipolar NAPs are compared to “normal” bipolar NAPs (Fig. 1A) for each electrode. A situation in which delay between templates is increased and amplitudes reduced (Fig. 1B) may simulate a loss of predominantly fast conducting axons. This may occur for instance with a primary axonal degeneration of sensory fibers. With a short interelectrode distance the amplitude of the resulting bipolar NAP was increased and the duration slightly prolonged although amplitude of the corresponding unipolar NAPs was decreased. With the longer electrode, the amplitude of the bipolar NAP was instead decreased and a double peak response was obtained. A different situation is shown in Figure l(C). The amplitude of the unipolar NAPs and delay were unchanged compared to Figure 1(A) but the
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Relative latency (ms) 0.0 0.1 0.2
0.3 0.4 0.5 0.6
0.0
- 0.6
FIGURE 3. A unipolar median nerve NAP (upper trace) is recorded proximal to the elbow (sweep duration 20 msec, stimulus delay 4.0 msec) with the reference electrode lateral at the same level. This unipolar NAP is successively delayed in steps of 0.1 msec (sweep duration 10 msec). Thus, 25 identical unipolar NAPs with relative latencies 0.0 to 2.4 msec are obtained and used as templates for simulation. Only the first 7 are demonstrated (raster and superimposed).
unipolar rise-time was doubled. This may simulate a local entrapment between the stimulating and recording electrodes with dispersion of the axonal action potentials but normal CV (delay) in the nerve under the recording electrode. In this case, where no loss of axons was simulated, the resulting amplitude of the bipolar NAP was decreased for both electrodes, more pronounced for the short electrode, and in addition to the expected increase in duration, also more pronounced for the short one. Finally, a combination of reduced amplitude of the unipolar NAPs, doubled unipolar rise-time, and doubled delay (Fig. 1D) simulated the findings in polyneuropathy. The duration of the bipolar NAP was increased and the amplitude was slightly decreased for both electrodes.
DISCUSSION
Recording of NAPs by means of bipolar surface electrodes is the most commonly used technique in routine nerve conduction investigations. In addition to CV, amplitude, area, and duration are used to detect deviations from normality. This
Uni- and Bipolar Recording
work complements earlier studies of the bipolar recording technique with computer simulations and demonstrates the dependence of the bipolar NAP on various factors. A bipolar NAP can be considered as the difference between two unipolar NAPs recorded between each of the poles of the bipolar recording electrode and a remote, indifferent reference electrode (Fig. 2). All bipolar NAP parameters (except onset latency of the first positive peak) vary considerably with the time taken for the nerve impulse to travel between the poles of the recording electrode (here called delay), which is determined by the interelectrode distance and the CV in the nerve segment below the recording electrode. Commercial electrodes have an interelectrode distance varying between 11 mm and 60 nim which makes it very difficult or even impossible to compare recordings from different laboratories. Furthermore, in many laboratories ring electrodes without any permanent fixation or standardized distances are used for digital nerve recordings. Amplitude and shape of the bipolar NAPs are influenced by the varying interelectrode distance; therefore, measurements of the parameters even
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B
A --\/A ----.--
0.1
-JflL---
Superimposed 0.1 0.8
0.3
-
0.5
0.7 Superimposed
0.9
_ _ I -
-
0.9 1.6
1.1
1.3
- Superimposed 1.7 - 2.4
1.5 1.7
1.9 Superlmposed
2.1
-
0.1 2.4 2.3
FIGURE 4. Simulation of bipolar NAPs with increasing time delay between the corresponding 2 unipolar NAPs: one template is kept constant (the template with relative latency 0.0 msec in Fig. 3), another identical template is delayed relative to the first in steps of 0.1 msec from 0.1 to 2.4 msec and subtracted from the first (templates with relative latencies 0.1 to 2.4 msec in Fig. 3). Every second of the resulting simulated bipolar NAPs are shown in (A). With increasing delay, the shape of the inverted second template becomes successively more obvious.
B
A Peak latency
(ms) 0.0 0.4 0.8
14
1.0
2.0
3.0
4.0
Amplitude
(Uv)
Duration (ms)
Area (nvs)
5.0
>
80
. 3.0
60 .
I
1.6 la2
2 *.O .4 Delay (ms)
1
i
’
2.0
40 .
. 1.0
20 .
1st pos
1st nag
2nd neg 2nd pos
0.0 0.4 0.8
1.2 1.6 2.0 2.4 Delay
(mS)
FIGURE 5. Changes in parameters of the simulated bipolar NAPs in Figure 4. With increasing delay between templates (simulating increasing interelectrode distance and/or decreasing CV) the parameters change following: (A) latencies of earlier peaks increase only initially, latencies of later peaks increase linearly, and a second negative peak appears with longer delays; and (B)total amplitude has a maximum at a certain delay, total area increases nonlinearly, and duration increases almost linearly.
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Uni- and Bipolar Recording
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Electrode distance (mm) ---.--8
32 40 48
56
8-40
40-56
FIGURE 6. Human median NAPs recorded bipolarly at the third digit with ring electrodes with increasing interelectrode distance following wrist stimulation. Changes of the recorded bipolar NAPs follow the same pattern as the simulated bipolar NAPs in Figure 4; the total amplitude has a maximum at a certain distance (delay), in this case at 40 mm. With longer distances the negative peak is broadened, its amplitude decreases, and the duration increases.
within one laboratory will not produce standardized normal results. Even when a laboratory uses only one type of bipolar electrode with a fixed interelectrode distance, interpretative difficulties occur. The assumption that fixed interelectrode distance will allow acceptable comparisons between reference values and patient data is incorrect. As seen from our simulations with varying delays between templates, the amplitude of an NAP recorded with a bipolar electrode relates in a complex way to the CV even in the normal nerve. This interaction is even more obvious in pathological situations where the change in CV may be larger. As examples of relations between nerve conduction parameters and bipolar NAPS some model situations were created. These show that the amplitude of the bipolar NAP may change op-
Uni- and Bipolar Recording
posite to the unipolar NAP for one interelectrode distance but not for another (Fig. 1). Amplitude varies in a complex way with changes in rise-time of the unipolar NAPS and the delay. T h e magnitude and even direction of change varies with electrode type, and there may be a decrease in amplitude of the bipolar NAP where obviously no loss of axons has occurred (Fig. 1(C), 17-mm electrode). The bipolar duration can be approximated according to the following: (bipolar duration) = (unipolar rise-time) + (delay) or: (bipolar duration) = (unipolar rise-time) + (interelectrode distance)/CV
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The rise-time of the unipolar NAP is the most important factor in determining the duration of the bipolar NAP, provided the interelectrode distance is small and CV is high (both giving a small value for the last factor). In situations of decreased CV and/or long interelectrode distance, the last factor will have an increased influence on the duration. This strongly points to the problem in correlating the bipolar NAP parameters with characteristics of the generators. In spite of the complex relationship between amplitude, duration, and other bipolar NAP parameters and underlying pathology, certain conclusions can be drawn, at least in relative terms. This assumes detailed knowledge about the abovementioned cancellation phenomena, electrode type, amplifier characteristics, and sometimes special signal analysis algorithms. It should be easier to obtain information from unipolarly recorded NAPs since these signals more closely reflect the summated activity from the generators. At the same time it needs to be borne in mind that a similar complex summation pattern also takes place on the level of action potentials from individual axons. Since this is not due to technical factors as in the case of electrode choice,
it cannot be avoided as long as mass recordings performed with surface or near nerve electrodes are performed. Unipolarly recorded NAPs often contain far field (Fig. 7). These may occur in any time relation to the main component of the NAP. When they have low amplitude, they can only be seen in the beginning and at the end of the signal and may influence the definition of start and end of the unipolar NAP. Any information that may be carried by these far field waves, for example, about abrupt changes in the volume conductor at entrapment points, is lost in the bipolar derivation. The unipolar recording technique should be preferred since it more closely reflects nerve parameters than the bipolar. But it also has some disadvantages: 2 separate electrodes are necessary and the unipolar recordings often contain more artifacts than the bipolar. By means of computer technique the unipolar- NAPS may be extracted from the bipolar. Here the far field potentials disappear but other parameters are accurately reproduced. This procedure should combine the advantages of both methods, the simplicity (one recording electrode) and freedom from artifacts
A from 1 (mm) ._____
-
1 2
FIGURE 7. (A) Median NAPs recorded unipolarly at the elbow (1) and at the upper arm (2-6) with increasing distances from (1) following wrist stimulation. A peripheral standing wave, unaffected by the increasing distance is seen at (*). (6)Subtractions made stepwise between the unipolar NAPs (1 -2, 2-3, . . .) give bipolar NAPs with increasing latencies. The standing wave is lost in the subtractions. Superimpositions are shown at bottom.
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in the bipolar recordings, and the better correlation to nerve parameters in the unipolar. Some
extraction techniques are currently under development.
REFERENCES 1. Bolton CF, Saiva GM, Carter K: Effects of temperature on human compound action potentia1s.j Neurol Neurosiirg Psychiatry 1981;44:407-413. 2. Buchthal F, Rosenfalck A-L: Evoked action potentials and conduction velocity in human sensory nerves. Brain Res 1966;3:1- 122. 3. Cummins KL, Perkel DH, Dorfman LJ: Nerve fiber conduction-velocity distributions. I. Estimation based o n the single-fiber and compound action potentials. Electroencephalogr Clzn Neurophysiol 1979;46:634-646. 4. Dorfman LJ: T h e distribution of conduction velocities in peripheral nerves: a review. Muscle Nerve 1984;1:2- 11. 5. Eisen A, Odusote K, Bozek C, Hoirch M: Far-field potentials from peripheral nerve: Generated at sites of muscle mass change. NeuroloQ 1986;36:815- 8 18. 6. Jewett DL, Deupree DL: Far-field potentials recorded from action potentials and from a tripole in a hemicylindrical volume. Electroencephalogr Clzn Neurophysiol 1989;72:439-449. 7. Kimura J, Machida M, Ishida T, Yamada T, Rodnitiky RL, Kudo Y, Suzuki S: Relation between size of compound sensory or muscle action potentials, and length of nerve segment. Neurology 1980;36:647-652. 8. Kimura J, Mitsudome A, Beck DO, Yamada T, Dickins
Uni- and Bipolar Recording
QS: Field distribution of antidromically activated digital nerve potentials: Model for far-field recording. A ' o i ~ t d q g 1983;33:1164- 1169. 9. Kimura J , Ishida T, Suzuki S, Kudo Y, hlatsuoka H , Yamada T: Far-field recording of the junctional potential generated by median neri'e volleys at the wrist. L \ ' ~ ~ ~ ( J ( ~ / ( ~ , q 1986;36:1451- 1457. 10. Kincaid J C , Minnick KA, Pappas S: A model o f the diftering change in motor and sensory action potentials over distance. Muscle N r n v 1988;l 1:318-323. 11. Rosenfalck A-L: Early recognition of nerve disorders by near-nerve recording of sensory action potentials. ll\lltrclr N r t w 1978;1:360-367. 12. Tashijian EA, Ellenberg MR, GI-OSSN, Chodoroff G , Honet .JC:Temperature effect on anticlroniic and orthodromic sensory nerve action potcntial latency and amplitude. A rch P l y izil~rlKeha hi1 1987 ;68:549 - 552. 13. Waxman S: Determinants of conduction velocity in myelinated nerve fibers. Mtcscle R i p t w 1980;3:141- 150. 14. Winkler T, Stilberg E: Trvo phenomena concerning transcutaneous peripheral nerve stimulation. Elpcrtoetrcc.f,halog,. C h i h ' e u ~ o ~ h y i o1985;6 l 1:83P. 15. Winkler T, Sdlberg E: Surface anodal stimulation of human peripheral nerves. Euf, Br& R e 1!)88;73:481-488.
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UNI= AND BIPOLAR SURFACE RECORDING OF HUMAN NERVE RESPONSES TOMAS WINKLER, MD, ERIK STALBERG, MD, PhD, and LINDSAY F. HAAS, MB, ChB, BMedSc, FRACP
Nerve conduction studies are of major importance in diagnosing focal and generalized diseases of nerves. For motor nerves, measurements of the muscle response latency and amplitude are usually used. For sensory and mixed nerve studies the nerve action potential (NAP) is recorded. Latency, amplitude, duration, and shape of the NAPS are measured to calculate nerve conduction velocity (CV), and indicate number of conducting axons,
From the Department of Clinical Neurophysiology. University Hospital, Uppsala, Sweden. Acknowledgment: This study was in part supported by the Swedish Medical Research Council (Grant 135, ES). Presented in part at the Forty-Sixth Annual Meeting of the Swedish Society of Clinical Neurophysiology, Stockholm, Sweden, December 1988. Address reprint requests to T Winkler. Department of Clinical Neurophysiology, University Hospital, S-751 85 Uppsala. Sweden. Accepted January 20, 1990 CCC 0148-639X/91/020133-09 $04.00 0 1991 John Wiley & Sons, Inc.
Uni- and Bipolar Recording
and their temporal dispersion. In most neurophysiological laboratories NAPS are recorded with bipolar surface electrodes placed along the nerve trunk. This method is noninvasive, easy to perform, and relatively free from artifacts. Less commonly, needle electrodes are used. T o interpret the factors determining the shape of the NAP, the factors contributing to it must be known. Major factors discussed in literature are: number of axons, axon diameter^,'^ density of axons in the nerve, distribution of axonal conduction v e l ~ c i t i e s , distance ~’~ between recording electrode and n e r ~ e , ~ ” stimulus ~’” strength, temperature of tissue and nerve,”12 polarity of stimulating electrodes, 14,15 filter settings in the recording equipment, and configuration of the recording electrode. The last factor has been carefully investigated by Buchthal and Rosenfalck.‘ They recorded the sensory NAPS from the median nerve at wrist and elbow with needle electrodes following digital stimulation. With bipolar recordings their main findings were:
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133
1. The bipolar NAP is the difference between 2 unipolarly recorded NAPs, slightly displaced in time. 2. Amplitude, duration, and shape of the bipolar NAP depend on distance between the poles of the recording electrode and CV. 3. Maximal amplitude is obtained when the time interval between the unipolar NAPs is such that the negative peak of the earlier unipolar NAP coincide with the positive peak of the latter. 4. The latency to the onset of the initial positive phase is determined by the unipolar NAP recorded by the electrode pole closest to the stimulus site. The importance of the distance between the poles of the recording bipolar electrode is often overlooked, and if ring or silver cup electrodes are used without any corrections for variations of interelectrode distances, errors will result. The aim of this study is to further investigate the effect on the bipolar NAP of different time delays (ie, the time taken for the NAP to travel between the two poles of the recording bipolar electrode) and variations of the shape of the corresponding unipolar NAPs.
METHODS
These were performed on 4 healthy volunteers aged 25 to 5 1 years. ‘Their median nerves were stimulated supramaximally at the wrist with short square pulses (duration 0.1 msec) at a frequency of 1 Hz. Bipolar recordings were made with a standard surface felt pad electrode (Dantec 9013 L, interpole distance 23 mm) placed over the nerve proximal to the elbow. Unipolar NAPs from one or the other of the pads of the bipolar electrode were obtained using a felt pad electrode (diameter 8 mm) as reference, placed on the lateral side of the arm at the same level as the bipolar electrode. The distance to the reference electrode was large enough to prevent signals from the nerve to be recorded by the reference. Recordings were made on a routine EMG equipment (Medelec MS 90, Mystro) with filter settings 2 Hz to 10 kHz. Sixty responses were averaged for each trace. Measurements of NAPs were made after manual setting of cursors. Amplitudes were measured between maximal positive and maximal negative peaks. Durations of bipolar NAPs were measured between the first and last positive peak, and total area from the onset of the Median Nerve Recordings.
134
Uni- and Bipolar Recording
first positive to the end of the last positive or negative phase.
A unipolar NAP recorded between the distal pad of the bipolar electrode and the reference was stored in the computer as template for simulation of bipolar recordings. This template was kept at a constant latency, then a succession of identical templates were delayed relative to the first in increasing steps of 0.1 msec from 0.1 to 2.4 msec. By subtracting each successive delayed template from the first a series of simulated bipolar NAPs with increasing delays between the corresponding unipolar NAPs were obtained.
Simulation.
In another series, the technique was used to simulate bipolar NAPs in different clinical situations. This was performed by changing the delay between the templates, and/or amplitude of and/or rise-time of the templates (rise-time defined as latency between positive and negative peaks of the template). For each of 4 conditions bipolar NAPs obtained with 2 different electrodes with interelectrode distances 17 and 45 mm (Fig. 1) were simulated, respectively. The conditions to be simulated are normality (Fig. lA), primary sensory axonal degeneration (Fig. 1B), nerve entrapment (Fig. IC), and polyneuropathy (Fig. ID). Figure 1(A). “Normal” delay (calculated for the two interelectrode distances) is 0.3 msec and 0.8 msec resp. if CV = 56 m/s. If this delay is 100% for the 17-mm electrode, the delay for the 45-mm electrode will be 265%; the “normal” amplitude is set to 100% and “normal” rise-time is also set to 100% of the templates. Figure I(B). Doubled delay (200% and 5304 for the 17- and 45-mm electrodes respectively, CV = 28 mis), decreased amplitude (84%), and normal rise-time (100%) of the templates. Figure I(C). Normal delay (ie, 100% and 265% respectively, CV = 56 m/s), normal amplitude (loo%), and doubled rise-time (200%) of the templates. Figure I(D). Doubled delay (ie, 200 and 530% respectively, CV = 28 m/s), decreased amplitude (84%), and doubled rise-time (200%) of the templates.
Simulation of Clinical Situations.
To validate the simulations, the median nerves in 2 volunteers were stimulated at the wrist. Bipolar recordings were obtained
Clinical Comparison.
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A
B
C
D
FIGURE 1. Bipolar recordings may be altered in different clinical situations. Bipolar recorded NAPs are simulated with interelectrode distances of 17 (trace 3) and 45 mm (trace 6). The corresponding unipolar NAPs are shown above each bipolar NAP respectively (trace 1-2 = 3 and trace 4-5 = 6). (A) Normal conditions. Delay between unipolar NAPs, duration of bipolar NAP for the 17-mm electrode, amplitude and rise-time of unipolar NAPs are all set to 100% and later used as references. Delay for the 45-mm electrode is here 265% and amplitudes of bipolar NAPs are 106% and 156%, respectively. (6)Primary axonal degeneration of sensory fibers may give a loss of fast axons = decrease of CV = increased delay (200% and 530%, respectively, are used). A decrease of the unipolar amplitude is also simulated (amplitude of unipolar NAPs is here 84%). Due to favorable or unfavorable summation effects, the amplitude of the bipolar NAPs is increased for 17 mm (129%) but decreased and biphasic for 45 mm (112%), respectively,compared with (A) (106% and 156%, respectively).(C) Local entrapment between stimulating and recording electrodes may give a dispersion of action potentials [rise-timeof unipolar NAP is here 200% compared with (A)] while CV (delay) and amplitude of unipolar NAPs are unchanged. The amplitudes of the bipolar NAPs are decreased (59% and 129%, respectively) compared with (A) (106% and 156%, respectively). Thus, the decrease of bipolar amplitudes does not reflect any loss of axons. If a decrease of amplitude of unipolar NAPs is also simulated (not shown here) amplitudes of bipolar NAPs would be even smaller. (D) An axonal and demyelinating neuropathy gives decrease of CV = increase in delay (here 200% and 530%, respectively),dispersion = increase in rise-time (here 200%) and a loss of axons = drop in amplitude of unipolar NAP (here 84%). Due to various summation effects the amplitudes of the bipolar NAPs (91% and 135%, respectively) are slightly decreased compared to (A) (106% and 156%, respectively).Compared to (C) (59% and 129%, respectively) they are increased and unchanged respectively. The durations of the bipolar NAPs show an increase from (A) to (D): loo%, 113%, 200%, and 206% for the 17-mm interelectrode separation and 31%, 194%, 206%, and 256% for the 45-mm electrode separation, respectively.
with ring electrodes at increasing interelectrode distances at the third digit.
3. RESULTS
When two recorded unipolar NAPs were subtracted, the constructed bipolar NAP was identical to the directly recorded bipolar NAP (Fig. 2) showing that the simulations were valid. Relation Between Uni- and Bipolar NAPs.
4.
Simulation of Bipolar NAPs With Increasing Delay Between Its Two Templates. As the delay be-
tween the two templates increased, the configuration of the constructed bipolar NAP showed the following characteristics (Figs. 3, 4 and 5 ) : 1. The latency to the onset of the first positive peak was unchanged. 2. The latency of the first positive peak increased slightly until its amplitude reached the maximal
Uni- and Bipolar Recording
5.
6.
value (equal to the maximal positive amplitude of the first template). The latency of the negative peak first increased. After a certain delay the peak was divided into two peaks. Following this only the second peak showed any major changes in latency. The amplitude of the negative peak increased until the peak divided. After this, the amplitudes of the 2 negative peaks decreased to minimum levels that were equal to the maximal negative amplitude of the first template and the maximal positive amplitude of the second template respectively. The amplitude of the last positive peak increased to a maximal value which was equal to the maximal negative amplitude of the second template. The total amplitude increased rapidly to a
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A dist
prox
FIGURE 2. Recordings (A) and recording setups (B) showing various combinations of signal derivations. Numbers in A and B correspond. Distal unipolar NAP ( l ) , proximal unipolar NAP (2), and bipolar NAP (3) from a median nerve recorded between each of the poles and a remote reference (1, 2) or between the poles (3) of a bipolar electrode placed at the elbow. Wrist stimulation. Trace (4) shows the subtraction of (2) from (1). This difference is equal to the recorded bipolar response (3); (3) and (4) are superimposed in (5). Differences in peak latencies and amplitudes between uni- and bipolarly recorded NAPs are demonstrated in (6).
maximum when the negative peak of the first and the positive peak of the second template coincided (here for a delay of 0.8 msec). 7 The duration between the first and last positive peaks increased only slightly for short delays (here for delays less than 0.5 msec) but linearly for longer delays (here for delays exceeding 0.8 msec; Fig. 4B). 8. The total area increased nonlinearly.
Recording of Bipolar NAPs With Increasing Interelec. trode Distance. The variation of bipolarly re-
corded NAPS when using various distances between the recording ring electrodes (Fig. 6), followed the same pattern as in the simulations already described. When the distance was increased from 8 mm to 56 mm (corresponding to a delay of 0.14 and 1.0 ms respectively for a CV of 56 m/s), the amplitude first increased and then decreased, the negative peak broadened and the duration increased. A second negative peak was not seen because the normal CV was too high (hence, the delay too short) to give sufficiently long delays
136
Uni- and Bipolar Recording
between 2 unipolar NAPs with the interelectrode distances used. Simulation of Bipolar NAPs With Various Combinations of Delay, Unipolar Amplitude, and Unipolar Rise-time. In the following presentation of re-
sults from simulations, the resulting bipolar NAPs are compared to “normal” bipolar NAPs (Fig. 1A) for each electrode. A situation in which delay between templates is increased and amplitudes reduced (Fig. 1B) may simulate a loss of predominantly fast conducting axons. This may occur for instance with a primary axonal degeneration of sensory fibers. With a short interelectrode distance the amplitude of the resulting bipolar NAP was increased and the duration slightly prolonged although amplitude of the corresponding unipolar NAPs was decreased. With the longer electrode, the amplitude of the bipolar NAP was instead decreased and a double peak response was obtained. A different situation is shown in Figure l(C). The amplitude of the unipolar NAPs and delay were unchanged compared to Figure 1(A) but the
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February 1991
Relative latency (ms) 0.0 0.1 0.2
0.3 0.4 0.5 0.6
0.0
- 0.6
FIGURE 3. A unipolar median nerve NAP (upper trace) is recorded proximal to the elbow (sweep duration 20 msec, stimulus delay 4.0 msec) with the reference electrode lateral at the same level. This unipolar NAP is successively delayed in steps of 0.1 msec (sweep duration 10 msec). Thus, 25 identical unipolar NAPs with relative latencies 0.0 to 2.4 msec are obtained and used as templates for simulation. Only the first 7 are demonstrated (raster and superimposed).
unipolar rise-time was doubled. This may simulate a local entrapment between the stimulating and recording electrodes with dispersion of the axonal action potentials but normal CV (delay) in the nerve under the recording electrode. In this case, where no loss of axons was simulated, the resulting amplitude of the bipolar NAP was decreased for both electrodes, more pronounced for the short electrode, and in addition to the expected increase in duration, also more pronounced for the short one. Finally, a combination of reduced amplitude of the unipolar NAPs, doubled unipolar rise-time, and doubled delay (Fig. 1D) simulated the findings in polyneuropathy. The duration of the bipolar NAP was increased and the amplitude was slightly decreased for both electrodes.
DISCUSSION
Recording of NAPs by means of bipolar surface electrodes is the most commonly used technique in routine nerve conduction investigations. In addition to CV, amplitude, area, and duration are used to detect deviations from normality. This
Uni- and Bipolar Recording
work complements earlier studies of the bipolar recording technique with computer simulations and demonstrates the dependence of the bipolar NAP on various factors. A bipolar NAP can be considered as the difference between two unipolar NAPs recorded between each of the poles of the bipolar recording electrode and a remote, indifferent reference electrode (Fig. 2). All bipolar NAP parameters (except onset latency of the first positive peak) vary considerably with the time taken for the nerve impulse to travel between the poles of the recording electrode (here called delay), which is determined by the interelectrode distance and the CV in the nerve segment below the recording electrode. Commercial electrodes have an interelectrode distance varying between 11 mm and 60 nim which makes it very difficult or even impossible to compare recordings from different laboratories. Furthermore, in many laboratories ring electrodes without any permanent fixation or standardized distances are used for digital nerve recordings. Amplitude and shape of the bipolar NAPs are influenced by the varying interelectrode distance; therefore, measurements of the parameters even
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B
A --\/A ----.--
0.1
-JflL---
Superimposed 0.1 0.8
0.3
-
0.5
0.7 Superimposed
0.9
_ _ I -
-
0.9 1.6
1.1
1.3
- Superimposed 1.7 - 2.4
1.5 1.7
1.9 Superlmposed
2.1
-
0.1 2.4 2.3
FIGURE 4. Simulation of bipolar NAPs with increasing time delay between the corresponding 2 unipolar NAPs: one template is kept constant (the template with relative latency 0.0 msec in Fig. 3), another identical template is delayed relative to the first in steps of 0.1 msec from 0.1 to 2.4 msec and subtracted from the first (templates with relative latencies 0.1 to 2.4 msec in Fig. 3). Every second of the resulting simulated bipolar NAPs are shown in (A). With increasing delay, the shape of the inverted second template becomes successively more obvious.
B
A Peak latency
(ms) 0.0 0.4 0.8
14
1.0
2.0
3.0
4.0
Amplitude
(Uv)
Duration (ms)
Area (nvs)
5.0
>
80
. 3.0
60 .
I
1.6 la2
2 *.O .4 Delay (ms)
1
i
’
2.0
40 .
. 1.0
20 .
1st pos
1st nag
2nd neg 2nd pos
0.0 0.4 0.8
1.2 1.6 2.0 2.4 Delay
(mS)
FIGURE 5. Changes in parameters of the simulated bipolar NAPs in Figure 4. With increasing delay between templates (simulating increasing interelectrode distance and/or decreasing CV) the parameters change following: (A) latencies of earlier peaks increase only initially, latencies of later peaks increase linearly, and a second negative peak appears with longer delays; and (B)total amplitude has a maximum at a certain delay, total area increases nonlinearly, and duration increases almost linearly.
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Uni- and Bipolar Recording
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Electrode distance (mm) ---.--8
32 40 48
56
8-40
40-56
FIGURE 6. Human median NAPs recorded bipolarly at the third digit with ring electrodes with increasing interelectrode distance following wrist stimulation. Changes of the recorded bipolar NAPs follow the same pattern as the simulated bipolar NAPs in Figure 4; the total amplitude has a maximum at a certain distance (delay), in this case at 40 mm. With longer distances the negative peak is broadened, its amplitude decreases, and the duration increases.
within one laboratory will not produce standardized normal results. Even when a laboratory uses only one type of bipolar electrode with a fixed interelectrode distance, interpretative difficulties occur. The assumption that fixed interelectrode distance will allow acceptable comparisons between reference values and patient data is incorrect. As seen from our simulations with varying delays between templates, the amplitude of an NAP recorded with a bipolar electrode relates in a complex way to the CV even in the normal nerve. This interaction is even more obvious in pathological situations where the change in CV may be larger. As examples of relations between nerve conduction parameters and bipolar NAPS some model situations were created. These show that the amplitude of the bipolar NAP may change op-
Uni- and Bipolar Recording
posite to the unipolar NAP for one interelectrode distance but not for another (Fig. 1). Amplitude varies in a complex way with changes in rise-time of the unipolar NAPS and the delay. T h e magnitude and even direction of change varies with electrode type, and there may be a decrease in amplitude of the bipolar NAP where obviously no loss of axons has occurred (Fig. 1(C), 17-mm electrode). The bipolar duration can be approximated according to the following: (bipolar duration) = (unipolar rise-time) + (delay) or: (bipolar duration) = (unipolar rise-time) + (interelectrode distance)/CV
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The rise-time of the unipolar NAP is the most important factor in determining the duration of the bipolar NAP, provided the interelectrode distance is small and CV is high (both giving a small value for the last factor). In situations of decreased CV and/or long interelectrode distance, the last factor will have an increased influence on the duration. This strongly points to the problem in correlating the bipolar NAP parameters with characteristics of the generators. In spite of the complex relationship between amplitude, duration, and other bipolar NAP parameters and underlying pathology, certain conclusions can be drawn, at least in relative terms. This assumes detailed knowledge about the abovementioned cancellation phenomena, electrode type, amplifier characteristics, and sometimes special signal analysis algorithms. It should be easier to obtain information from unipolarly recorded NAPs since these signals more closely reflect the summated activity from the generators. At the same time it needs to be borne in mind that a similar complex summation pattern also takes place on the level of action potentials from individual axons. Since this is not due to technical factors as in the case of electrode choice,
it cannot be avoided as long as mass recordings performed with surface or near nerve electrodes are performed. Unipolarly recorded NAPs often contain far field (Fig. 7). These may occur in any time relation to the main component of the NAP. When they have low amplitude, they can only be seen in the beginning and at the end of the signal and may influence the definition of start and end of the unipolar NAP. Any information that may be carried by these far field waves, for example, about abrupt changes in the volume conductor at entrapment points, is lost in the bipolar derivation. The unipolar recording technique should be preferred since it more closely reflects nerve parameters than the bipolar. But it also has some disadvantages: 2 separate electrodes are necessary and the unipolar recordings often contain more artifacts than the bipolar. By means of computer technique the unipolar- NAPS may be extracted from the bipolar. Here the far field potentials disappear but other parameters are accurately reproduced. This procedure should combine the advantages of both methods, the simplicity (one recording electrode) and freedom from artifacts
A from 1 (mm) ._____
-
1 2
FIGURE 7. (A) Median NAPs recorded unipolarly at the elbow (1) and at the upper arm (2-6) with increasing distances from (1) following wrist stimulation. A peripheral standing wave, unaffected by the increasing distance is seen at (*). (6)Subtractions made stepwise between the unipolar NAPs (1 -2, 2-3, . . .) give bipolar NAPs with increasing latencies. The standing wave is lost in the subtractions. Superimpositions are shown at bottom.
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Uni- and Bipolar Recording
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in the bipolar recordings, and the better correlation to nerve parameters in the unipolar. Some
extraction techniques are currently under development.
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Uni- and Bipolar Recording
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