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Short latency somatosensory evoked potentials from radial, median and ulnar nerve stimulation in man
Electroencephalography and Clinical Neurophysiology, 1980, 5 0 : 3 7 5 - - 3 8 1 © Elsevier/North-Holland Scientific Publishers, Ltd.
375
SHORT LATENCY SOMATOSENSORY EVOKED POTENTIALS FROM RADIAL, MEDIAN AND U L N A R N E R V E STIMULATION IN MAN 1 J.S. GRISOLIA and W.C. WIEDERHOLT
Veterans Administration Medical Center, San Diego, Calif. 92161 and Department o f Neurosciences, University o f California at San Diego, School o f Medicine, La Jolla, Calif. 92093 (U.S.A.) (Accepted for publication: June 12, 1980)
Short latency components of the somatosensory evoked potential (SEP) have been recorded in humans (Desmedt 1971; Cracco and Cracco 1976; Goff et al. 1977; Wiederholt and Iragui-Madoz 1977; Anziska et al. 1978). Anatomical correlates of these components have been tentatively assigned on the basis of latency and scalp distribution in humans (Kritchevsky and Wiederholt 1978) supplemented b y depth recordings and lesion experiments in animals (Iragui-Madoz and Wiederholt 1977; Wiederholt and Iragui-Madoz 1977; Arezzo et al. 1979). The clinical utility of short latency auditory evoked potentials has been well demonstrated (Stockard et al. 1976; Stockard and Rossiter 1977; Starr 1978). Short latency SEPs have been examined in multiple sclerosis (Anziska et al. 1979), in coma (Goldie et al. 1979; Anziska and Cracco 1980), and o t h e r CNS lesions (Yamada et al. 1978; Anziska and Cracco 1979). To enhance the clinical utility of short latency SEP and to further investigate its underlying generators in humans, we have examined SEPs in normal volunteers after stimulation of several peripheral nerves in the forearm. Implications for diagnosis of diseases of both the central and peripheral nervous system will be considered.
1 Supported by the Medical Research Service of the Veterans Administration.
Method Ten normal volunteers (7 men, 3 women, aged 20--27 years) were examined. This study was approved b y the University of California and Veterans Administration Committees on Investigations Involving Human Subjects. Informed consent was obtained from all participants. Stimulating needle electrodes (platinum alloy, 12 mm long, 0.3 mm diameter) were inserted subcutaneously to overlie the median, ulnar and superficial branch of radial nerves at the wrist with cathode placed 1 cm proximal to anode. A stimulator delivered square wave pulses of 0.2 msec duration at a frequency of 4/sec through a stimulus isolation unit. Stimulus voltage was adjusted to produce a small muscle twitch for ulnar and median nerve stimulation, while radial nerve stimulation voltage was adjusted to equal the subjective intensity of stimulation at the other sites. In most cases, stimulus voltage was a b o u t 4 times the least detectable stimulus intensity. SEPs were recorded with platinum alloy needle electrodes placed subcutaneously at F3, F4, C3 and C4 (International 10-20 system) referenced to needle electrodes placed subcutaneously in the forehead (FPz) and in the right knee. A ground electrode was placed in the skin of the right forearm. O u t p u t from the recording electrodes went to a differential amplifier with a 10--3000 c/ sec bandpass (50% attenuation at 8 c/sec and
376
J.S. G R I S O L I A , W.C. W I E D E R H O L T
3000 c/sec) and was fed on-line to a laborat o r y computer and/or stored on FM magnetic tape for later analysis. All amplifier channels were calibrated with a 20 pV signal of 10 msec duration. The computer averaged a total of 1500 sweeps at a sampling rate of 1 point for 127 psec which has been shown to give equivalent results to a sampling rate of 40 psec per point (Kritchevsky and Wiederholt 1978). Sweep duration was 80 msec. Averages were displayed on an oscilloscope screen and were plotted on an electrostatic matrix plotter. In all recordings and tracings, an upward deflection signifies relative positivity in grid one of the differential amplifier. Peak latencies and amplitudes were measured on traces from the plotter. Amplitudes were measured on both of the duplicate traces in each subject and data from all subjects were pooled {Table II). All measurements were made on traces from C3 or C4 referenced to knee, except for measurements made on N19 and P20. These latter components were measured on recordings from F3 or F4 referenced to knee because P20 was seen most reliably at these locations. Means and standard errors were calculated and compared by Student's t-test for different stimulation sites. Median, ulnar, and radial nerves were each stimulated unilaterally and bilaterally. In addition, several nerves within one limb were stimulated simultaneously in the following combinations: median and radial; radial and ulnar; median and ulnar; and median, radial,
and ulnar. For unilateral stimulation, the right arm was used in 7 subjects and the left in three, determined by the subject's preference. SEP components were specified by polarity and average peak latency in conformance with the recommendations of the Committee on Methods of the International Symposium on Cerebral Evoked Potentials in Man, Brussels, 1974.
Results
Typical traces of short latency SEPs from all stimulation combinations are presented in Figs. 1 and 2. Latency and amplitude characteristics of the different short latency components are presented in Tables I and II. Unilateral and bilateral median nerve stimulation yielded 6 early potentials (P10, P12, P14, N19, P20, P23) as described previously (Kritchevsky and Wiederholt 1978) 2. Bilateral stimulation significantly increased the amplitudes of components in P10, P14, and N19 (P < 0.005, P <: 0 . 0 2 , P < 0.005, respectively) but not those of P20 and P23. The amplitude increase of P12 was not significant due to small sample size. With ulnar nerve stimulation, a similar SEP
2 P10, P14 a n d N19 were i d e n t i f i e d w i t h s t i m u l a t i o n o f each o f t h e 3 nerves in all subjects. P12 was seen in six, a n d P20 a n d P23 were p r e s e n t in nine.
TABLE I Peak latency (msec) o f SEP with radial, m e d i a n and ulnar nerve s t i m u l a t i o n . P10, P12, P14 a n d P23 latencies were P20 were m e a s u r e d f r o m t h e contralateral frontal e l e c t r o d e (F3 or F4) r e f e r e n c e d to knee. (Ten n o r m a l subjects.
P10 P12 P14 N19 P20 P23
Unilateral median
Unilateral radial
Unilateral ulnar
Bilateral median
Bilateral ulnar
10.1 12.3 14.2 18.7 20.2 23.1
10.1 12.7 14.9 18.6 20.2 23.7
10.0 12.7 15.0 19.2 21.0 22.9
10.0 12.0 14.2 18.7 20.3 23.2
10.2 12.0 14.6 18.9 20.4 23.2
+ 0.27 -+0.38 -+ 0.43 -+ 0.35 -+ 0.43 -+ 0.38
-+ 0.23 -+0.46 -+ 0.35 + 0.45 + 0.53 -+ 0.48
+ 0.24 -+0.46 -+ 0.58 -+ 0.45 -+ 0.44 -+ 0.45
-+ 0.26 -+0.43 -+ 0.45 + 0.27 -+ 0.26 -+ 0.51
-+ 0.25 -+0.45 -+ 0.44 +- 0.36 + 0.38 -+ 0.51
S H O R T L A T E N C Y SEPs
377 MEDIAN +
M E D I A N + RADIAL BILATERAt MEOIAN-
BILATERAL RAOIAL
!
,,
BILATERALULNAR
ULNAR
/% ,,~ I'i
J I i' !: \ lO MSEC
-
UNILATERAL MEDIAN
UNILATERAL RADIAL
UNILATERAL ULNAR m
PISEC •
~l
, ~ ,
.
RADIAL + ULNAR
f:?>:j::5;:*
M E D I A N + RADIAL +
ULNAR
eI
/
Fig. 1. Early SEP c o m p o n e n t s w i t h median, radial, and ulnar nerve stimulation. All traces are from the same subject. T w o successive averages of 1 5 0 0 s w e e p s are displayed. Upper traces are F3 referenced to right knee; l o w e r traces are C3 refereneed to right knee.
pattern was seen except that P10 was frequently bilobed and significantly smaller in amplitude compared to median nerve stimulation (P < 0.005). Bilateral stimulation resulted in increased amplitude and clarity of the potentials although this was not reflected in a significant increase in amplitude except for N19 {P < 0.02).
fJ PW'
Fig. 2. Early SEP c o m p o n e n t s w i t h s i m u l t a n e o u s nerve stimulation. T w o successive averages of 1 5 0 0 s w e e p s from the same subject as Fig. 1 are s h o w n . Upper traces are F3 referenced to right knee; lower traces are C3 referenced to right knee.
Radial nerve stimulation elicited a pattern of potentials similar to that seen with either median nerve or ulnar nerve stimulation. P10
measured on potentials recorded from C3 or C4, referenced to knee, on the side contralateral to stimulation. N 1 9 and Values are means _+ S.E.) Bilateral radial
Median + radial
Median + ulnar
Radial + ulnar
Median + ulnar + radial
10.2 13.2 14.8 18.7 20.6 23.2
10.0 12.5 14.3 19.3 20.7 23.5
10.3 12.6 14.7 18.7 20.9 23.2
10.6 13.0 15.0 19.5 20.6 23.9
10.3 12.7 14.8 18.9 20.9 23.5
+ 0.25 +0.85 -+ 0 . 4 8 _+0.55 -+ 0 . 5 2 -+ 0 . 4 6
+ 0.27 _+0.46 -+ 0 . 3 3 _+0.32 -+ 0 . 5 9 -+ 0 . 3 7
-+ 0 . 2 6 _+0.30 _+ 0 . 4 0 +0.41 _+0 . 5 2 _+ 0 . 5 8
+ 0.18 +0.37 _+ 0 . 3 9 -+0.52 + 0.47 _+0 . 6 4
-+ 0 . 2 6 -+0.63 _+0 . 3 9 -+0.54 -+ 0 . 5 5 _+0 . 6 9
378
J.S. G R I S O L I A , W.C. W I E D E R H O L T
T A B L E II A m p l i t u d e s (pV) o f SEP with radial, m e d i a n , and ulnar nerve s t i m u l a t i o n . Each c o m p o n e n t was m e a s u r e d f r o m its ont u d e s were m e a s u r e d o n p o t e n t i a l s r e c o r d e d f r o m C3 or C4, r e f e r e n c e d to knee, o n t h e side contralateral t o stimulasubjects. Values are m e a n s -+ S.E.)
P10 P12 P14 N19 P20 P23
Unilateral median
Unilateral radial
Unilateral ulnar
Bilateral median
Bilateral radial
2.4 0.43 1.13 3.74 1.37 1.85
0.81 0.46 1.03 1.69 0.73 0.79
1.19 0.80 0.85 1.89 1.14 1.12
4.49 0.54 1.92 6.03 1.61 1.92
1.23 0.63 0.96 1.96 0.93 0.93
+0.25 -+0.07 -+0.08 -+ 0.33 -+ 0.23 -+0.69
-+0.09 -+0.11 -+ 0.11 -+ 0.21 -+ 0.14 -+0.11
was significantly smaller in amplitude compared with the P10 of median nerve stimulation ( P ( 0 . 0 0 5 ) . Bilateral stimulation improved clarity of potentials without a significant increase in amplitude. In individual subjects, P12 was often larger and better defined with radial or ulnar nerve stimulation than with median nerve stimulation. The P12 amplitude was significantly larger only with ulnar nerve stimulation (unilateral stimulation, P ~ 0.01; bilateral stimulation, P < 0.005). Simultaneous unilateral stimulation of several nerves produced higher amplitudes of some components b u t with some sacrifice in clarity (see Fig. 2). SEPs from median nerve stimulation were compared with SEPs from all other stimulus combinations by paired ttest for amplitude of each component. With simultaneous median, radial and ulnar nerve stimulation, P10 was significantly larger (P 0.005} as was N19 ( P < 0.01). Increases in amplitudes of other components were not statistically significant.
Discussion Short latency SEP components were recorded after stimulation of median, ulnar and radial nerves, singly or in combination. Although the wave forms with each stimulation site were similar, there were significant differences which may have both theoretical
-+0.22 -+0.10 +0.14 -+ 0.18 -+ 0.16 +0.22
_+0.43 -+0.06 -+0.33 -+ 0.37 -+ 0.39 -+0.85
-+0.27 -+0.12 -+0.20 -+ 0.27 -+ 0.15 -+0.15
and clinical importance. With stimulation of the superficial branch of radial nerve, a pure sensory nerve, P10 was low in amplitude and frequently was bilobed. Ulnar~lerived P10 was intermediate in amplitude between radial and median. P10 has been localized to brachial plexus fibers b y recordings from supraclavicular electrodes (Jones 1977) and b y its preservation despite complete C5-T1 r o o t avulsion (Anziska and Cracco 1979). The strikingly larger amplitude of P10 with median nerve stimulation may partly result from activity in antidromically stimulated m o t o r fibers. Beyond P10, there appear to be no significant differences between radial, ulnar and median
S H O R T L A T E N C Y SEPs
379
set to peak e x c e p t N19, w h i c h is m e a s u r e d f r o m t h e peak o f P14 to the t r o u g h o f N19. P10, P12, P14, and P23 amplition. N19 and P20 were m e a s u r e d f r o m t h e c o n t r a l a t e r a l frontal e l e c t r o d e (F3 or F4) r e f e r e n c e d to knee. (Ten n o r m a l
Bilateral ulnar
Median + radial
Median + ulnar
Radial + ulnar
Median + ulnar + radial
1.87 0.73 1.12 2.50 1.56 1.44
2.79 0.47 1.02 3.21 1.13 1.77
2.30 0.53 1.07 3.11 1.61 2.00
1.94 0.55 1.11 2.82 0.86 1.93
3.60 0.74 1.37 4.83 1.73 2.47
+ 0.33 + 0.21 + 0.20 +__0.26 -+0.26 -+ 0.46
-+ 0.39 -+ 0.10 + 0.11 +- 0.43 -+0.36 -+ 0.57
-+ 0.26 + 0.09 -+ 0.18 __+0.41 -+0.38 -+ 0.55
times less well defined. The slightly different latencies and morphologies of certain ulnarderived components probably explain the slurring of P12 and P14 when ulnar nerve is stimulated in combination with the others. Desmedt and Noel (1973) have called attention to the diagnostic value of cortical SEP in peripheral lesions, and other workers have also used cortical SEP in diagnosis of brachial plexus injuries ( Z v ~ i n a and Kredba 1977). Recognition of early SEP components
C7
C8
IT1
ULNAR NERVE
Fig. 3. Brachial plexus fibers activated by m e d i a n , radial, a n d ulnar nerve s t i m u l a t i o n a t the wrist. Affere n t s o m a t o s e n s o r y fibers are s h o w n in black. M o t o r fibers w h i c h are a n t i d r o m i c a l l y activated are s h a d e d .
+ 0.10 -+ 0.09 -+ 0.14 __+0.46 -+0.09 -+ 0.80
+ 0.30 + 0.25 -+ 0.66 __+0.50 __+0.20 + 0.49
following median, radial and ulnar stimulation will be particularly helpful in anatomical diagnosis of peripheral nerve and brachial plexus disorders. As shown in Fig. 3, the afferent and efferent pathways from the 3 stimulation sites at the wrist embrace every major subdivision of the brachial plexus except the C5 root. Median nerve stimulation at the wrist activates somatosensory fibers which pass along the lateral cord to reach the upper and middle trunks and then enter the spinal cord through the posterior C6 and C7 roots. The antidromic m o t o r activity traverses the medial cord and lower trunk to enter through the anterior C8 and T1 roots. Radial somatosensory impulses travel up the posterior cord and upper trunk to reach C6. Ulnar somatosensory impulses enter the medial cord and lower trunk to reach C8, while the antidromic m o t o r c o m p o n e n t crosses the medial cord and lower trunk to reach T1. The short latency SEP patterns with the 4 most c o m m o n brachial plexus injuries are readily predicted from inspection of Fig. 3. Injuries to the upper trunk will delay or attenuate all components of the median and radial
380 stimulation. Radial
Summary Short latency somatosensory evoked potentials (SEPs) were elicited by stimulation at the wrist of median, radial, and ulnar nerves, singly or in combination, using normal subjects. Amplitude of P10 was strikingly lower with radial stimulation than with median stimulation, while ulnar
J.S. GRISOLIA, W.C. WIEDERHOLT of ra.dial, ulnar, and median stimulation for localizing peripheral lesions derives from the distinct anatomical pathways of the stimulated fibers through the brachial plexus and from the separable m o t o r and sensory components of P10. SEP is less invasive than EMG; this fact, plus its freedom from sampiing error, make it potentially more suitable than conventional EMG for sequentially following a patient's clinical course.
R~sum~ Potentiels dvoquds somatosensoriels de latence courte par stimulation des nerfs radial, mddian et ulnaire chez l ' h o m m e Les potentiels ~voqu~s somatosensoriels (PES) de latence courte ont ~t~ provoqu~s par stimulation au poignet des nerfs m~dian, radial et ulnaire, isol~ment ou de faqon conjugu~e, chez des sujets normaux. L'amplitude de P10 est n e t t e m e n t plus faible avec la stimulation radiale qu'avec la stimulation m~diane tandis que le P10 par stimulation ulnaire est interm~diaire quant ~ son amplitude. Cette difference refl~te probablement la d~charge antidromique des fibres motrices contenues dans le nerf m~dian compar~es ~ la branche superficielle du nerf radial qui est entibrement sensitif. Au
SHORT LATENCY SEPs The authors gratefully acknowledge the technical assistance of Mr. Byron Budnick.
References Anziska, B.J. and Cracco, R.Q. Short latency somatosensory evoked potentials in patients with focal lesions of the nervous system. Neurology (Minneap.), 1979, 29: 582. Anziska, B.J. and Cracco, R.Q. Somatosensory evoked short latency potentials in brain dead patients. Electroenceph. clin. Neurophysiol., 1980, 49: 10P. Anziska, B.J., Cracco, R.Q., Cook, A.W. and Feld, E.W. Somatosensory far-field potentials: studies in normal subjects and patients with multiple sclerosis. Electroenceph. clin. Neurophysiol., 1978, 45: 602--610. Anziska, B.J., Cracco, R.Q., Cook, A.W. and Feld, E.W. Somatosensory evoked far-field potentials in patients with multiple sclerosis. Electroenceph. clin. Neurophysiol., 1979, 46 : l l P . Arezzo, J., Legatt, A.D. and Vaughan, Jr., H.G. Topography and intracranial sources of somatosensory evoked potentials in the monkey. I. Early components. Electroenceph. clin. Neurophysiol., 1979, 46: 155--172. Cracco, R.Q. and Cracco, J.B. Somatosensory evoked potentials in man: far-field potentials. Electroenceph. clin. Neurophysiol., 1976, 41 : 460--466. Desmedt, J.E. Somatosensory cerebral evoked potentials in man. In: A. RSmond (Ed.), Handbook of Electroencephalography and Clinical Neurophysiology, Vol. 8. Elsevier, Amsterdam, 1971: 55--82. Desmedt, J.E. and No~l, P. Average cerebral evoked potentials in the evaluation of the sensory nerves and of the central somatosensory pathway. In: J.E. Desmedt (Ed.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 2. Karger, Basel, 1973: 352--371.
381 Goldie, W.D., Chiappa, K.H. and Young, R.R. Brainstem auditory evoked responses in the evaluation of deeply comatose patients. Neurology (Minneap.), 1979, 29: 581. Goff, G.D., Matsumiya, Y., Allison, T. and Goff, W.R. The scalp topography of human somatosensory and auditory evoked potentials. Electroenceph. clin. Neurophysiol., 1977, 42: 57--76. Iragui-Madoz, V.J. and Wiederholt, W.C. Far-field somatosensory evoked potentials in the cat: correlation with depth recording. Ann. Neurol., 1977, 1 : 569--574. Jones, S.J. Dipolar properties and peripheral origin of the first component in the human somatosensory evoked response. J. Physiol. (Lond.), 1977, 271: 56P--57P. Kritchevsky, M. and Wiederholt, W.C. Short latency somatosensory evoked potentials. Arch. Neurol. (Chic.), 1978, 35: 706--711. Starr, A. Sensory evoked potentials in clinical disorders of the nervous system. Ann. Rev. Neurosci., 1978, 1: 103--127. Stockard, J.J. and Rossiter, V.S. Clinical and pathological correlates of brainstem auditory response abnormalities. Neurology (Minneap.), 1977, 27: 316--325. Stockard, J.J., Rossiter, V.S., Wiederholt, W.C. and Kobayashi, R.M. Brainstem auditory evoked responses in suspected central pontine myelinolysis. Arch. Neurol. (Chic.), 1976, 33: 726--728. Wiederholt, W.C. and Iragui-Madoz, V.J. Far-field somatosensory potentials in the rat. Electroenceph. clin. Neurophysiol., 1977, 42: 456--465. Yamada, T., Kimura, J., Young, S. and Powers, M. Somatosensory~evoked potentials elicited by bilateral stimulation of the median nerve and its clinical application. Neurology (Minneap.), 1978, 28: 218--223. Zv~ina, E. and Kredba, J. The significance of investigating somatosensory cerebral evoked potentials in brachial plexus injuries. Cs. Neurol. Neurochir., 1977, 40- 240--250.
375
SHORT LATENCY SOMATOSENSORY EVOKED POTENTIALS FROM RADIAL, MEDIAN AND U L N A R N E R V E STIMULATION IN MAN 1 J.S. GRISOLIA and W.C. WIEDERHOLT
Veterans Administration Medical Center, San Diego, Calif. 92161 and Department o f Neurosciences, University o f California at San Diego, School o f Medicine, La Jolla, Calif. 92093 (U.S.A.) (Accepted for publication: June 12, 1980)
Short latency components of the somatosensory evoked potential (SEP) have been recorded in humans (Desmedt 1971; Cracco and Cracco 1976; Goff et al. 1977; Wiederholt and Iragui-Madoz 1977; Anziska et al. 1978). Anatomical correlates of these components have been tentatively assigned on the basis of latency and scalp distribution in humans (Kritchevsky and Wiederholt 1978) supplemented b y depth recordings and lesion experiments in animals (Iragui-Madoz and Wiederholt 1977; Wiederholt and Iragui-Madoz 1977; Arezzo et al. 1979). The clinical utility of short latency auditory evoked potentials has been well demonstrated (Stockard et al. 1976; Stockard and Rossiter 1977; Starr 1978). Short latency SEPs have been examined in multiple sclerosis (Anziska et al. 1979), in coma (Goldie et al. 1979; Anziska and Cracco 1980), and o t h e r CNS lesions (Yamada et al. 1978; Anziska and Cracco 1979). To enhance the clinical utility of short latency SEP and to further investigate its underlying generators in humans, we have examined SEPs in normal volunteers after stimulation of several peripheral nerves in the forearm. Implications for diagnosis of diseases of both the central and peripheral nervous system will be considered.
1 Supported by the Medical Research Service of the Veterans Administration.
Method Ten normal volunteers (7 men, 3 women, aged 20--27 years) were examined. This study was approved b y the University of California and Veterans Administration Committees on Investigations Involving Human Subjects. Informed consent was obtained from all participants. Stimulating needle electrodes (platinum alloy, 12 mm long, 0.3 mm diameter) were inserted subcutaneously to overlie the median, ulnar and superficial branch of radial nerves at the wrist with cathode placed 1 cm proximal to anode. A stimulator delivered square wave pulses of 0.2 msec duration at a frequency of 4/sec through a stimulus isolation unit. Stimulus voltage was adjusted to produce a small muscle twitch for ulnar and median nerve stimulation, while radial nerve stimulation voltage was adjusted to equal the subjective intensity of stimulation at the other sites. In most cases, stimulus voltage was a b o u t 4 times the least detectable stimulus intensity. SEPs were recorded with platinum alloy needle electrodes placed subcutaneously at F3, F4, C3 and C4 (International 10-20 system) referenced to needle electrodes placed subcutaneously in the forehead (FPz) and in the right knee. A ground electrode was placed in the skin of the right forearm. O u t p u t from the recording electrodes went to a differential amplifier with a 10--3000 c/ sec bandpass (50% attenuation at 8 c/sec and
376
J.S. G R I S O L I A , W.C. W I E D E R H O L T
3000 c/sec) and was fed on-line to a laborat o r y computer and/or stored on FM magnetic tape for later analysis. All amplifier channels were calibrated with a 20 pV signal of 10 msec duration. The computer averaged a total of 1500 sweeps at a sampling rate of 1 point for 127 psec which has been shown to give equivalent results to a sampling rate of 40 psec per point (Kritchevsky and Wiederholt 1978). Sweep duration was 80 msec. Averages were displayed on an oscilloscope screen and were plotted on an electrostatic matrix plotter. In all recordings and tracings, an upward deflection signifies relative positivity in grid one of the differential amplifier. Peak latencies and amplitudes were measured on traces from the plotter. Amplitudes were measured on both of the duplicate traces in each subject and data from all subjects were pooled {Table II). All measurements were made on traces from C3 or C4 referenced to knee, except for measurements made on N19 and P20. These latter components were measured on recordings from F3 or F4 referenced to knee because P20 was seen most reliably at these locations. Means and standard errors were calculated and compared by Student's t-test for different stimulation sites. Median, ulnar, and radial nerves were each stimulated unilaterally and bilaterally. In addition, several nerves within one limb were stimulated simultaneously in the following combinations: median and radial; radial and ulnar; median and ulnar; and median, radial,
and ulnar. For unilateral stimulation, the right arm was used in 7 subjects and the left in three, determined by the subject's preference. SEP components were specified by polarity and average peak latency in conformance with the recommendations of the Committee on Methods of the International Symposium on Cerebral Evoked Potentials in Man, Brussels, 1974.
Results
Typical traces of short latency SEPs from all stimulation combinations are presented in Figs. 1 and 2. Latency and amplitude characteristics of the different short latency components are presented in Tables I and II. Unilateral and bilateral median nerve stimulation yielded 6 early potentials (P10, P12, P14, N19, P20, P23) as described previously (Kritchevsky and Wiederholt 1978) 2. Bilateral stimulation significantly increased the amplitudes of components in P10, P14, and N19 (P < 0.005, P <: 0 . 0 2 , P < 0.005, respectively) but not those of P20 and P23. The amplitude increase of P12 was not significant due to small sample size. With ulnar nerve stimulation, a similar SEP
2 P10, P14 a n d N19 were i d e n t i f i e d w i t h s t i m u l a t i o n o f each o f t h e 3 nerves in all subjects. P12 was seen in six, a n d P20 a n d P23 were p r e s e n t in nine.
TABLE I Peak latency (msec) o f SEP with radial, m e d i a n and ulnar nerve s t i m u l a t i o n . P10, P12, P14 a n d P23 latencies were P20 were m e a s u r e d f r o m t h e contralateral frontal e l e c t r o d e (F3 or F4) r e f e r e n c e d to knee. (Ten n o r m a l subjects.
P10 P12 P14 N19 P20 P23
Unilateral median
Unilateral radial
Unilateral ulnar
Bilateral median
Bilateral ulnar
10.1 12.3 14.2 18.7 20.2 23.1
10.1 12.7 14.9 18.6 20.2 23.7
10.0 12.7 15.0 19.2 21.0 22.9
10.0 12.0 14.2 18.7 20.3 23.2
10.2 12.0 14.6 18.9 20.4 23.2
+ 0.27 -+0.38 -+ 0.43 -+ 0.35 -+ 0.43 -+ 0.38
-+ 0.23 -+0.46 -+ 0.35 + 0.45 + 0.53 -+ 0.48
+ 0.24 -+0.46 -+ 0.58 -+ 0.45 -+ 0.44 -+ 0.45
-+ 0.26 -+0.43 -+ 0.45 + 0.27 -+ 0.26 -+ 0.51
-+ 0.25 -+0.45 -+ 0.44 +- 0.36 + 0.38 -+ 0.51
S H O R T L A T E N C Y SEPs
377 MEDIAN +
M E D I A N + RADIAL BILATERAt MEOIAN-
BILATERAL RAOIAL
!
,,
BILATERALULNAR
ULNAR
/% ,,~ I'i
J I i' !: \ lO MSEC
-
UNILATERAL MEDIAN
UNILATERAL RADIAL
UNILATERAL ULNAR m
PISEC •
~l
, ~ ,
.
RADIAL + ULNAR
f:?>:j::5;:*
M E D I A N + RADIAL +
ULNAR
eI
/
Fig. 1. Early SEP c o m p o n e n t s w i t h median, radial, and ulnar nerve stimulation. All traces are from the same subject. T w o successive averages of 1 5 0 0 s w e e p s are displayed. Upper traces are F3 referenced to right knee; l o w e r traces are C3 refereneed to right knee.
pattern was seen except that P10 was frequently bilobed and significantly smaller in amplitude compared to median nerve stimulation (P < 0.005). Bilateral stimulation resulted in increased amplitude and clarity of the potentials although this was not reflected in a significant increase in amplitude except for N19 {P < 0.02).
fJ PW'
Fig. 2. Early SEP c o m p o n e n t s w i t h s i m u l t a n e o u s nerve stimulation. T w o successive averages of 1 5 0 0 s w e e p s from the same subject as Fig. 1 are s h o w n . Upper traces are F3 referenced to right knee; lower traces are C3 referenced to right knee.
Radial nerve stimulation elicited a pattern of potentials similar to that seen with either median nerve or ulnar nerve stimulation. P10
measured on potentials recorded from C3 or C4, referenced to knee, on the side contralateral to stimulation. N 1 9 and Values are means _+ S.E.) Bilateral radial
Median + radial
Median + ulnar
Radial + ulnar
Median + ulnar + radial
10.2 13.2 14.8 18.7 20.6 23.2
10.0 12.5 14.3 19.3 20.7 23.5
10.3 12.6 14.7 18.7 20.9 23.2
10.6 13.0 15.0 19.5 20.6 23.9
10.3 12.7 14.8 18.9 20.9 23.5
+ 0.25 +0.85 -+ 0 . 4 8 _+0.55 -+ 0 . 5 2 -+ 0 . 4 6
+ 0.27 _+0.46 -+ 0 . 3 3 _+0.32 -+ 0 . 5 9 -+ 0 . 3 7
-+ 0 . 2 6 _+0.30 _+ 0 . 4 0 +0.41 _+0 . 5 2 _+ 0 . 5 8
+ 0.18 +0.37 _+ 0 . 3 9 -+0.52 + 0.47 _+0 . 6 4
-+ 0 . 2 6 -+0.63 _+0 . 3 9 -+0.54 -+ 0 . 5 5 _+0 . 6 9
378
J.S. G R I S O L I A , W.C. W I E D E R H O L T
T A B L E II A m p l i t u d e s (pV) o f SEP with radial, m e d i a n , and ulnar nerve s t i m u l a t i o n . Each c o m p o n e n t was m e a s u r e d f r o m its ont u d e s were m e a s u r e d o n p o t e n t i a l s r e c o r d e d f r o m C3 or C4, r e f e r e n c e d to knee, o n t h e side contralateral t o stimulasubjects. Values are m e a n s -+ S.E.)
P10 P12 P14 N19 P20 P23
Unilateral median
Unilateral radial
Unilateral ulnar
Bilateral median
Bilateral radial
2.4 0.43 1.13 3.74 1.37 1.85
0.81 0.46 1.03 1.69 0.73 0.79
1.19 0.80 0.85 1.89 1.14 1.12
4.49 0.54 1.92 6.03 1.61 1.92
1.23 0.63 0.96 1.96 0.93 0.93
+0.25 -+0.07 -+0.08 -+ 0.33 -+ 0.23 -+0.69
-+0.09 -+0.11 -+ 0.11 -+ 0.21 -+ 0.14 -+0.11
was significantly smaller in amplitude compared with the P10 of median nerve stimulation ( P ( 0 . 0 0 5 ) . Bilateral stimulation improved clarity of potentials without a significant increase in amplitude. In individual subjects, P12 was often larger and better defined with radial or ulnar nerve stimulation than with median nerve stimulation. The P12 amplitude was significantly larger only with ulnar nerve stimulation (unilateral stimulation, P ~ 0.01; bilateral stimulation, P < 0.005). Simultaneous unilateral stimulation of several nerves produced higher amplitudes of some components b u t with some sacrifice in clarity (see Fig. 2). SEPs from median nerve stimulation were compared with SEPs from all other stimulus combinations by paired ttest for amplitude of each component. With simultaneous median, radial and ulnar nerve stimulation, P10 was significantly larger (P 0.005} as was N19 ( P < 0.01). Increases in amplitudes of other components were not statistically significant.
Discussion Short latency SEP components were recorded after stimulation of median, ulnar and radial nerves, singly or in combination. Although the wave forms with each stimulation site were similar, there were significant differences which may have both theoretical
-+0.22 -+0.10 +0.14 -+ 0.18 -+ 0.16 +0.22
_+0.43 -+0.06 -+0.33 -+ 0.37 -+ 0.39 -+0.85
-+0.27 -+0.12 -+0.20 -+ 0.27 -+ 0.15 -+0.15
and clinical importance. With stimulation of the superficial branch of radial nerve, a pure sensory nerve, P10 was low in amplitude and frequently was bilobed. Ulnar~lerived P10 was intermediate in amplitude between radial and median. P10 has been localized to brachial plexus fibers b y recordings from supraclavicular electrodes (Jones 1977) and b y its preservation despite complete C5-T1 r o o t avulsion (Anziska and Cracco 1979). The strikingly larger amplitude of P10 with median nerve stimulation may partly result from activity in antidromically stimulated m o t o r fibers. Beyond P10, there appear to be no significant differences between radial, ulnar and median
S H O R T L A T E N C Y SEPs
379
set to peak e x c e p t N19, w h i c h is m e a s u r e d f r o m t h e peak o f P14 to the t r o u g h o f N19. P10, P12, P14, and P23 amplition. N19 and P20 were m e a s u r e d f r o m t h e c o n t r a l a t e r a l frontal e l e c t r o d e (F3 or F4) r e f e r e n c e d to knee. (Ten n o r m a l
Bilateral ulnar
Median + radial
Median + ulnar
Radial + ulnar
Median + ulnar + radial
1.87 0.73 1.12 2.50 1.56 1.44
2.79 0.47 1.02 3.21 1.13 1.77
2.30 0.53 1.07 3.11 1.61 2.00
1.94 0.55 1.11 2.82 0.86 1.93
3.60 0.74 1.37 4.83 1.73 2.47
+ 0.33 + 0.21 + 0.20 +__0.26 -+0.26 -+ 0.46
-+ 0.39 -+ 0.10 + 0.11 +- 0.43 -+0.36 -+ 0.57
-+ 0.26 + 0.09 -+ 0.18 __+0.41 -+0.38 -+ 0.55
times less well defined. The slightly different latencies and morphologies of certain ulnarderived components probably explain the slurring of P12 and P14 when ulnar nerve is stimulated in combination with the others. Desmedt and Noel (1973) have called attention to the diagnostic value of cortical SEP in peripheral lesions, and other workers have also used cortical SEP in diagnosis of brachial plexus injuries ( Z v ~ i n a and Kredba 1977). Recognition of early SEP components
C7
C8
IT1
ULNAR NERVE
Fig. 3. Brachial plexus fibers activated by m e d i a n , radial, a n d ulnar nerve s t i m u l a t i o n a t the wrist. Affere n t s o m a t o s e n s o r y fibers are s h o w n in black. M o t o r fibers w h i c h are a n t i d r o m i c a l l y activated are s h a d e d .
+ 0.10 -+ 0.09 -+ 0.14 __+0.46 -+0.09 -+ 0.80
+ 0.30 + 0.25 -+ 0.66 __+0.50 __+0.20 + 0.49
following median, radial and ulnar stimulation will be particularly helpful in anatomical diagnosis of peripheral nerve and brachial plexus disorders. As shown in Fig. 3, the afferent and efferent pathways from the 3 stimulation sites at the wrist embrace every major subdivision of the brachial plexus except the C5 root. Median nerve stimulation at the wrist activates somatosensory fibers which pass along the lateral cord to reach the upper and middle trunks and then enter the spinal cord through the posterior C6 and C7 roots. The antidromic m o t o r activity traverses the medial cord and lower trunk to enter through the anterior C8 and T1 roots. Radial somatosensory impulses travel up the posterior cord and upper trunk to reach C6. Ulnar somatosensory impulses enter the medial cord and lower trunk to reach C8, while the antidromic m o t o r c o m p o n e n t crosses the medial cord and lower trunk to reach T1. The short latency SEP patterns with the 4 most c o m m o n brachial plexus injuries are readily predicted from inspection of Fig. 3. Injuries to the upper trunk will delay or attenuate all components of the median and radial
380 stimulation. Radial
Summary Short latency somatosensory evoked potentials (SEPs) were elicited by stimulation at the wrist of median, radial, and ulnar nerves, singly or in combination, using normal subjects. Amplitude of P10 was strikingly lower with radial stimulation than with median stimulation, while ulnar
J.S. GRISOLIA, W.C. WIEDERHOLT of ra.dial, ulnar, and median stimulation for localizing peripheral lesions derives from the distinct anatomical pathways of the stimulated fibers through the brachial plexus and from the separable m o t o r and sensory components of P10. SEP is less invasive than EMG; this fact, plus its freedom from sampiing error, make it potentially more suitable than conventional EMG for sequentially following a patient's clinical course.
R~sum~ Potentiels dvoquds somatosensoriels de latence courte par stimulation des nerfs radial, mddian et ulnaire chez l ' h o m m e Les potentiels ~voqu~s somatosensoriels (PES) de latence courte ont ~t~ provoqu~s par stimulation au poignet des nerfs m~dian, radial et ulnaire, isol~ment ou de faqon conjugu~e, chez des sujets normaux. L'amplitude de P10 est n e t t e m e n t plus faible avec la stimulation radiale qu'avec la stimulation m~diane tandis que le P10 par stimulation ulnaire est interm~diaire quant ~ son amplitude. Cette difference refl~te probablement la d~charge antidromique des fibres motrices contenues dans le nerf m~dian compar~es ~ la branche superficielle du nerf radial qui est entibrement sensitif. Au
SHORT LATENCY SEPs The authors gratefully acknowledge the technical assistance of Mr. Byron Budnick.
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