The effect of stimulus frequency on post- and pre-central short-latency somatosensory evoked potentials (SEPs)

86

Electroencephalography and clinical Neurophysiology , 1990, 77:86-92

Elsevier Scientific Publishers Ireland, Ltd. EVOPOT 02382

The effect of stimulus frequency on post- and pre-central short-latency somatosensory evoked potentials (SEPs) X. Delberghe, N. Mavroudakis, D. Zegers de Beyl and E. Brunko * Service de Neurologie, HOpital Erasme, Brussels (Belgium), and * Unit6 de Recherche sur le Cerveau, Facult6 de M6decine, Universit6 Libre de Bruxelles, Brussels (Belgium)

(Accepted for publication: 1 July 1989)

Summary We assessed the influence of the stimulus frequency on short-latency SEPs recorded over the parietal and frontal scalp of 26 subjects to median nerve stimulation and 16 subjects to digital nerve stimulation. When the stimulus frequency is increased from 1.6 Hz to 5.7 Hz, the amplitude of the N13 potential decreases whereas the P14 remains stable. The amplitude of the N20 is not changed significantly whereas the P22, the P27 and the N30 decrease significantly. In 50% of the subjects 2 components can be seen within the frontal negativity that follows the P22: an early 'N24' component, which is not affected by the stimulus rate, and the later N30, which is highly sensitive to the stimulus frequency. The distinct amplitude changes of the N20 and P22 with increasing stimulus frequency is one among other arguments to show that these potentials arise from separate generators. Key words: Evoked potentials; Somatosensory evoked potentials

P u b l i s h e d d a t a d e a l i n g with the effects of the stimulus frequency on short-latency somatos e n s o r y e v o k e d p o t e n t i a l s (SEPs) are rare a n d s o m e t i m e s c o n t r a d i c t o r y . S t i m u l u s frequencies v a r y c o n s i d e r a b l y in p u b l i s h e d studies: G o f f et al. (1962) used an i n t e r s t i m u l u s interval of 4 . 5 - 6 . 0 sec, D e s m e d t a n d C h e r o n (1980) an interval of 0 . 2 - 0 . 8 sec, a n d stimulus frequencies of 2 H z ( K i n g a n d G r e e n 1979), 5.1 H z (Willis et al. 1984) a n d 10 H z (Sebel et al. 1987) are e x a m p l e s of c u r r e n t l y used stimulus c o n d i t i o n s . K r i t c h e v s k y a n d W i e d e r h o l t (1978) a n d W i e d e r h o l t et al. (1982) state that the a m p l i t u d e s of cortical s h o r t - l a t e n c y SEPs are h a r d l y c h a n g e d if the stimulus r a t e d o e s n o t exceed 10 Hz. Small et al. (1980), however, n o t e d that increasing the stimulus rate f r o m 1 to 10 H z i n d u c e d p r o m i n e n t changes of the cortical SEP. Jones (1981) r e p o r t s changes of shape a n d

Correspondence to: D. Zegers de Beyl, Service de Neurologie, H6pital Erasme, Route de Lennik 808, B-1070 Brussels (Belgium).

a m p l i t u d e when the stimulus f r e q u e n c y is increased up to 18 H z a n d this is c o n f i r m e d b y K i n g a n d G r e e n (1979) for the f r e q u e n c y of 20 Hz. C h i a p p a a n d R o p p e r (1982) suggest an o p t i m a l stimulus r a t e of 5 Hz. A l l these studies, however, have neglected the S E P c o m p o n e n t s t h a t are rec o r d e d in front of the central sulcus a n d are o n l y c o n c e r n e d with the p o s t - c e n t r a l ( p a r i e t a l ) SEP. Some of the r e p o r t e d d a t a a r e b a s e d on r e c o r d i n g with f r o n t a l reference, resulting in a trace in w h i c h post- a n d p r e - c e n t r a l SEPs are mixed. SEPs r e c o r d e d over the post- a n d p r e - c e n t r a l scalp, however, m o s t p r o b a b l y originate from multiple i n d e p e n d e n t g e n e r a t o r s ( D e s m e d t a n d C h e r o n 1981; M a u g u i r r e et al. 1983; D e i b e r et al. 1986; D e s m e d t et al. 1987). T h u s the stimulus f r e q u e n c y might have different effects on p a r i e t a l a n d frontal SEPs. T h e a i m of this s t u d y is to e v a l u a t e the effect of 3 stimulus frequencies, chosen w i t h i n the r a n g e of c u r r e n t l y r e p o r t e d rates, o n the a m p l i t u d e a n d latencies of s h o r t - l a t e n c y SEPs r e c o r d e d over the neck a n d the p a r i e t a l a n d frontal scalp.

0168-5597/90/$03.50 © 1990 Elsevier Scientific Publishers Ireland, Ltd.

EFFECT OF STIMULUS FREQUENCY ON SEP

Subjects and methods The data were collected from 26 selected normal adults (10 males and 16 females) of 19-75 years (mean age: 33.0 + 15.8 years). All subjects were in good health, free from neurological, psychiatric or medical disease, and gave informed consent. Mental state and gait were normal and the criteria for selection involved ability to relax fully in order to minimize muscle or eyeblink interference during recording. The subjects lay comfortably on a couch with a constant room temperature of 24 ° C. The skin temperature of the stimulated upper limb was kept constant and checked several times during the recording session. SEPs were elicited in all subjects by right median nerve stimulation delivered through a pair of cup electrodes just above the wrist; for 16 of these subjects (9 males and 7 females; mean age: 28.9 + 6 . 2 years) additional studies were performed by stimulating the digital nerves of the right index and middle fingers through 2 pairs of ring electrodes. The proximal electrode of each pair was the cathode. The stimuli were square electrical pulses (0.2 msec duration) of constant current at an intensity eliciting a minimal thumb twitch when applied at the wrist or at 3 times the subjective sensory threshold for finger stimulation. Stimulus rates of 1.6 Hz, 3.1 Hz and 5.7 Hz were used for median nerve stimulation and 1.6 Hz and 5.7 Hz for finger stimulation. The stimulus intensity was kept rigorously constant throughout each experiment and the stimulated limb was kept immobile. To ensure that no minor displacement of the stimulation electrodes occurred, the sensory threshold for the stimulus was checked at the beginning, in the middle and at the end of the recordings. The afferent volley was recorded with silver cup electrodes over the spinous process of C6, the parietal scalp (70 mm laterally from the midline and 30 mm behind Cz) ipsi- and contralateral to stimulation and over the frontal scalp at F3 and F4. For median nerve stimulation, the potential of the median nerve at the elbow was recorded with a bipolar derivation. All electrodes were referred to linked earlobes and their impedance was maintained under 3000 $2. The trials were averaged with a Pathfinder II (Nicolet), anal-

87 ysis time was 50 msec, bin width was 100/~sec and overall bandpass was 5 H z - l . 5 kHz. Every experiment included 4 runs of 512 trials for each frequency. The reproducibility of the runs was assessed by superimposing the traces on the screen. Each experiment began and ended with 2 separate runs at 3.1 Hz. For the intermediate runs, the sequence of stimulus frequencies followed a random-like pattern. The traces were stored on floppy disk for later off-line analysis and written out on a system-integrated X - Y plotter. Latencies and amplitudes were measured independently by two of us on the traces obtained by electronic summation of the reproducible runs for each frequency with system-integrated cursors. SEP components recorded over the scalp were measured on the traces referred to earlobes and on traces obtained after electronic subtraction of the ipsilateral parietal trace from the contralateral parietal and frontal traces. SEP components were labeled from the positive (P) or negative (N) polarity and their modal peak latency. The following parameters were determined for each frequency after median nerve or finger stimulation. Amplitudes

Latencies

Elbow

median nerve potential

Neck

N13 (from baseline)

Nll (onset); N13 (peak)

Parietal scalp

P14 (from baseline) N20 * and P27 * (from baseline)

P14 (onset) N20 (onset and peak): P27 (peak)

Frontal scalp

P22 * (peak to peak); N30 * (from baseline) 'N24' (peak to peak)

P22 (peak); N30 (peak) 'N24' (peak)

* Components measured on traces with earlobe and on traces with ipsilateral parietal reference. Amplitudes were measured either from baseline or from the previous peaks. Baseline was determined from the segment following the stimulus artifact and preceding the onset of the far-field potentials after superimposing the contra- and ipsilateral parietal traces on the screen. If the superimposition of this segment was not satisfactory (as judged by visual inspection on the screen)

88

X. D E L B E R G H E ET AL.

the contralateral parietal and frontal traces were superimposed. The distribution of the amplitudes of the SEPs was shown to be normal according to the Kolmogorov-Smirnov goodness of fit test. To determine whether the change in stimulus frequency produced significant changes of the amplitudes and latencies of the SEP, the results were examined by a repeated measures analysis of variances ( M A N O V A ) for median nerve stimulation and pairwise comparisons (t test) for digital nerve stimulation. If for median nerve stimulation a significant change was detected by MANOVA, pairwise comparisons were performed to determine at what stimulus frequency the change

Fingers

became significant. These pairwise comparisons employed the analysis of contrast.

Results

Effects of stimulus frequency on ampfitudes The SEPs of 2 subjects recorded with stimulus frequencies of 1.6 Hz, 3.1 Hz and 5.7 Hz are shown in Figs. 1 and 2. The components consistently identified are indicated with black arrows and labeled: N13 (neck), P14 far-field (FF), N20 and P27 over the parietal scalp, P22 and N30 over the frontal scalp. A negative potential which occurs just after the P22 and well before the N30 on

Fingers

Freq.: 1.6 Hz

Freq.: 5,7 Hz

o

P22

: ~

N30

Pare

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I 20

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Fig. 1. Two superimposed averages of SEPs of a 34-year-old man with digital nerve stimulation at frequencies of 1.6 Hz (left side) and 5.7 Hz (fight side). The lower 3 traces recorded over contra- and ipsilateral parietal (Pare; Pail) scalp and over F3 (Frc) are referred to linked earlobes (ear ref.), the upper 2 traces are referred to the ipsilateral parietal (Pari ref.) electrode.

EFFECT OF STIMULUS F R E Q U E N C Y ON SEP

Rt.med.

89

n. Freq. (Hz)

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Fig. 2. Superimposed SEPs of a 28-year-old woman with right median nerve (Rt. med. n.) on the left and digital nerve stimulation on the right; stimulus frequencies (Freq. Hz) are 1.6, 3.1 and 5.7 Hz on the left and 1.6 and 5.7 Hz on the right. The white triangle below the frontal trace (Frc) indicates the 'N24.' Note the stability of the N20 (Pare) and of the 'N24.' In this case, there was no evidence of P22 decrease at a stimulus rate of 5-7 Hz.

the frontal trace was seen in 13 subjects after median nerve stimulation and in 8 subjects after digital nerve stimulation. We refer to this potential (which we indicate with a white triangle in Fig. 2) as 'N24.' The results of the mean amplitudes of SEPs at different stimulation frequencies are shown in Table I: the P14 far-field is stable and its stability contrasts with the significant attenuation of the N13 (over the neck). The parietal N20 is stable despite the increase of the stimulus rate and its stability (both with median and digital nerve stimulation) contrasts with the significant attenuation of the P22 (over F3; Fig. 1). The parietal P27 and frontal N30 are both very sensitive to the stimulus rate. The increase of the stimulus frequency dissociates the frontal ' N 2 4 ' and the N30: when the frontal N30 is attenuated in a striking 'way at 5.7 Hz (Fig. 2), the ' N 2 4 ' is not affected significantly by the stimulus rate (Table I

and Fig. 2). These results are confirmed when N20, P22, P27 and N30 are measured on traces referred to the ipsilateral parietal electrode (Table II). However, in 7 of the 26 subjects with median nerve stimulation the ipsilateral parietal trace shows a residual P22 or N30 (or both) with reduced amplitude; this never occurs with digital nerve stimulation. These 7 traces were not included in the analysis of the data with ipsilateral parietal electronic subtraction (thus Table II shows the results of 19 instead of 26 subjects with median nerve stimulation). As far as latencies are concerned the mean peak latencies of the N13 and N20 do change significantly when the rate of median nerve stimulation is increased. Digital nerve stimulation confirms the significant increase of the N13 latency at 5.7 Hz. All other latencies remain stable and the central conduction time (CCT), whether determined from onset ( N I l - N 2 0 ) or p e a k

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X, DELBERGHE ET AL.

TABLE I

TABLE IIl

Mean amplitude (+- 1 S.D.) of SEPs referred to earlobes of 26 normal subjects with median nerve stimulation and of 16 normal subjects with digital nerve stimulation at different frequencies.

Mean latencies ( + 1 S.D.) of SEPs to median nerve stimulation of 26 normal subjects and to digital nerve stimulations of 16 normal subjects at different frequencies.

1.6 Hz (~v)

3.1 Hz (~v)

Nerve stimulation Elbow 19.20_+10.01 N13 1.24_+ 0.44 P14 * 0.71_+ 0.22 N20 * 1.19_+ 0.65 P22 0.68 _+ 0.43 P27 * 1.70 +- 1.29 N30 * 1.62_+ 0.87 N24 * * 1.08_+ 0.52 Digital stimulation N13 0.69+P14 * 0.27+N20 * 0.89_+ P22 0.40_+ P27 * 1.05 _+ N30 * 1.27_+ N24 * * * 0.90_+

5.7 Hz (~v)

19.10_+11.11 19.80_+11.11 1.13_+ 0.37 1.02+- 0.39 0.67+- 0.23 0.64_+ 0.21 1.16+- 0.68 1.09_+ 0.66 0.62_+ 0,34 0.54+- 0.44 1.47+- 1.28 1.06_+ 0.93 1.16_+ 0,82 0.72+- 0.53 1.15_+ 0,61 1.05+ 0.46

0.21 0.89 0.48 0.19 0.44 0.63 0.62

0.60_+ 0.27_+ 0.79_+ 0.26_+ 0.51+ 0.57+0.75+-

1.6 Hz (msec)

P

0.17 0.84 0.43 0.18 0.34 0.47 0.55

NS <0,005 NS NS <0.03 <0.001 <0.0001 NS <0,025 NS NS <0,001 < 0.005 <0.001 NS

* Amplitude measured from baseline. ** n = 1 3 . *** n=8. P = significance for pairwise comparison between 1.6 and 5.7 Hz; NS = non-significant (P > 0.05).

Nerve stimulation Nil(onset) 10.38+0.79 N13(peak) 13.34+1.02 N20(onset) 16.69+-1.02 N20(peak) 18.88+1.22 P22(peak) 19.93-+1.53

3.1 Hz (msec)

5.7 Hz (msec)

P

10.39+0.79 13.39_+1.06 16.68+-0.96 18.98-+1.23 19.76-+1.62

10.45+_0.78 13.46+1.06 16.67_+1.09 19.08+-1.18 20.02-+1.53

NS <0.002 NS <0.03 NS

12.81_+0.63 16.16_+0.64 19.14_+0.80 21.99_+0.93 23.16+-2.01

NS < 0.001 NS NS NS

Digital stimulation N l l (onset) 12.74+-0.74 N13 (peak) 15.88_+0.64 N20 (onset) 19.05+-0.85 N20(peak) 21.90_+1.02 P22(peak) 23.01+-1.84

P = significance for pairwise comparison between 1.6 and 5.7 Hz; NS = non-significant (P > 0.05).

(N13-N20)

l a t e n c i e s ( Z e g e r s d e Beyl et al. 1988),

is n o t i n f l u e n c e d b y t h e s t i m u l u s f r e q u e n c y .

Discussion T o t h e b e s t o f o u r k n o w l e d g e , o u r w o r k is t h e only systematic study on the effects of the stimu-

TABLE II Mean amplitude (+ 1 S.D.) of SEPs referred to the ipsilateral parietal electrode to median nerve stimulation (19 subjects) and digital nerve stimulation (16 subjects) at different frequencies measured from baseline. 1.6 Hz (ttv) Nerve stimulation N20 0.75+0.58 P22 0.68 + 0.48 P27 1.63 + 1.32 N30 0.95 + 0.82 Digital N20 P22 P27 N30

stimulation 0.50 + 0.23 0.50 + 0.42 0.94 + 0.70 0.82+0.63

3.1 Hz (~v)

5.7 Hz (gv)

P

0.74-t-0.58 0.64+0.41 1.44+1.31 0.72 + 0.75

0.68+0.54 0.49+0.36 1.12+0.87 0.48 + 0.45

NS < 0.01 < 0.01 < 0.005

lus r a t e o n p o s t - a n d p r e - r o l a n d i c s h o r t l a t e n c y SEPs. Our results show that the increase of the s t i m u l u s f r e q u e n c y f r o m 1.6 t o 5.7 H z h a s d i f f e r e n t e f f e c t s o n t h e p a r i e t a l N 2 0 a n d t h e P 2 2 recorded over the frontal scalp: despite the similar l a t e n c i e s o f t h e s e p o t e n t i a l s , t h e m e a n P22 a m p l i t u d e is s i g n i f i c a n t l y t h o u g h m o d e r a t e l y a t t e n u a t e d while the mean N20 amplitude does not change. These findings noted with median nerve stimulation are the s a m e w h e n digital nerves are stimulated. Furthermore,

0.44+0.18 0.36+0.30 0.58+0.36 0.24+0.35

NS < 0.05 < 0.05 < 0.002

P = significance for pairwise comparison between 1.6 and 5.7 Hz; NS = non-significant ( P < 0.05).

measurements

of the ampli-

tudes of the cortical SEPs after electronic subtraction of the ipsilateral parietal

t r a c e , w h i c h ex-

cludes the u n c e r t a i n t i e s related to precise b a s e l i n e d e t e r m i n a t i o n , fully c o n f i r m t h e s e r e s u l t s . T h e s e d a t a are a further a r g u m e n t a m o n g the g r o w i n g number of observations which indicate that the

EFFECT OF STIMULUS FREQUENCY ON SEP

N20 and the P22 are generated by separate neural structures (Cracco 1972). There are at present several arguments in favor of independent generators. First, focal cortical and subcortical peri-rolandic lesions may abolish the post-rolandic N20-P27, whereas the pre-rolandic P22-N30 are still recorded, and vice versa (Maugui+re et al. 1983; Slimp et al. 1986). The second argument is based on experiments in which stimuli applied to the median nerve or the digital nerves are linked to voluntary finger movements (Cohen and Starr 1987; Cheron and Borenstein 1987): the N20 is not affected by voluntary finger movements, whereas the P22 and N30 potentials are markedly attenuated. Furthermore, digital multichannel recordings have elucidated some aspects of the relation between the N20 and the P22: the P22 is a focal pre-central event which occurs 2-3 msec after a more diffuse frontal P20 potential which is concomitant with the parietal N20 (Deiber et al. 1986; Desmedt et al. 1987). The frontal P20 potential is supposed to be the positive aspect of the N20- P20 dipole within the posterior border of the central fissure, whereas the P22 is a quite distinct phenomenon and its occurrence after the N20 and its distribution distinct from the P20 are compatible with the hypothesis of a pre-central radial dipole. Recently we have shown that during anesthesia with low concentrations of isoflurane, there is a dramatic increase of the mean P22 amplitude (mean increase: 100%) whereas the parietal N20 amplitude remains unchanged (Nogueira et al. 1989). These data and our present results of independent amplitude changes of the N20 and the P22 with the increasing stimulus rate are additional arguments in favor of independent neural generators of the N20 and P22. The amplitude changes of the P22 are modest when compared with the marked attenuation of the P27 (recorded over the parietal scalp) and the N30 (over the frontal scalp). Ot~r experiment illustrates the complex nature of the frontal negativity that follows the P22: whereas the N30 is highly sensitive to the stimulus frequency, the earlier negative peak 'N24' is not significantly changed. This dissociation of the 'N24' and the N30 indicates that the long lasting negativity recorded over

91

the frontal scalp following the P22 is the result of activity in at least two neural structures. The precise localization of these generators is still to be defined. The early negative frontal peak is not a constant feature: in our normative SEP data based on recordings from 75 normal subjects (mean age: 44 _+ 21.7 years), with median nerve stimulation at 3.1 Hz, the 'N24' peak was identified in only 40%. The 'N24' was noted as a constant feature by Jones and Power (1984) ('N22' in their terminology) and it is interesting that interfering tactile stimulation did not affect the amplitude of this potential although the P14, the N20 (their 'N19') and the N30 (their 'N29') potentials were significantly attenuated. More recently, the 'N24' potential was mentioned by Rossini et al. (1987) in 16 out of 20 normal subjects with a maximal amplitude 4 - 6 cm frontal to Cz and 2 - 4 cm lateral to the midline. Jones and Power (1984) speculated that the frontal 'N24' (' N22' in their terminology) is related to activation of I A fibers that project to cortical area 3a. We do not believe that there is any evidence in favor of this hypothesis, especially since we recorded the frontal 'N24' after selective digital nerve stimulation, which does not concern I A fibers. The latency changes are only minor for the range of frequencies chosen, and our results are in agreement with recent animal data which indicate that stimulus frequencies below 7 Hz only marginally affect the latencies of cortical SEPs in rats (Shaw 1987). The only significant latency change, both with median nerve and digital nerve stimulation, is the delay of the N13 peak recorded over the neck. The CCT, whether measured from onset or from peak latencies, is stable. In conclusion, the stimulus frequency of 5.7 Hz significantly attenuates the amplitude of most of the shortqatency SEPs recorded over the neck and the scalp. The amplitude of the N20, however, remains stable within the range of stimulus frequencies between 1.6 and 5.7 Hz and this stability contrasts with the significant attenuation of P22. Normative studies on short-latency SEPs should use stimulus frequencies that do not exceed 3,1 Hz, if the amplitudes of cortical SEPs are considered.

92

References Cheron, G. and Borenstein, S. Specific gating of the early somatosensory evoked potentials during active movement. Electroenceph. clin. Neurophysiol., 1987, 67: 537-548. Chiappa, K.H. and Ropper, A.H. Evoked potentials in clinical medicine. New Engl. J. Med., 1982, 306: 1205-1211. Cohen, L.G. and Starr, A. Localisation, timing and specificity of gating of somatosensory evoked potentials during active movement in man. Brain, 1987, 110: 451-467. Cracco, R.Q. Traveling waves of the human scalp-recorded somatosensory evoked response: effects of differences in recording technique and sleep on somatosensory and somatomotor responses. Electroenceph. clin. Neurophysiol., 1972, 33: 557-566. Deiber, M.P., Giard, M.H. and Maugui~re, F. Separate generators with distinct orientations for N20 and P22 somatosensory evoked potentials to finger stimulation. Electroenceph. clin. Neurophysiol., 1986, 65: 321-334. Desmedt, J.E. and Cheron, G. Central somatosensory conduction in man: neural generators and interpeak latencies of the far-field components recorded from neck and right o r left scalp and earlobe. Electroenceph. clin. Neurophysiol., 1980, 50: 382-403. Desmedt, J.E. and Cheron, G. Non-cephalic reference recording of early somatosensory potentials to finger stimulation in adult or aging normal man: differentiation of widespread N18 and contralateral N20 from the pre-rolandic P22 and N30 components. Electroenceph. clin. Neurophysiol., 1981, 52: 553-570. Desmedt, J.E., Nguyen, T.H. and Bourguet, M. Bit-mapped color imaging of human evoked potentials with reference to the N20, P27 and N30 somatosensory responses. Electroenceph. clin. Neurophysiol., 1987, 68: 1-19. Goff, W.R., Rosner, B.S. and Allison, T. Distribution of cerebral evoked responses in normal man. Electroenceph. clin. Neurophysiol., 1962, 14: 697-713. Jones, S.J. An 'interference' approach to the study of somatosensory evoked potentials in man. Electroenceph. clin. Neurophysiol., 1981, 52: 517-550. Jones, S.J. and Power, C.N. Scalp topography of human somatosensory evoked potentials: the effect of interfering tactile stimulation applied to the hand. Electroenceph. clin. Neurophysiol., 1984, 58: 25-36. King, D.W. and Green, J.B. Short latency somatosensory

X. DELBERGHE ET AL. potentials in human. Electroenceph. clin. Neurophysiol., 1979, 46: 702-708. Kritchevsky, M. and Wiederholt, W.C. Short-latency somatosensory evoked potentials. Arch. Neurol., 1978, 35: 706-711. Maugui~re, F., Desmedt, J.E. and Courjon, J. Astereognosis and dissociated loss of frontal or parietal components of somatosensory evoked potentials in hemispheric lesions: detailed correlations with clinical signs and computerized tomography scanning. Brain, 1983, 106: 271-311. Nogueira, M.C., Brunko, E., De Rood, M., Trempont, V. and Zegers de Beyl, D. Effects of isoflurane on pre- and postrolandic short-latency somatosensory evoked potentials. Neurology, 1989, 39: 1210-1215. Rossini, P.M., Gigli, G.L., Marciani, M.G., Zarola, F. and Caramia, M. Non-invasive evaluation of input-output characteristics of sensorimotor cerebral areas in healthy humans. Electroenceph. clin. Neurophysiol., 1987, 68: 88-100. Sebel, P.S., Erwin, C.W. and Neville, W.K. Effects of halothane and enflurane on far and near field somatosensory evoked potentials. Br. J. Anaesth., 1987, 59: 1492-1496. Shaw, N.A. The effects of stimulus rate on the cortical somatosensory evoked potential in the rat. Electromyogr. Clin. Neurophysiol., 1987, 27: 235-241. Slimp, J.C., Tamas, L.B., Stolov, W.C. and Wyler, A.R. Somatosensory evoked potentials after removal of somatosensory cortex in man. Electroenceph. clin. Neurophysiol., 1986, 65: 111-117. Small, D.G., Beauchamp, M. and Matthews, W.B. Subcortical somatosensory evoked potentials in normal man and in patients with central nervous system lesions. In: J.E. Desmedt (Ed.), Progress in Clinical Neurophysiology, Vol. 7. Karger, Basel, 1980: 190-204. Wiederholt, W.C., Meyer-Hardting, E., Budnick, B. and McKeown, K.L. Stimulating and recording methods used in obtaining short-latency somatosensory evoked potentials (SEPs) in patients with central and peripheral neurologic disorders. Ann NY Acad. Sci., 1982, 388: 349-358. Willis, J., Seales, D. and Frazier, E. Short-latency somatosensory evoked potentials in infants. Electroenceph. clin. Neurophysiol., 1984, 59: 366-373. Zegers de Beyl, D., Delberghe, X., Herbaut, A.G. and Brunko, E. The somatosensory central conduction time: physiological considerations and normative data. Electroenceph. clin. Neurophysiol., 1988, 71: 17-26.