Modification of cortical somatosensory evoked potentials during tactile exploration and simple active and passive movements

Electroencephalography and clinical Neurophysiology , 81 (1991) 216-223 © 1991 Elsevier Scientific Publishers Ireland, Ltd. 0924-980X/91/$03.50 A D O N I S 0924980X91000761

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Modification of cortical somatosensory evoked potentials during tactile exploration and simple active and passive movements J. Huttunen and V. H6mberg Neurological Therapy Center, Heinrich-Heine- University of Dfisseldorf 4000 Diisseldorf 13 (F. R. G.) (Accepted for publication: 15 September 1990)

Summary The present study compares the effects of different types of movement on median nerve somatosensory evoked potentials (SEPs) recorded from frontal, central and parietal electrodes. Test conditions included tactile exploratory movements, repetitive active and passive thumb movements and isometric contraction. All these conditions modified the SEPs in a similar manner. Parietal N20, P25, and N60, central P22 and N32, and frontal N25, N30 and P40 deflections were diminished, while later centro-parietal P40 and fronto-central N60 were unchanged. A small frontal P35 emerged during movement. The subcortical P14 was not changed in any of the conditions. The similar modulatory effects of simple active movements and of tactile exploration indicate that the modification of SEPs does not depend on the importance of proprioceptive feedback information for movement execution. As all modulatory effects were present also during passive movement, these observed effects are most likely to be caused by afferent occlusion in the ascending thalamo-cortical pathways or sensorimotor cortical cell populations. Key words: Somatosensory evoked potential; Movement; Sensorimotor integration

It is well known that active movement of the stimulated limb alters somatosensory evoked potentials (SEPs), the principal effect being amplitude reduction of early and middle-latency cortical components (Lee and White 1974; Hazemann et al. 1975; Coquery 1978; Abbruzzese et al. 1981; Jones 1981; Rushton et al. 1981; Cohen and Starr 1985, 1987; Cheron and Borenstein 1987; Jones et al. 1989). The mechanism of this phenomenon is unresolved. Both efferent control from sensorimotor cortex over afferent pathways (Cohen and Starr 1987) and afferent occlusive mechanisms (Rushton et al. 1981) have been suggested (see also Jones et al. 1989). Coquery (1978) proposed that during simple movements, which are relatively independent of guidance by sensory input, afferent signals might be irrelevant or even disturbing for movement execution and might therefore be actively suppressed by the central nervous system. Following this argument it could be expected that ascending impulses would not be suppressed during skilled movements which depend on sensory feedback information, e.g., during tactile exploratory movements. This proposition is also supported by the finding of Evarts and Fromm (1978) that rapid "ballistic" movements reduced the responsiveness of monkey cortical

Correspondence to: V. Hrmberg, Neurological Therapy Centre, Hohensandweg 37, 4000 Diisseldorf 13 (F.R.G.).

motor neurones to peripheral stimuli, whereas small precision movements requiring sensory feedback rather enhanced the cortical responses. The present study examines whether differential effects of different types of movements can be found in cortical SEPs in man. Therefore SEPs were recorded during simple repetitive thumb movements and during a tactile exploration task. A further objective was to reexamine the question (Rushton et al. 1981; Jones et al. 1989), of whether active and passive movements and isometric contraction have differential effects on SEPs.

Methods Eighteen right-handed healthy volunteers (3 males, 15 females, age range 19-43 years) were studied. Using bipolar surface electrodes, the right median nerve at the wrist was stimulated with constant voltage square-wave pulses of 0.2 msec duration. Stimulus intensity was adjusted to produce a clear thumb twitch without causing discomfort to the subject. The interstimulus interval (ISI) was either held constant at 1.21 sec (8 subjects) or was varied randomly between 0.49 and 1.59 sec (12 subjects, 2 of whom were tested also with the constant ISI); the latter condition was used to avoid synchronization of movement with the stimulation cycle. No differences were observed in the results obtained with these two ISis.

SEP M O D I F I C A T I O N

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During recording the subject lay on a bed with eyes closed and the stimulated hand lightly fixed on a flat support. Averaged responses were repeatedly obtained in a resting condition, randomly mixed with the test conditions. During rest the subject was instructed to relax and to ignore the stimuli. The following test conditions were presented in a random order: (1) Active alternating abduction-adduction movement of the right thumb (i.e., ipsilateral to stimulation). The subject perfomed alternating rapid abduction and adduction movements of the right thumb at a frequency of about 1 Hz. Verbal feedback by the experimenter was used to keep the movement as close to 1 Hz as possible. (2) Passive movement of the right thumb. The experi-

Ag/AgC1 disk electrodes were attached to scalp locations F3, C3 and P3, and to the left earlobe, which served as reference. The recording bandpass was 10 H z - 2 kHz. One hundred to 500 artefact-free responses were digitized at 5 k H z and averaged on-line. Analysis time was 100 msec including a 10 msec period preceding the stimulus. To ensure stability of stimulation during different conditions, the surface neurogram from the median nerve at the elbow was recorded simultaneously with the SEPs in 8 subjects. Muscular activity was monitored by surface E M G recording from thenar muscles, and the movements were monitored with a light-weight accelerometer attached to the dorsum of the thumb.

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Fig, 1. Effects of test c o n d i t i o n s on frontal, central a n d parietal SEPs in 1 subject. A b b r e v i a t i o n s : A c t = active t h u m b m o v e m e n t , E x p l = tactile exploration, Pass = passive t h u m b m o v e m e n t , l s o = i s o m e t r i c contraction. T o p rows: s i m u l t a n e o u s l y r e c o r d e d e l b o w n e u r o g r a m s .

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3 sec. The task was difficult and none of the subjects reported the number of coins correctly, the average error rate being 3070. Component latencies were measured to peaks of identified deflections. Amplitudes were calculated with respect to a baseline from 2 to 10 msec. Whenever a given deflection was so much attenuated in the test conditions that it could no longer be identified, its amplitude was assigned to be zero. Mean amplitudes of 2 records were calculated for each condition and used in statistical comparisons, which were performed using analyses of variance for repeated measures (Winer 1971). Individual differences between the test conditions and rest were assessed with a posteriori comparisons according to the Newman-Keuls method (Winer 1971).

menter moved the subject's thumb at a rate and amplitude similar to the active movement condition. Absence of active movement was ensured by E M G monitoring. (3) Isometric contraction. An attempted abduction of the right thumb by the subject was counteracted by the experimenter. The subject was instructed to keep the abducting force as constant as possible at about 3070 of m a x i m u m contraction force. (4) Tactile exploration. A series of 10 different coins were used. During recording these were repeatedly placed in a random order in the right hand of the subject, who actively touched the coins with the thumb, index and middle fingers. His task was to indicate afterwards, how m a n y different coins had been presented. Each coin could be explored for approximately

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Results Representative examples of i n d i v i d u a l wave forms in different c o n d i t i o n s are presented in Figs. 1 a n d 2, each showing responses from 1 subject. The following deflections were consistently identified at different electrode locations a n d were i n c l u d e d in the analysis: F3: P14, N25, N30, P40, N60; C3: P14, P22, N32, P40, N60; P3: P14, N20, P27, N34, P40, N60. As P40 a n d N60 do n o t necessarily share a c o m m o n generator at all recording locations, they were separately analysed for each electrode. Active a n d passive m o v e m e n t as well as tactile exp l o r a t i o n h a d qualitatively similar effects o n all frontal, central a n d parietal SEP c o m p o n e n t s . Isometric contraction p r o d u c e d only slight changes, which nevertheless were similar to those d u r i n g other test conditions. Over all test conditions, early c o m p o n e n t s before 40 msec were consistently modified in the same m a n n e r in all subjects, whereas some intersubject variability was observed in the later P40 a n d N60 deflections (see Figs. 1 a n d 2). T a b l e I s u m m a r i z e s the A N O V A s for each SEP c o m p o n e n t , i n c l u d i n g a posteriori c o m p a r i s o n s of individual test c o n d i t i o n s with rest. N o significant shifts in peak latencies were found. Frontal S E P deflections At F3, P14 was followed by a p r o m i n e n t N30 ( m e a n latency 31.6, S.D. 2.2 msec). In 12 subjects (67%) N30 was preceded by a separable N25 deflection (24.9 + 1.7

msec), in agreement with the recent report by Delberghe et al. (1990), who also separated a frontal N 2 4 from N30 in 50% of healthy subjects. I n Fig. 1 N25 a n d N30 can be seen as clearly separable deflections, whereas in Fig. 2 the separation is less obvious. Nevertheless, in this case also the negative p o t e n t i a l shift b e t w e e n 20 msec a n d 40 msec shows a bifid configuration, corres p o n d i n g to a n N25 a n d a n N30. N30 is followed b y P40 a n d N60, the latter of which is n o t detectable in the subject of Fig. 2. N o n e of the test c o n d i t i o n s affected frontal P14. With the exception of the isometric c o n d i t i o n , all test c o n d i t i o n s i n v a r i a b l y caused a r e m a r k a b l e d i m i n u t i o n of the frontal N30, whereas N25 was usually less affected (Fig. 1). N30 was often completely abolished in the test conditions, as in b o t h subjects of Figs. 1 a n d 2, a n d a small positive potential at 35 msec emerged instead. This deflection is designated as P35. Its m e a n latencies (33.5-35.4 msec for different test c o n d i t i o n s ) were significantly ( P < 0.01) shorter t h a n for P40 (42.4 + 3.6 msec) in the resting c o n d i t i o n , i n d i c a t i n g that the a p p e a r a n c e of P35 m a y n o t be considered as a simple increase of P40 amplitude. I n contrast to the a p p e a r a n c e of P35, the small frontal P40 was a t t e n u a t e d in the test conditions. This is clearly seen in Fig. 2, in which P40 is present at rest as a positive peak directly after 40 msec, b u t is a b s e n t in the test conditions. F r o n t a l N60 is present only in the subject of Fig. 1, in w h o m it a p p e a r s slightly b u t r e p r o d u c i b l y e n h a n c e d in the test conditions.

TABLE I Group means and standard errors (in parentheses) of SEP amplitudes at F3, C3 and P3 during different test conditions compared with rest. Significance levels are derived from the analysis of variance for repeated measures. N.S. = non-significant. N denotes the number of subjects in whom a given component was identified. The asterisks give the significant levels (*P < 0.05, **P < 0.01) when the test conditions were individually compared with the rest by the Newman-Keuls method. Unmarked values did not differ significantly from rest values. Rest

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0.4 (0.1) 1.6 (0.3) ** 1.1 (0.4) ** 0.4 (0.1) 0.7 (0.3) * 2.4 (0.3)

0.4 (0.1) 1.4 (0.2) ** 0.5 (0.2) ** 0.6 (0.2) * 0.7 (0.2) * 2.5 (0,5)

0.4 (0.1) 1.9 (0.3) ** 1.2 (0.2) ** 0.3 (0.1) 0.8 (0.3) 2.5 (0.4)

0.4 (0.1) 2.6 (0.5) 2.2 (0.5) ** 0.3 (0.1) 0.8 (0.3) 2.8 (0.6)

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0.4 (0A) 1.3 (0.4) ** 0.7 (0.2) * 3.8 (0.7) 1.7 (0.8)

0.5 (0.1) 1.8 (0.4) ** 1.4 (0.3) 3.5 (0.7) 2.1 (0.8)

0.4 (0.1) 2.7 (0.6) * 1.1 (0.3) 3.7 (0.6) 2.6 (0.8)

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0.4 (0.1) 1.9 (0.2) 2.6 (0.5) 0.2 (0.1) 2.6 (0.6) 1.9 (0.4)

0.5 (0.1) 1.5 (0.3) 1.2 (0.5) ** 0.6 (0.2) 2.3 (0.5) 1.1 (0.5) *

0.4 (0,1) 1.0 (0,2) ** 0.9 (0.3) ** 1.3 (0.3) 2.3 (0,5) 0.6 (0.3) **

0.4 (0.1) 1.4 (0.2) 1.3 (0.4) ** 1.2 (0.3) 2.3 (0.6) 0.9 (0.3) *

0.4 (0.1) 1.2 (0.2) 1.8 (0.3) 1.3 (0.4) 3.1 (0.7) 1.2 (0.4)

N.S. 0.01 0.001 N.S, N.S, 0.05

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Fig. 3. Effects of tactile exploration on parietal SEPs in 6 subjects with simultaneous elbow neurogram records. The SEP traces at P3 are shown on the left, thin curves representing responses during rest and thick curves during tactile exploration. The bottom pair of SEP curves show the respective grand averages of the 6 subjects. Neurograms during rest and exploration are depicted on the right so that the neurogram during exploration is shifted by 2.4 msec to the right to facilitate comparison. All individual curves are averages of at least 2 separate records, total N being 500-1000. Amplitude calibration: 2/~V for SEPs and 20 ~V for neurograms.

SEP MODIFICATION BY MOVEMENT The ANOVA showed that frontal N25, N30 and P40 were all significantly affected (Table I). In contrast, N60 was not significantly modified despite an apparent enhancement in several subjects. Central S E P components At C3 P14 (13.8 _+ 0.6 msec) was followed by P22 (22.9 + 2.0 msec), N32 (31.2 __+3.5 msec), P40 (40.6 _+ 3.3 msec) and N60 (57.2 + 7.8 msec) deflections. Again, PI4 was not affected in the test conditions. In contrast, P22 was markedly reduced in all subjects. N32 was likewise invariably attenuated in the test conditions and appeared sometimes totally abolished, as in Fig. 2 in the exploration condition. P40 and N60, which were more prominent at C3 than at F3, were clearly less or not at all changed. It must be emphasized, however, that these later potentials showed more intersubject variability than the earlier deflections: for example, in the subject of Fig. 1 the central N60 appeared diminished in the exploration condition, but in the subject of Fig. 2 it was unaltered despite clear attenuation of the preceding P22 and N32. The ANOVAs confirmed that the changes were significant for P22 and N32, but insignificant for P40 and N60 (Table I). Parietal S E P components At P3, P14 and N20 (19.1 _+ 0.8 msec) were followed by P25 (25.1 + 3.29 msec), N34 (34.7 + 4.1 msec), P40 (40.9 +_ 6.1 msec) and N60 (54.5 _+ 9.4 msec), the latter being poorly developed in some subjects (see Fig. 1). P14 was not altered by the test conditions. N20 often appeared little or not at all reduced, but measurement of the amplitude revealed slight reductions in most of the subjects. P25 was remarkably attenuated in all subjects. N34 was identified only in a minority of subjects, and it was either unchanged (Figs. 1 and 2) or appeared slightly enhanced in occasional subjects especially during tactile exploration. P40 and N60 showed again some interindividual variability in their behaviour. In Fig. 1 P40 amplitude is not markedly affected, whereas in Fig. 2 active, passive and exploration conditions caused a small enhancement of P40. N60 is clearly identifiable only in the subject of Fig. 2, in whom it is slightly attenuated in the test conditions. The ANOVAs at P3 revealed significant reductions of N20, P27 and N60 over the test conditions, while N34 and P40 remained statistically unchanged (Table I). In addition to assessment of individual amplitude values, we calculated the amplitude ratio P - N 2 0 / F - N 3 0 for each subject and condition, as suggested by Rossini et al. (1989) to overcome some of the intersubject variability of these potentials. At rest, this ratio was 0.7 (standard error 0.09). In the test conditions it was

221 significantly ( P < 0.01) increased, being 1.9 (0.7) for active movement, 2.5 (0.8) for tactile exploration, 1.9 (0.8) for passive movement and 1.2 (0.5) for isometric contraction. Comparison with Table I shows that these ratios paralleled the attenuations of N30 and did not reveal additional differences between the effects of various conditions on the frontal and parietal SEPs. It is evident from the examples of Figs. 1 and 2, and from the group results in Table I, that active and passive movement and tactile exploration had qualitatively very similar effects upon the SEP deflections. This was confirmed with a 2-way ANOVA, which did not disclose any significant interaction between test conditions and component amplitudes. Quantitatively, the effects of tactile exploration were the most pronounced for all affected SEP components. Active and passive movement produced nearly equally strong effects on all components. Isometric contraction exerted only slight modifications, which nevertheless were similar to the effects of other test conditions (Table I). In the 8 subjects with elbow neurogram records, mean amplitudes of the compound nerve action potential showed no significant changes between rest and test conditions. Yet these subjects, tested under the same conditions as all other subjects, showed the characteristic modification of SEPs. The observed effects cannot therefore be ascribed to altered stimulation conditions during movements. Fig. 3 illustrates parietal SEP traces and neurograms in 6 subjects during rest and tactile exploration. The SEPs show the slight diminutions of N20 and N60, the marked reduction of P27 and relative preservation of P40 in the presence of remarkably well preserved neurograms.

Discussion This study showed that all movements affected frontal, central and parietal SEPs in a similar manner. The P14 with a subcortical origin (Desmedt and Cheron 1980; Chiappa 1983) remained unchanged. The early cortical components were attenuated, while later waves were unchanged, except for the reduction of parietal N60. At F3 a P35 appeared during movement conditions in place of the attenuated N30. Evarts and Fromm (1978) studied the effects of kinesthetic stimulation on motor cortex neurones during different types of movement tasks. They trained monkeys to move a handle toward a target position under visual feedback. Torque pulses were injected to the handle as kinesthetic stimuli during movement. The authors found that relatively large ballistic movements suppressed responsiveness of the pyramidal cells to this type of stimulation. In contrast, these responses were rather enhanced when the monkeys performed fine precision movements of small amplitude. The authors con-

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chided that the differences of cortical responsiveness might be due to different kinds of central programmes employed in these two tasks. According to this concept the ballistic movements are relatively independent of sensory input and cause suppression of ascending sensory volleys. However, the precision movements are dependent on continuous proprioceptive feedback, whose access to the cortex would then be enhanced. In the present study, repetitive thumb movement was chosen as a task supposed to be relatively independent of continuous fine adjustment by feedback information. While these movements may not be rapid enough to be termed truly "ballistic," they are likely to involve less guidance by afferent impluses than tactile exploration. The exploration task was used to represent finely graded movements, which must rely on continuous kinesthetic feedback. Since some of the frontally recorded SEP deflections appear to be generated in the precentral cortex (Mauguirre et al. 1983; Slimp et al. 1986), one would have expected differences similar to those reported from the motor cortex by Evarts and Fromm. Lack of such differences could result from several factors. First, according to F r o m m and Evarts, precise fine movements were preferentially controlled by smaller pyramidal neurones than large ballistic movements. It is not known to what extent such small neurones contribute to the mass potentials of the scalp-recorded SEPs. Another possibility is that the changes in SEPs result from occlusive afferent mechanisms rather than centrifugal effects of motor programmes, and that these could override any subtle "enhancement" of input during tactile exploration. During the movement tasks, particularly tactile exploration, the subject is likely to direct more attention to the stimulated limb than during rest. However, selective attention to target finger stimuli has been shown to increase the amplitudes of middle-latency (30-100 msec) positive parietal SEP components (Desmedt and Tomberg 1989). Hence, the decrease of these potentials during movement tasks cannot be attributed to enhanced attention. The possibility of afferent occlusion as underlying SEP changes during movement was suggested by Rushton et al. (1981), who found, in agreement with the present study, that passive and active movements caused very similar modifications of the SEPs. Recently the same possibility was discussed by Jones et al. (1989), who also reported similar effects of active and passive movements on the SEP wave forms. In addition, these authors studied the effect of concurrent tactile stimulation of the thumb without any movement and found this effect to be similar to those of both active and passive movements. However, the extent of modification between these conditions differed for various SEP components: active movement was most effective in attenuating frontal N30, while passive movement had

J. HUTTUNEN, V. HOMBERG

the strongest effect on central P25 (P22 in our study), and tactile stimulation on parietal N20. In the present study, no such differences between the conditions were observed. In particular, the effects of active and passive movements were essentially identical on all SEP components. Furthermore, the effects of tactile exploration were larger compared with active and passive movement for all deflections studied. Hence, no qualitative difference was found between the effect of tactile exploration and active or passive movement. The finding that tactile exploration appeared quantitatively most effective in modifying the SEPs might result from the fact that more muscle afferents, including those from several forearm muscles, and cutaneous afferents from 3 digits must have been activated during this task. Animal studies have shown that the lemniscal afferent volleys are suppressed before movement onset, indicating a centrifugal "gating" of ascending signals at the dorsal column nuclei (Ghez and Pisa 1972; Coulter 1974; Chapman et al. 1988). C h a p m a n and coworkers found an additional suppression at the thalamo-cortical level, which was present also during passive movement and hence probably caused by centripetal afferent occlusion. In our and previous studies (Cheron and Borenstein 1987; Cohen and Starr 1987; Jones et al. 1989), the P14 potential with a thalamic or lemniscal origin (cf., Chiappa 1983) was not diminished by movement, indicating that the changes in SEPs mainly occur at the thalamo-cortical level. Cohen and Starr (1985) found also that the lumbar potentials elicited by posterior tibial or sural nerve stimulation were not affected by contraction of the gastrocnemius muscle, while the cortical potentials were diminished. As pointed out by Jones et al. (1989), active movement causes afferent volleys in the cutaneous fibres of the median nerve (Hulliger et al. 1979), and an afferent occlusion by cutaneous signals cannot be excluded during active movement. Hence, afferent occlusion is a sufficient, even if not the only possible, explanation for SEP modification during movement. The greater extent of modification during tactile exploration might be due to more intense activation of cutaneous afferents during this task. Although afferent mechanisms are thus sufficient to account for the changes during movement, the finding of Cohen and Starr (1987) that the postcentral P27 is attenuated already 100 msec prior to the onset of movement cannot be reconciled with this concept. However, these authors used movements time-locked to the stimuli. Hence an algebraic summation of a movementrelated negative potential with P27 cannot be entirely ruled out as a cause of P27 attenuation. It should be recognized, nevertheless, that efferent mechanisms may play a role, when SEPs are recorded prior to movement

SEP MODIFICATION BY MOVEMENT

onset. Along with previous studies, the present results suggest that these efferent mechanisms may be reliably studied only before movement onset. This work was supported by a grant from the Alexander von Humboldt Foundation to J.H., and grants from the Deutsche Forschungsgemeinschaft (SFB 200, B9) to V.H.

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