- Email: [email protected]
Brain macropotentials associated with distinct phases of voluntary sustained isometric contraction in man
INTERNATIONAL JOURNAL OF PSYCHOPHYSIOLOGY International
Journal of Psychophysiology
22 ( 19%) 35-44
Brain macropotentials associated with distinct phases of voluntary sustained isometric contraction in man Bozhidar Dimitrov *, Gantcho N. Gantchev, David Popivanov Motor Control
Section, Institute of Physiology, Bulgarian Academy of Sciences, Acad. G. Bonrchev St., bl. 23. 1113 Sofia. Bulgaria
Received30 November 1993; revised 30 October 1994; accepted 12 May 1995
Abstract Brain potentials recorded from the scalp during voluntary sustained isometric contraction have been consistently found to accompany both the beginning and the termination of the contraction. This study attempts to evaluate the dependence of the potentials related to the voluntary termination of a sustained effort on the physical parameters of the motor task and also to further investigate the relationship between potentials related to the initiation and to the termination of action. Brain potentials from healthy male volunteers performing hand-grip squeeze were time-locked to (1) beginning of contraction; (2) execution of an additional effort; and (3) the moment of voluntary relaxation, and then averaged. The waveshape and amplitude of the entire potential curve preceding and following the decision to act were evaluated with best-fit mathematical approximation procedures. Few correlations between the various descriptive parameters of the three types of potentials were found. The brain potentials accompanying beginning of the contraction from state of rest differed significantly from those accompanying execution of an additional effort and both potentials preceding initiation of voluntary effort differed from potentials preceding decision to terminate the action. It is hypothesised that brain macropotentials are linked to separate underlying commands for initiation and termination of voluntary action. Keywords: Brain macropotential; area; Motivation
Bereitschaftspotential;
Isometric
contraction;
1. Introduction Movement related brain potentials have been exhaustively studied mainly in situations related to beginning of action. Although it was pointed out by Wainberg (1980) that slow potentials related to the inhibition of movement do exist, this notion has not been extensively explored. We have shown (Dimitrov, 1985; Dimitrov et al., 1987) that the termination of an ongoing voluntary sustained effort was
Corresponding author. Tel.: (0359)-2-713-3701; 2-7 19- 1090; e-mail: [email protected]. l
Fax: (0359)
0167-8760/%/$1.5.00 0 1996 Elsevier Science B.V. All rights resewed P1I SO167-8760(96)00012-8
Voluntary
effort; Muscle relaxation;
Supplementary
motor
consistently accompanied by potentials similar in waveshape and amplitude to those related to the beginning of action. However, we have not strictly controlled the physical parameters of the motor task and a predominantly qualitative description has been performed. In the present study we aimed at further exploring two important notions. First, we felt it might be of crucial importance to verify if the appearance of potentials related to the termination of contraction was exclusively attributed to a decision for ending the task, or it might constitute a by-product of additional muscle involvement. Second, we have had to
36
B. Dimitrou et al./Intermtional
Journul of Psychophysiology
estimate the influence of the ammount of physical effort exerted at the moments of both initiation and termination of the task. There are contradictory reports about the relative contribution of task parameters, some supporting their role in augmenting brain potentials’ amplitude (Kutas and Donchin, 1977; Kristeva and Becker, 1978), some others disconfirming it (McAdam and Seales, 1969; Dimitrov et al., 1987). The isometric contraction was chosen as a suitable model providing relatively clear-cut start and end of a voluntary effort. Experiments employing voluntary sustained contraction have produced either sustained positivity (Otto et al., 1977) or steady negativity (Rebert et al., 1976; Grunewald-Zuberbier et al., 1980; Grunewald et al., 1984; Deecke et al., 1984; Lang et al., 1988). The negativity maintained during so-called ‘goal-directed’ tasks was so uniformly present, that it could be revealed even upon the background of a sustained positive DC-shift, as in an experiment of maintained contraction we performed earlier (Gantchev et al., 1982). Potentials preceding the initiation of contraction from state of rest and potentials preceding the termination of contraction obviously develop upon different DC-levels. Nevertheless, we decided to link the two situations, since there is no other way of doing the comparison, and besides, even with a superimposed negativity generated by the task itself, we could have always made the expected extrapolations. Regardless of possible interference or superimposition with motivation- or attention-related DC-shifts, the mere fact of finding a waveshape and amplitude shift preceding the end of contraction, would satisfy our prediction of an existence of distinctive potential related to a central command. On the other hand, a possible relation of such potentials with the variable muscle force exerted at two different kinds of termination would clarify to an extent the contribution of physical factors. Thus, alternating releases from state of maintained effort were compared with brief additional squeezes before the termination, both executed upon subjects’ own discretion and pace. 2. Methods Six healthy male paid volunteers, aged between 23 and 36 years (mean 28.51, put to a questionnaire
22 (1996) 35-44
for right-handedness, were studied. They performed isometric contraction of the dominant right hand by squeezing a tensometric device held in a semipronated arm. The experiment was preceded by a training session during which subjects learned to initiate the contraction with 30% of the maximum, individually estimated force; to maintain steady force for about 5 s; and to either abruptly relax or to execute brisk additional squeeze up to 50% maximum force, followed by relaxation. Visual feedback about the force output level was presented as a continuous beam on a monitor placed in front of the reclining subject with the instruction that it should be used only for checking the approximate durations and strenghts, rather than strictly keeping within the specified boundaries and thus executing a goal-directed task. The experimenter intervened only in cases of extremely disproportionate performance. Thus, the instruction of keeping the steady effort for 5 s was considered satisfied, when the range of actual maintenance ranged within 3- to 7-s intervals. Subjects performed a total of 120 trials alternately choosing either simple release or additional effort as the way of termination and leaving another 5- to 10-s intervals for complete relaxation and rest between trials. Abrupt initiation, rather than precise force control was the primary consideration. The electroencephalogram (EEG) was recorded with silver disc electrodes affixed with adhesive paste over scalp positions FC, (equidistant between F, and C,, believed to overly the supplementary motor area - SMA), C3+ 2 (2 cm ahead of C,, over the hand motor area), and C, (vertex) and referred to linked earlobes. The EEG was recorded in the range 0.026 to 70 Hz on an ALVAR REEGA machine and was fed into the preamplifiers of a MINC-23 minicomputer programmed to automatically fill in the full range of its 12 bit A/D convertor. The electrooculogram (EOG) was recorded bipolarly from above and aside the right orbit as a monitor for eye-movement-related artifacts and the electromyogram (EMG) was recorded with skin surface electrodes over the ulnar wrist flexor muscle in the bandpass 16- 1000 Hz. Sampling was done at a rate of 142 Hz and individual trials were accepted off-line on an artifact-free basis, viewing the EEG, EOG and EMG traces and on compliance with the biomechanical requirements for isometric contraction.
B. Dimitroo et al./International
Journal of Psychophysiology 22 (1996) 35-44
.
REST
s.rrl?r
3
I 0
7 ret
37 [RELAX
RELEASE
Fig. 1. Single trial EMG epochs. Both left samples are the initiation of contraction from state of rest; upper right hate contraction as simple release; lower right trace is additional voluntary contraction, followed by relaxation.
Single-trial EMG traces were scrutinized for appropriate initiation, duration and termination, and selected into four categories using dialogue mode in Fortran- programme. The first EMG burst initiating contraction, the first increase of the steadily maintained firing and the first steep decline of the ongoing plateau were marked with precision of 7 ms on single trials (see Fig. 1) and the accompanying EEG traces were averaged time-locked to either start or
. .
.
.
of
end of contraction, respectively, using a modified procedure of Popivanov (1986). The beginning and the end of the voluntary effort (marked with vertical bars) were viewed separately. Due to automatic equalizing the images of maintained and additional effort appear of a lower than real amplitudes on the figure. Two sets of 30 to 40 averaged EEG epochs were yielded for every subject and one subject was discarded for reasons of excessive artifacts. The
.
i
i
is termination
.
.
l
.
700
Fig. 2. Brain macropotentials related to tie beginning of sustained isometric contraction (A and C) and to termination either by simple release (B) or by additional voluntary effort (D). Chebyshev’s polynomials of second order are marked with dots below: 1 to 2 - baseline; 2 to vertical bar - preceding negativity (BP); 2 to 3 - onset to peak negativity (BP + NS); 3 to end - resolution towards positivity (MP). Total epoch = 2800 ms. Dwell time = 7 ms. EMC onset/offset at I750 ms, marked with vertical bar. Lead C,.
38
B. Dimitrou et al./Internationul
Journal of Psychophysiology 22 (1996) 35-44
ensuing brain potentials coincided with four distinct contraction phases: (1) initiation of contraction from rest; (2) corresponding simple release; (3) initiation of contraction from rest; (4) corresponding additional effort. The averaged potentials were analysed over an epoch preceding the EMG mark by 1750 ms and following it for another 1050 ms. The initial 350 ms were used as a baseline and the beginning of a steady upward shift was marked as the start of the potential curve to be analysed. The mathematical description of the entire curve was proved to be best achieved by employing second order Chebyshev’s polynomial approximation. The equation: Ax2 + Bx + C provided three coefficients characterizing the slope of the curve (A), the steepness of its rise (B) and the shift over the baseline CC). Positive values of slope suggested upward-bend and negative values downward-bend curves. The incrementing or decrementing rise of the curve was described by its steepness. The shift was related to the magnitude of negativity. Detailed description of the method is given in another paper by Popivanov (1992). Three segments were separately analysed borrowing the nomenclature of Barrett et al. (1986): from onset up to the EMG mark (Bereitschaftspotential, BP); from onset up to the peak negativity (Bereitschaftspotential + Negative Shift, BP + NS); from maximum negativity to the end of epoch (Motor Potential, MP); see also Fig. 2. The onset of the BP was estimated to be the point of ‘take-off’ above the baseline of the polynomial approximation. All coefficients were sub jetted to multiple regression and Student’s t-test analysis.
The termination of the contraction was also preceded by a steady rise in negativity, similar in appearance to that related to the initiation of effort, and was followed by swift downward resolution toward positivity (lower traces). The waveshape of the complex potential remained the same, regardless of the type of termination - simple release or additional contraction. The onset times showed earlier appearance of negativity preceding termination of contraction for both simple relaxation (p < 0.001) and additional contraction ( p < 0.05) in comparison to their respective initiations (Fig. 3). This relationship, however, was significant only for the SMA derivation. The analysis of coefficients characterizing segments’ parameters of Chebyshev’s polynomials revealed quite distinct differences between otherwise similar in appearance waveshapes (Fig. 4). The slope of preceding negativity over the vertex had an upward bend, thus showing incrementing rate of change before the start of contraction (positive values of A, top left), while before the termination the rate of change turned into a decrementing one, with downward bend (negative values of A) and this was significant for both segments BP ( p < 0.05) and BP + NS (p < 0.05). The steepness of preceding negativity (BP + NS) over the midline showed opposite courses before the start of isometric contraction
ONSET T I ME
3. Results A typical set of the four potentials in one subject that is characteristic for the group is shown in Fig. 2. The beginnings of sustained contraction (A and C) are matched with their respective terminations simple release (B) or additional voluntary effort CD). EMG onset/offset was at the 1750ieth ms from the beginning of trace, marked with a vertical bar. The beginning of contraction was preceded by a negative shift and the sustained effort was accompanied by a sustained negativity over the baseline (upper traces).
FELAXATKM
CDOIT~M
FCr Fig. 3. Onset time latencies. Preceding negativity (BP) over the SMA lead (FC,) associated with beginning of sustained contraction (hatched) occurred later than negativity preceding termination (dotted), regardless of its type.
B. DimiWou et al./International
Journal of Psychophysiology 22 (1996) 35-44
(negative increment) and before simple release (positive increment; p < 0.001 for FC, and p < 0.05 for C,, bottom left). The shift above baseline of preceding negativity (BP + NS) showed lesser amplitude preceding simple release in comparison to the beginning of contraction for both midline leads ( p < 0.01 at FC, and p < 0.05 at C,; bottom right). Interestingly enough, this was not valid for BP segment alone, i.e. amplitudes at time EMG = 0 were of equal magnitudes. Thus, both waveshape and amplitude of potentials related to initiation and termination of sustained contraction revealed different patterns. The preceding negativity up to the maximum peak (BP + NS) over the SMA was different in all respects (p < 0.01 for slope, A; p < 0.001 for steepness, B; p < 0.01 for shift, C) between the beginning of sustained contraction and the execution of
39
additional contraction (Fig. 5, left). Over the vertex the steep rise of negativity up to the EMG mark (BP) showed negative correlation between contraction from state of rest and additional contraction (R = -0.808, F = 0.023, t < 0.01 - Fig. 5, top right) and positive correlation between contraction from rest and simple release (R = 0.899, F = 0.003, r < 0.001 - Fig. 5, bottom right). Significant correlations were found for the steepness of decreasing negativity (coefficient B for segment MP) over the contralateral hand area (C,,,) between simple release and additional contraction (R = 0.865, F = 0.008, t < 0.001 - Fig. 6, top left); and for the shift above baseline of decreasing negativity (coefficent C for segment MP) over the SMA (R = 0.902, F = 0.003, I < 0.001 - Fig. 6, bottom left) for the same conditions. The two types of
T-test, coefficients A - slope
-I_ . -3 A
A.BP+NS
BP
Cz; REL
coefficients B - steep
BP+NS;
coefficients C - shift
REL
Fig. 4. Student’s t-test for the three coefficients of Chebyshev’s polynomials: slope of curve (A), Comparisons are between initiation (hatched) and termination (dotted) of sustained contraction.
BP+NS;
REL
steepness (B), shift above baseline CC).
B. Dimitrou et al./lntemational
40
Journal of Psychophysiology 22 (1996) 3544
‘S-test, PAIRED COEFFICIENTS
-’
5
6 A
B
C
FCz; ADD; BP+NS
Fig. 5. Left: Three coefficients for preceding negativity (BP + NS) over the SMA lead (Fe,) during initiation of effort from rest (hatched) and during additional contraction (gray). Right: Polynomial regression of steepness over the vertex lead (C,). Correlations between BPS accompanying initiation of contraction from rest and initiation from state of sustained effort (top) and between BPS preceding the beginning
of sustained contraction and preceding simple release (bottom).
termination of contraction - simple relaxation and additional effort - thus differed only marginally ( p = 0.056) for the amplitude of resolution negativity (MF’) over the SMA (Fig. 6, right).
4. Discussion The experimental results provided a convincing evidence that end-related slow macropotentials of the brain do exist. Their waveshape and magnitude were similar to potentials preceding the decision to act. Furthermore, when measured against their own baseline, i.e. the DC-level established in the course of a sustained contraction, the potentials preceding both simple release and additional contraction were composed of a steady negativity. Similar findings were
reported in our previous works (Gantchev et al., 1982; Gantchev and Dimitrov, 1983). Thus, they should not be regarded as a mere by-product of agonist-antagonist muscle involvement at the task completeion, but rather as related to a separate internal command for cessation of action. Negativity accompanying cessation of sustained motor activity was also reported by Trimmel et al. (1989). The task we have designed employed a persistent visual feedback. In similar conditions demanding decision-making toward the end of the contraction or aiming at a goal (Grunewald-Zuberbier et al., 1980; Grunewald and Grunewald-Zuberbier, 1983; Deecke et al., 1984; McCallum et al., 1989) a prevailing negativity was always observed. Therefore, even superimposed on such negative DC-shift, the potentials elicited in our study were of distinctive magnitude as to allow measurement against their own baseline, different
B. Dimitrou
et al./lnrernutional
Journal
ofPsychophysiology
from rest. This proves first that a possible restrictive ‘ceiling-effect’ (Rebert et al., 1976) was not present and second, that sustained positivities similar to those found in the studies of Otto et al. (1977) and Gantchev et al. (1982) were not very likely to influence the negative-going slope of potentials. A sole possible artifact from the mostly informative and not demanding visual feedback, especially providing the instruction was specifically unrelated with a goal-directed task, could be the somewhat higher amplitude of potentials compared to a ‘pure’ self-paced Bereitschaftspotential; similar DC-shifts were described during visuomotor learning by Deecke et al. (1988). The requirement for brisk action and the visual guidance created a situation similar to the ‘precueing’ isometric contraction of Van Boxtel et al. (1989), that favours earlier increase in negativity while mon-
41
22 (1996) 35-44
itoring the screen. In any event, the major finding that we have sought for was that, regardless of possible DC-level influences, negative shifts related to the termination of voluntary effort did exist. The subsequent elaborate mathematical analysis of Chebyshev’s polynomials provided more intricate details. The slope of the averaged curve and the steepness of its increase did differ between potentials preceding initiation of sustained contraction and potentials preceding its termination. These differences were better expressed alongside midline leads. The difference was obvious when the entire segment up to the maximum peak was considered (BP + NS), while there were no significant differences at the moment of EMG initiation/cessation (BP). This provides further support for the notion of Libet et al. (1981) and Barrett et al. (1986) that, indeed, two
C - shift, MP & Resolution 60 z q &50 q 1
Fig. 6. Top left: Polynomial regression of steepness (B) of decreasing Correlation between simple release and additional contraction shows lack negativity’s shift over the baseline (C) at SMA lead (FC,). Correlation force effect. Right: Student’s r-test for amplitudes of resolution negativity additional contraction shows lack of significance.
negativity (MP) over the contralateral hand motor of force effect. Bottom left: Polynomial regression between simple release and additional contraction (MP) over SMA area (FC,) accompanying simple
ADDITIONAL RELAXATK)N
area (C3+ *). of decreasing shows lack of relaxation and
42
B. Dimitrov et ol./Internationnl
Journal
separate periods of preparation might exist, represented by different components of the compound potential. Since most of the hypotheses concerning the movement related potentials are based on measurements of an arbitrarily taken short segments, preceding the initiation of voluntary contraction, we might stipulate that they could have been based on incomplete data. Although it was determined that the maximum negativity followed the EMG onset (Vaughan et al., 1968; Deecke et al., 1969; Gerbrandt, 1977) it is our impression that not many comparisons were done between those segments separated in time by the EMG occurrence. Neshige et al. (1988) estimated the lag of peaking negativity at around 150 ms, which is comparable with the peak occurrence of BP + NS in our study. Of particular interest was the finding of positive correlation between start and end of the voluntary effort. On the other side, the correlation between start of contraction from state of rest and the additional effort exerted during sustained effort turned out to be negative. Obviously, the contribution of force level for magnitude and shape of the movement related potentials should be considered in terms of subjective involvement (as in McAdam and Seales, 1969; Kutas and Donchin, 19771, rather than the precise amount of the incoming peripheral afferent information. Just measuring the force gradation might not provide significant differences (like in experiments of Kristeva et al., 1989; Gantchev et al., 1987; Trimmel et al., 1989) because in these experiments the factor of influence was not a perceptible difference in subjective involvement. In an earlier experiment of ours (Dimitrov et al., 1987) it was found that the preceding negativity did not differ between biceps contraction and biceps/triceps cocontraction so the conclusion was drawn that it was independent of the muscle mass involved. On the other hand, the requirement to perform selectively, as in this experiment, might influence the magnitude of potentials. The level of negativity is related to the level of task demand or workload (Deecke et al., 1984; McCallum et al,, 1989). It is of interest that there was no difference in negativities preceding simple release and additional contraction at the C3+2 lead - over the hand motor area - which should be mostly linked to physical effort. There were changes in both steepness of the resolution towards positivity (MP)
ofPsychophysiology 22 (1996) 35-44 and its shift over the baseline, the changes being pronounced over the SMA lead. Such dependence of the ensuing positivity on the physical parameters of the task has already been described (Dimitrov, 1985). Most of the significant correlations and differences in Chebyshev’s polynomials parameters were observed over the SMA lead. Following the description of Brinkman and Porter (1983) many studies have found evidence for the role of SMA in the initiation of action and decision making (Wiesendanger, 1986; Deecke, 1987; Brunia and Damen, 1988; Neshige et al., 1988; Ikeda et al., 1993). In our study the termination of action was preceded by an earlier negativity over the SMA in comparison to initiation of contraction, regardless of its type (release or additional effort). The only difference in magnitude of preceding negativity between initiation and termination was also found above SMA and vertex. The marginally significant difference in resolution positivity between simple release and additional contraction was observed only over SMA. All these findings suggest SMA involvement not only in earlier stages of preparation, but also during the control of action. The lack of SMA involvement found in other studies might be attributed to a relatively easy and automatic mode of performance, as in the case of simple repetitive movements, studied by Botzel et al. (1993). In conclusion, it was found that the termination of sustained isometric contraction was accompanied by brain macropotentials of distinctive waveshape, regardless of the type of termination. There occurred differences between potentials accompanying initiation of effort from a state of rest and from a state of maintained force on one side, and there occurred similarities between potentials accompanying termination of effort and potentials accompanying exertion of additional effort, on the other side. The generation of movement related brain potentials should be attributed to central cerebral command for decision to act, rather than to particular task parameters or agonist-antagonist muscle engagement.
References Barrett, G., Shibasaki, H. and Neshige, R. (1986) Cortical potentials preceding voluntary movement: evidence for three peri-
B. Dimitrov et aI./lnternational
JournaI of Psychophysiology
ods of preparation in man. Electroenceph. Clin. Neurophysiol., 63: 327-339. Botzel, K.. Plendl, H., Paulus, W. and Scherg, M. (1993) Bereitschaftspotential - is there a contribution of the supplementary motor area. Electroenceph. Clin. Neurophysiol., 89: 187196. Brinkman, C. and Porter, R. (1983) Supplementary motor area and premotor area of monkey cerebral cortex: functional organization and activities of single neurons during performance of a learned movement. In: J.E. Desmedt (Ed.), Motor Control Mechanisms in Health and Disease. Adv. Neurol., Vol. 39, Raven Pmss, New York, pp. 393-420. Brunia, C.H.M. and Damen, E.J.P. (1988) Distribution of slow brain potentials related to motor preparation and stimulus anticipation in a time estimation task. Electroenceph. Clin. Neurophysiol., 69: 234-243. Deecke, L. (1987) Bereitschaftspotential as an indicator of movement preparation in supplementary motor area and motor cortex. In: R. Porter (Ed.), Motor Areas of the Cerebral Cortex. CIBA Foundation Symposium 132, Wiley, Chichester, pp. 23 l-250. Deecke, L., Scheidt, P. and Komhuber, H.H. (1%9) Distribution of readiness potential, pre.-motion positivity and motor potential of the human cerebral cortex preceding voluntary movement. Exp. Brain Res., 7: 158-168. Deecke, L., Bashore, T., Bnmia, C.H.M., Gmnewald-Zuberbier, E.. Gmnewald, G. and Kristeva, R. (1984) Movement-associated potentials and motor control. Ann. NY Acad. Sci., 398428. Dimitrov, B. (1985) Brain potentials related to the beginning and to the termination of voluntary flexion and extension in man. Int. J. Psychophysiol., 3: 13-22. Dimitrov, B.. Gantchev, G.N. and Popivanov, D. (1987) Movement related brain potentials in sustained isometric voluntary contraction. In: G.N., Gantchev, B. Dimitrov and P. Gatev (Eds.), Motor Control, Plenum Press, New York, pp. 93-98. Gantchev, G.N. and Dimitrov, B. (1983) Brain potentials related to additional isometric contraction. Activ. Nerv. Super. (Praha), 25: 285-292. Gantchev. G.N., Dimitrov, B. and Popivanov, D. (1982) Brain potentials related to voluntary sustained effort. Acta Physiol. Pharmacol. Bulg., 8: 14-22. Gerbrandt, L.K. (1977) Analysis of movement potential components In: J.E. Desmedt (Ed.), Attention, Voluntary Contraction and Event-Related Cerebral Potentials. Progress in Clinical Neurophysiology, Vol. I, Karger, Basel, pp. 174- 188. Gnmewald-Zuberbier, E., Gnmewald, G., Schumacher, H. and Wehler, A. (1980) Scalp recorded siow potential shifts during isometric tamp and hold contractions in human subjects. Pflugers Arch., 389: 55-60. Grunewald, G. and Grunewald-Zubcrbier, E. (1983) Cerebral potentials during voluntary ramp movements in aiming tasks. In: A.W.K. Gaillard and W. Ritter (Eds.), Tutorials in ERP Research - Endogenous Components, Elsevier, Amsterdam, New York, pp. 3 1 l-327. Ikeda, A., Luders, H.O., Burgess, R.C. and Shibasaki. H. (1993)
22 (1996) 35-44
43
Movement-related potentials associated with single and repetitive movements recorded from human supplementary motor area. Electroenceph. Clin. Neurophysiol., 89: 269-277. Kristeva, R. and Becker, W. (1978) Cerebral potentials preceding voluntary isometric force deployments of varying amplitudes. Pfliigers Arch., Suppl. 373: R74. Kristeva, R., Cheyne, D., Lang, W., Lindmger, G. and Deecke, L. (1989) Movement-related potentials accompanying unilateral and bilateral simultaneous movements with different inertial load. In: EPIC IX, Vol. 2, No. 16, Noordwijk, The Netherlands. Kutas, M. and Donchin, E. (1977) The effect of handedness, of responding hand and of response force on the contralateral dominance of the readiness potential. In: J.E. Desmedt (Ed.), Attention, Voluntary Contraction and Event-Related Cerebral Potentials. Progress in Clinical Neurophysiology, Vol. I, S. Karger, Basel, pp. 189-210. Lang, W., Lang, M., Podreka, I., Steiner, M., Uhl, F., Suess, E., Muller, Ch. and Deecke, L. (1988) DC-potential shifts and regional cerebral blood flow reveal frontal cortex involvement in human visuomotor learning. Exp. Brain Res., 71: 353-364. Libet, B., Wright, E.W., Jr. and Gleason, C.A. (1981) Readiness potentials preceding unrestricted ‘spontaneous’ vs pre-planned voluntary acts. Electroenceph. Clin. Neurophysiol., 54: 322335. McAdam, D.W. and Seales, D.M. (1%9) Bereitschaftspotential enhancement with increased level of motivation. Electroenceph. Clin. Neurophysiol., 27: 73-75. McCallum, W.C., Cooper, R. and Pocock, P.V. (1989) Brain DC shifts associated with monitoring a visual display. In: EPIC IX, Vol. 2, No. 13, Noordwijk, ‘The Netherlands. Neshige, R., Luders, H. and Shibasaki, H. (1988) Recording of movement-related potentials from scalp and cortex in man. Brain, 111: 719-736. Otto, D., Benignus, V., Ryan, L. and Leifer, L. (1977) Slow potential components of stimulus, response and preparatory process in man. In: J.E. Desmedt (Ed.), Attention, Voluntary Contraction and Event-Related Cerebral Potentials. Progress in Clinical Neurophysiology, Vol. I, S. Karger, Basel, pp. 211230. Popivauov, D. (1986) Computer detection of EMG edges for synchronization of movement-related brain potentials. Electroenceph. Clin. Neurophysiol., 64: 171- 176. Popivanov, D. (1992) Tie series analysis of brain potentials preceding voluntary movements. Med. Biol. Eng. & Comput., 30: 9-14. Rebert, C., Berry, R. and Merlo, J. (1976) DC potential consequences of induced muscle tension. Effects on contingent negative variation. In: W.C. McCallum and J. Knott (Bds.), The Responsive Brain, John Wright & Sons, Bristol, pp. 126-131. Trimmel, M., Groll-Knapp, E., Streicher, F. and Haider, M. (1989) DC potentials during and after cued, sustained motor activity (muscle tension). In: EPIC IX, Vol. 2, No. 28, Noordwijk, The Netherlands. Van Boxtel, G.J.M., Van den Boogaart. B. and Brunia, C.H.M.
44
B. Dimitrov
( 1989) The effects of precueing
et ol./lnternational
Journal of Psychophysiology 22 (1996) 35-44
isometric contraction speed on the contingent negative variation and reaction time. In: EPIC IX, Vol. 2, No. 23, Noordwijk, The Netherlands. Vaughan, H.B., Jr., Costa, L.D. and Ritter, W. (1968) Topography of human motor potential. Electroenceph. Chn. Neurophysiol., 25: I-10. Wait&erg, H. (1980) Slow potentials related to initiation and inhibition of proprioceptively guided movements. In: H.H.
Komhuber and L. Dee&e (Eds.), Motivation, Motor and Sensory Processes of the Brain: Electrical Potentials, Behaviour and Clinical Use. Progress in Brain Ressearch, Vol. 54, Elsevier, Amsterdam, pp. 183- 186. Wiesendanger. M. (1986) Recent developments in studies of the supplementary motor area of primates. Rev. Physiol. B&hem. Pharmacol., 103: 1-59.
Journal of Psychophysiology
22 ( 19%) 35-44
Brain macropotentials associated with distinct phases of voluntary sustained isometric contraction in man Bozhidar Dimitrov *, Gantcho N. Gantchev, David Popivanov Motor Control
Section, Institute of Physiology, Bulgarian Academy of Sciences, Acad. G. Bonrchev St., bl. 23. 1113 Sofia. Bulgaria
Received30 November 1993; revised 30 October 1994; accepted 12 May 1995
Abstract Brain potentials recorded from the scalp during voluntary sustained isometric contraction have been consistently found to accompany both the beginning and the termination of the contraction. This study attempts to evaluate the dependence of the potentials related to the voluntary termination of a sustained effort on the physical parameters of the motor task and also to further investigate the relationship between potentials related to the initiation and to the termination of action. Brain potentials from healthy male volunteers performing hand-grip squeeze were time-locked to (1) beginning of contraction; (2) execution of an additional effort; and (3) the moment of voluntary relaxation, and then averaged. The waveshape and amplitude of the entire potential curve preceding and following the decision to act were evaluated with best-fit mathematical approximation procedures. Few correlations between the various descriptive parameters of the three types of potentials were found. The brain potentials accompanying beginning of the contraction from state of rest differed significantly from those accompanying execution of an additional effort and both potentials preceding initiation of voluntary effort differed from potentials preceding decision to terminate the action. It is hypothesised that brain macropotentials are linked to separate underlying commands for initiation and termination of voluntary action. Keywords: Brain macropotential; area; Motivation
Bereitschaftspotential;
Isometric
contraction;
1. Introduction Movement related brain potentials have been exhaustively studied mainly in situations related to beginning of action. Although it was pointed out by Wainberg (1980) that slow potentials related to the inhibition of movement do exist, this notion has not been extensively explored. We have shown (Dimitrov, 1985; Dimitrov et al., 1987) that the termination of an ongoing voluntary sustained effort was
Corresponding author. Tel.: (0359)-2-713-3701; 2-7 19- 1090; e-mail: [email protected]. l
Fax: (0359)
0167-8760/%/$1.5.00 0 1996 Elsevier Science B.V. All rights resewed P1I SO167-8760(96)00012-8
Voluntary
effort; Muscle relaxation;
Supplementary
motor
consistently accompanied by potentials similar in waveshape and amplitude to those related to the beginning of action. However, we have not strictly controlled the physical parameters of the motor task and a predominantly qualitative description has been performed. In the present study we aimed at further exploring two important notions. First, we felt it might be of crucial importance to verify if the appearance of potentials related to the termination of contraction was exclusively attributed to a decision for ending the task, or it might constitute a by-product of additional muscle involvement. Second, we have had to
36
B. Dimitrou et al./Intermtional
Journul of Psychophysiology
estimate the influence of the ammount of physical effort exerted at the moments of both initiation and termination of the task. There are contradictory reports about the relative contribution of task parameters, some supporting their role in augmenting brain potentials’ amplitude (Kutas and Donchin, 1977; Kristeva and Becker, 1978), some others disconfirming it (McAdam and Seales, 1969; Dimitrov et al., 1987). The isometric contraction was chosen as a suitable model providing relatively clear-cut start and end of a voluntary effort. Experiments employing voluntary sustained contraction have produced either sustained positivity (Otto et al., 1977) or steady negativity (Rebert et al., 1976; Grunewald-Zuberbier et al., 1980; Grunewald et al., 1984; Deecke et al., 1984; Lang et al., 1988). The negativity maintained during so-called ‘goal-directed’ tasks was so uniformly present, that it could be revealed even upon the background of a sustained positive DC-shift, as in an experiment of maintained contraction we performed earlier (Gantchev et al., 1982). Potentials preceding the initiation of contraction from state of rest and potentials preceding the termination of contraction obviously develop upon different DC-levels. Nevertheless, we decided to link the two situations, since there is no other way of doing the comparison, and besides, even with a superimposed negativity generated by the task itself, we could have always made the expected extrapolations. Regardless of possible interference or superimposition with motivation- or attention-related DC-shifts, the mere fact of finding a waveshape and amplitude shift preceding the end of contraction, would satisfy our prediction of an existence of distinctive potential related to a central command. On the other hand, a possible relation of such potentials with the variable muscle force exerted at two different kinds of termination would clarify to an extent the contribution of physical factors. Thus, alternating releases from state of maintained effort were compared with brief additional squeezes before the termination, both executed upon subjects’ own discretion and pace. 2. Methods Six healthy male paid volunteers, aged between 23 and 36 years (mean 28.51, put to a questionnaire
22 (1996) 35-44
for right-handedness, were studied. They performed isometric contraction of the dominant right hand by squeezing a tensometric device held in a semipronated arm. The experiment was preceded by a training session during which subjects learned to initiate the contraction with 30% of the maximum, individually estimated force; to maintain steady force for about 5 s; and to either abruptly relax or to execute brisk additional squeeze up to 50% maximum force, followed by relaxation. Visual feedback about the force output level was presented as a continuous beam on a monitor placed in front of the reclining subject with the instruction that it should be used only for checking the approximate durations and strenghts, rather than strictly keeping within the specified boundaries and thus executing a goal-directed task. The experimenter intervened only in cases of extremely disproportionate performance. Thus, the instruction of keeping the steady effort for 5 s was considered satisfied, when the range of actual maintenance ranged within 3- to 7-s intervals. Subjects performed a total of 120 trials alternately choosing either simple release or additional effort as the way of termination and leaving another 5- to 10-s intervals for complete relaxation and rest between trials. Abrupt initiation, rather than precise force control was the primary consideration. The electroencephalogram (EEG) was recorded with silver disc electrodes affixed with adhesive paste over scalp positions FC, (equidistant between F, and C,, believed to overly the supplementary motor area - SMA), C3+ 2 (2 cm ahead of C,, over the hand motor area), and C, (vertex) and referred to linked earlobes. The EEG was recorded in the range 0.026 to 70 Hz on an ALVAR REEGA machine and was fed into the preamplifiers of a MINC-23 minicomputer programmed to automatically fill in the full range of its 12 bit A/D convertor. The electrooculogram (EOG) was recorded bipolarly from above and aside the right orbit as a monitor for eye-movement-related artifacts and the electromyogram (EMG) was recorded with skin surface electrodes over the ulnar wrist flexor muscle in the bandpass 16- 1000 Hz. Sampling was done at a rate of 142 Hz and individual trials were accepted off-line on an artifact-free basis, viewing the EEG, EOG and EMG traces and on compliance with the biomechanical requirements for isometric contraction.
B. Dimitroo et al./International
Journal of Psychophysiology 22 (1996) 35-44
.
REST
s.rrl?r
3
I 0
7 ret
37 [RELAX
RELEASE
Fig. 1. Single trial EMG epochs. Both left samples are the initiation of contraction from state of rest; upper right hate contraction as simple release; lower right trace is additional voluntary contraction, followed by relaxation.
Single-trial EMG traces were scrutinized for appropriate initiation, duration and termination, and selected into four categories using dialogue mode in Fortran- programme. The first EMG burst initiating contraction, the first increase of the steadily maintained firing and the first steep decline of the ongoing plateau were marked with precision of 7 ms on single trials (see Fig. 1) and the accompanying EEG traces were averaged time-locked to either start or
. .
.
.
of
end of contraction, respectively, using a modified procedure of Popivanov (1986). The beginning and the end of the voluntary effort (marked with vertical bars) were viewed separately. Due to automatic equalizing the images of maintained and additional effort appear of a lower than real amplitudes on the figure. Two sets of 30 to 40 averaged EEG epochs were yielded for every subject and one subject was discarded for reasons of excessive artifacts. The
.
i
i
is termination
.
.
l
.
700
Fig. 2. Brain macropotentials related to tie beginning of sustained isometric contraction (A and C) and to termination either by simple release (B) or by additional voluntary effort (D). Chebyshev’s polynomials of second order are marked with dots below: 1 to 2 - baseline; 2 to vertical bar - preceding negativity (BP); 2 to 3 - onset to peak negativity (BP + NS); 3 to end - resolution towards positivity (MP). Total epoch = 2800 ms. Dwell time = 7 ms. EMC onset/offset at I750 ms, marked with vertical bar. Lead C,.
38
B. Dimitrou et al./Internationul
Journal of Psychophysiology 22 (1996) 35-44
ensuing brain potentials coincided with four distinct contraction phases: (1) initiation of contraction from rest; (2) corresponding simple release; (3) initiation of contraction from rest; (4) corresponding additional effort. The averaged potentials were analysed over an epoch preceding the EMG mark by 1750 ms and following it for another 1050 ms. The initial 350 ms were used as a baseline and the beginning of a steady upward shift was marked as the start of the potential curve to be analysed. The mathematical description of the entire curve was proved to be best achieved by employing second order Chebyshev’s polynomial approximation. The equation: Ax2 + Bx + C provided three coefficients characterizing the slope of the curve (A), the steepness of its rise (B) and the shift over the baseline CC). Positive values of slope suggested upward-bend and negative values downward-bend curves. The incrementing or decrementing rise of the curve was described by its steepness. The shift was related to the magnitude of negativity. Detailed description of the method is given in another paper by Popivanov (1992). Three segments were separately analysed borrowing the nomenclature of Barrett et al. (1986): from onset up to the EMG mark (Bereitschaftspotential, BP); from onset up to the peak negativity (Bereitschaftspotential + Negative Shift, BP + NS); from maximum negativity to the end of epoch (Motor Potential, MP); see also Fig. 2. The onset of the BP was estimated to be the point of ‘take-off’ above the baseline of the polynomial approximation. All coefficients were sub jetted to multiple regression and Student’s t-test analysis.
The termination of the contraction was also preceded by a steady rise in negativity, similar in appearance to that related to the initiation of effort, and was followed by swift downward resolution toward positivity (lower traces). The waveshape of the complex potential remained the same, regardless of the type of termination - simple release or additional contraction. The onset times showed earlier appearance of negativity preceding termination of contraction for both simple relaxation (p < 0.001) and additional contraction ( p < 0.05) in comparison to their respective initiations (Fig. 3). This relationship, however, was significant only for the SMA derivation. The analysis of coefficients characterizing segments’ parameters of Chebyshev’s polynomials revealed quite distinct differences between otherwise similar in appearance waveshapes (Fig. 4). The slope of preceding negativity over the vertex had an upward bend, thus showing incrementing rate of change before the start of contraction (positive values of A, top left), while before the termination the rate of change turned into a decrementing one, with downward bend (negative values of A) and this was significant for both segments BP ( p < 0.05) and BP + NS (p < 0.05). The steepness of preceding negativity (BP + NS) over the midline showed opposite courses before the start of isometric contraction
ONSET T I ME
3. Results A typical set of the four potentials in one subject that is characteristic for the group is shown in Fig. 2. The beginnings of sustained contraction (A and C) are matched with their respective terminations simple release (B) or additional voluntary effort CD). EMG onset/offset was at the 1750ieth ms from the beginning of trace, marked with a vertical bar. The beginning of contraction was preceded by a negative shift and the sustained effort was accompanied by a sustained negativity over the baseline (upper traces).
FELAXATKM
CDOIT~M
FCr Fig. 3. Onset time latencies. Preceding negativity (BP) over the SMA lead (FC,) associated with beginning of sustained contraction (hatched) occurred later than negativity preceding termination (dotted), regardless of its type.
B. DimiWou et al./International
Journal of Psychophysiology 22 (1996) 35-44
(negative increment) and before simple release (positive increment; p < 0.001 for FC, and p < 0.05 for C,, bottom left). The shift above baseline of preceding negativity (BP + NS) showed lesser amplitude preceding simple release in comparison to the beginning of contraction for both midline leads ( p < 0.01 at FC, and p < 0.05 at C,; bottom right). Interestingly enough, this was not valid for BP segment alone, i.e. amplitudes at time EMG = 0 were of equal magnitudes. Thus, both waveshape and amplitude of potentials related to initiation and termination of sustained contraction revealed different patterns. The preceding negativity up to the maximum peak (BP + NS) over the SMA was different in all respects (p < 0.01 for slope, A; p < 0.001 for steepness, B; p < 0.01 for shift, C) between the beginning of sustained contraction and the execution of
39
additional contraction (Fig. 5, left). Over the vertex the steep rise of negativity up to the EMG mark (BP) showed negative correlation between contraction from state of rest and additional contraction (R = -0.808, F = 0.023, t < 0.01 - Fig. 5, top right) and positive correlation between contraction from rest and simple release (R = 0.899, F = 0.003, r < 0.001 - Fig. 5, bottom right). Significant correlations were found for the steepness of decreasing negativity (coefficient B for segment MP) over the contralateral hand area (C,,,) between simple release and additional contraction (R = 0.865, F = 0.008, t < 0.001 - Fig. 6, top left); and for the shift above baseline of decreasing negativity (coefficent C for segment MP) over the SMA (R = 0.902, F = 0.003, I < 0.001 - Fig. 6, bottom left) for the same conditions. The two types of
T-test, coefficients A - slope
-I_ . -3 A
A.BP+NS
BP
Cz; REL
coefficients B - steep
BP+NS;
coefficients C - shift
REL
Fig. 4. Student’s t-test for the three coefficients of Chebyshev’s polynomials: slope of curve (A), Comparisons are between initiation (hatched) and termination (dotted) of sustained contraction.
BP+NS;
REL
steepness (B), shift above baseline CC).
B. Dimitrou et al./lntemational
40
Journal of Psychophysiology 22 (1996) 3544
‘S-test, PAIRED COEFFICIENTS
-’
5
6 A
B
C
FCz; ADD; BP+NS
Fig. 5. Left: Three coefficients for preceding negativity (BP + NS) over the SMA lead (Fe,) during initiation of effort from rest (hatched) and during additional contraction (gray). Right: Polynomial regression of steepness over the vertex lead (C,). Correlations between BPS accompanying initiation of contraction from rest and initiation from state of sustained effort (top) and between BPS preceding the beginning
of sustained contraction and preceding simple release (bottom).
termination of contraction - simple relaxation and additional effort - thus differed only marginally ( p = 0.056) for the amplitude of resolution negativity (MF’) over the SMA (Fig. 6, right).
4. Discussion The experimental results provided a convincing evidence that end-related slow macropotentials of the brain do exist. Their waveshape and magnitude were similar to potentials preceding the decision to act. Furthermore, when measured against their own baseline, i.e. the DC-level established in the course of a sustained contraction, the potentials preceding both simple release and additional contraction were composed of a steady negativity. Similar findings were
reported in our previous works (Gantchev et al., 1982; Gantchev and Dimitrov, 1983). Thus, they should not be regarded as a mere by-product of agonist-antagonist muscle involvement at the task completeion, but rather as related to a separate internal command for cessation of action. Negativity accompanying cessation of sustained motor activity was also reported by Trimmel et al. (1989). The task we have designed employed a persistent visual feedback. In similar conditions demanding decision-making toward the end of the contraction or aiming at a goal (Grunewald-Zuberbier et al., 1980; Grunewald and Grunewald-Zuberbier, 1983; Deecke et al., 1984; McCallum et al., 1989) a prevailing negativity was always observed. Therefore, even superimposed on such negative DC-shift, the potentials elicited in our study were of distinctive magnitude as to allow measurement against their own baseline, different
B. Dimitrou
et al./lnrernutional
Journal
ofPsychophysiology
from rest. This proves first that a possible restrictive ‘ceiling-effect’ (Rebert et al., 1976) was not present and second, that sustained positivities similar to those found in the studies of Otto et al. (1977) and Gantchev et al. (1982) were not very likely to influence the negative-going slope of potentials. A sole possible artifact from the mostly informative and not demanding visual feedback, especially providing the instruction was specifically unrelated with a goal-directed task, could be the somewhat higher amplitude of potentials compared to a ‘pure’ self-paced Bereitschaftspotential; similar DC-shifts were described during visuomotor learning by Deecke et al. (1988). The requirement for brisk action and the visual guidance created a situation similar to the ‘precueing’ isometric contraction of Van Boxtel et al. (1989), that favours earlier increase in negativity while mon-
41
22 (1996) 35-44
itoring the screen. In any event, the major finding that we have sought for was that, regardless of possible DC-level influences, negative shifts related to the termination of voluntary effort did exist. The subsequent elaborate mathematical analysis of Chebyshev’s polynomials provided more intricate details. The slope of the averaged curve and the steepness of its increase did differ between potentials preceding initiation of sustained contraction and potentials preceding its termination. These differences were better expressed alongside midline leads. The difference was obvious when the entire segment up to the maximum peak was considered (BP + NS), while there were no significant differences at the moment of EMG initiation/cessation (BP). This provides further support for the notion of Libet et al. (1981) and Barrett et al. (1986) that, indeed, two
C - shift, MP & Resolution 60 z q &50 q 1
Fig. 6. Top left: Polynomial regression of steepness (B) of decreasing Correlation between simple release and additional contraction shows lack negativity’s shift over the baseline (C) at SMA lead (FC,). Correlation force effect. Right: Student’s r-test for amplitudes of resolution negativity additional contraction shows lack of significance.
negativity (MP) over the contralateral hand motor of force effect. Bottom left: Polynomial regression between simple release and additional contraction (MP) over SMA area (FC,) accompanying simple
ADDITIONAL RELAXATK)N
area (C3+ *). of decreasing shows lack of relaxation and
42
B. Dimitrov et ol./Internationnl
Journal
separate periods of preparation might exist, represented by different components of the compound potential. Since most of the hypotheses concerning the movement related potentials are based on measurements of an arbitrarily taken short segments, preceding the initiation of voluntary contraction, we might stipulate that they could have been based on incomplete data. Although it was determined that the maximum negativity followed the EMG onset (Vaughan et al., 1968; Deecke et al., 1969; Gerbrandt, 1977) it is our impression that not many comparisons were done between those segments separated in time by the EMG occurrence. Neshige et al. (1988) estimated the lag of peaking negativity at around 150 ms, which is comparable with the peak occurrence of BP + NS in our study. Of particular interest was the finding of positive correlation between start and end of the voluntary effort. On the other side, the correlation between start of contraction from state of rest and the additional effort exerted during sustained effort turned out to be negative. Obviously, the contribution of force level for magnitude and shape of the movement related potentials should be considered in terms of subjective involvement (as in McAdam and Seales, 1969; Kutas and Donchin, 19771, rather than the precise amount of the incoming peripheral afferent information. Just measuring the force gradation might not provide significant differences (like in experiments of Kristeva et al., 1989; Gantchev et al., 1987; Trimmel et al., 1989) because in these experiments the factor of influence was not a perceptible difference in subjective involvement. In an earlier experiment of ours (Dimitrov et al., 1987) it was found that the preceding negativity did not differ between biceps contraction and biceps/triceps cocontraction so the conclusion was drawn that it was independent of the muscle mass involved. On the other hand, the requirement to perform selectively, as in this experiment, might influence the magnitude of potentials. The level of negativity is related to the level of task demand or workload (Deecke et al., 1984; McCallum et al,, 1989). It is of interest that there was no difference in negativities preceding simple release and additional contraction at the C3+2 lead - over the hand motor area - which should be mostly linked to physical effort. There were changes in both steepness of the resolution towards positivity (MP)
ofPsychophysiology 22 (1996) 35-44 and its shift over the baseline, the changes being pronounced over the SMA lead. Such dependence of the ensuing positivity on the physical parameters of the task has already been described (Dimitrov, 1985). Most of the significant correlations and differences in Chebyshev’s polynomials parameters were observed over the SMA lead. Following the description of Brinkman and Porter (1983) many studies have found evidence for the role of SMA in the initiation of action and decision making (Wiesendanger, 1986; Deecke, 1987; Brunia and Damen, 1988; Neshige et al., 1988; Ikeda et al., 1993). In our study the termination of action was preceded by an earlier negativity over the SMA in comparison to initiation of contraction, regardless of its type (release or additional effort). The only difference in magnitude of preceding negativity between initiation and termination was also found above SMA and vertex. The marginally significant difference in resolution positivity between simple release and additional contraction was observed only over SMA. All these findings suggest SMA involvement not only in earlier stages of preparation, but also during the control of action. The lack of SMA involvement found in other studies might be attributed to a relatively easy and automatic mode of performance, as in the case of simple repetitive movements, studied by Botzel et al. (1993). In conclusion, it was found that the termination of sustained isometric contraction was accompanied by brain macropotentials of distinctive waveshape, regardless of the type of termination. There occurred differences between potentials accompanying initiation of effort from a state of rest and from a state of maintained force on one side, and there occurred similarities between potentials accompanying termination of effort and potentials accompanying exertion of additional effort, on the other side. The generation of movement related brain potentials should be attributed to central cerebral command for decision to act, rather than to particular task parameters or agonist-antagonist muscle engagement.
References Barrett, G., Shibasaki, H. and Neshige, R. (1986) Cortical potentials preceding voluntary movement: evidence for three peri-
B. Dimitrov et aI./lnternational
JournaI of Psychophysiology
ods of preparation in man. Electroenceph. Clin. Neurophysiol., 63: 327-339. Botzel, K.. Plendl, H., Paulus, W. and Scherg, M. (1993) Bereitschaftspotential - is there a contribution of the supplementary motor area. Electroenceph. Clin. Neurophysiol., 89: 187196. Brinkman, C. and Porter, R. (1983) Supplementary motor area and premotor area of monkey cerebral cortex: functional organization and activities of single neurons during performance of a learned movement. In: J.E. Desmedt (Ed.), Motor Control Mechanisms in Health and Disease. Adv. Neurol., Vol. 39, Raven Pmss, New York, pp. 393-420. Brunia, C.H.M. and Damen, E.J.P. (1988) Distribution of slow brain potentials related to motor preparation and stimulus anticipation in a time estimation task. Electroenceph. Clin. Neurophysiol., 69: 234-243. Deecke, L. (1987) Bereitschaftspotential as an indicator of movement preparation in supplementary motor area and motor cortex. In: R. Porter (Ed.), Motor Areas of the Cerebral Cortex. CIBA Foundation Symposium 132, Wiley, Chichester, pp. 23 l-250. Deecke, L., Scheidt, P. and Komhuber, H.H. (1%9) Distribution of readiness potential, pre.-motion positivity and motor potential of the human cerebral cortex preceding voluntary movement. Exp. Brain Res., 7: 158-168. Deecke, L., Bashore, T., Bnmia, C.H.M., Gmnewald-Zuberbier, E.. Gmnewald, G. and Kristeva, R. (1984) Movement-associated potentials and motor control. Ann. NY Acad. Sci., 398428. Dimitrov, B. (1985) Brain potentials related to the beginning and to the termination of voluntary flexion and extension in man. Int. J. Psychophysiol., 3: 13-22. Dimitrov, B.. Gantchev, G.N. and Popivanov, D. (1987) Movement related brain potentials in sustained isometric voluntary contraction. In: G.N., Gantchev, B. Dimitrov and P. Gatev (Eds.), Motor Control, Plenum Press, New York, pp. 93-98. Gantchev, G.N. and Dimitrov, B. (1983) Brain potentials related to additional isometric contraction. Activ. Nerv. Super. (Praha), 25: 285-292. Gantchev. G.N., Dimitrov, B. and Popivanov, D. (1982) Brain potentials related to voluntary sustained effort. Acta Physiol. Pharmacol. Bulg., 8: 14-22. Gerbrandt, L.K. (1977) Analysis of movement potential components In: J.E. Desmedt (Ed.), Attention, Voluntary Contraction and Event-Related Cerebral Potentials. Progress in Clinical Neurophysiology, Vol. I, Karger, Basel, pp. 174- 188. Gnmewald-Zuberbier, E., Gnmewald, G., Schumacher, H. and Wehler, A. (1980) Scalp recorded siow potential shifts during isometric tamp and hold contractions in human subjects. Pflugers Arch., 389: 55-60. Grunewald, G. and Grunewald-Zubcrbier, E. (1983) Cerebral potentials during voluntary ramp movements in aiming tasks. In: A.W.K. Gaillard and W. Ritter (Eds.), Tutorials in ERP Research - Endogenous Components, Elsevier, Amsterdam, New York, pp. 3 1 l-327. Ikeda, A., Luders, H.O., Burgess, R.C. and Shibasaki. H. (1993)
22 (1996) 35-44
43
Movement-related potentials associated with single and repetitive movements recorded from human supplementary motor area. Electroenceph. Clin. Neurophysiol., 89: 269-277. Kristeva, R. and Becker, W. (1978) Cerebral potentials preceding voluntary isometric force deployments of varying amplitudes. Pfliigers Arch., Suppl. 373: R74. Kristeva, R., Cheyne, D., Lang, W., Lindmger, G. and Deecke, L. (1989) Movement-related potentials accompanying unilateral and bilateral simultaneous movements with different inertial load. In: EPIC IX, Vol. 2, No. 16, Noordwijk, The Netherlands. Kutas, M. and Donchin, E. (1977) The effect of handedness, of responding hand and of response force on the contralateral dominance of the readiness potential. In: J.E. Desmedt (Ed.), Attention, Voluntary Contraction and Event-Related Cerebral Potentials. Progress in Clinical Neurophysiology, Vol. I, S. Karger, Basel, pp. 189-210. Lang, W., Lang, M., Podreka, I., Steiner, M., Uhl, F., Suess, E., Muller, Ch. and Deecke, L. (1988) DC-potential shifts and regional cerebral blood flow reveal frontal cortex involvement in human visuomotor learning. Exp. Brain Res., 71: 353-364. Libet, B., Wright, E.W., Jr. and Gleason, C.A. (1981) Readiness potentials preceding unrestricted ‘spontaneous’ vs pre-planned voluntary acts. Electroenceph. Clin. Neurophysiol., 54: 322335. McAdam, D.W. and Seales, D.M. (1%9) Bereitschaftspotential enhancement with increased level of motivation. Electroenceph. Clin. Neurophysiol., 27: 73-75. McCallum, W.C., Cooper, R. and Pocock, P.V. (1989) Brain DC shifts associated with monitoring a visual display. In: EPIC IX, Vol. 2, No. 13, Noordwijk, ‘The Netherlands. Neshige, R., Luders, H. and Shibasaki, H. (1988) Recording of movement-related potentials from scalp and cortex in man. Brain, 111: 719-736. Otto, D., Benignus, V., Ryan, L. and Leifer, L. (1977) Slow potential components of stimulus, response and preparatory process in man. In: J.E. Desmedt (Ed.), Attention, Voluntary Contraction and Event-Related Cerebral Potentials. Progress in Clinical Neurophysiology, Vol. I, S. Karger, Basel, pp. 211230. Popivauov, D. (1986) Computer detection of EMG edges for synchronization of movement-related brain potentials. Electroenceph. Clin. Neurophysiol., 64: 171- 176. Popivanov, D. (1992) Tie series analysis of brain potentials preceding voluntary movements. Med. Biol. Eng. & Comput., 30: 9-14. Rebert, C., Berry, R. and Merlo, J. (1976) DC potential consequences of induced muscle tension. Effects on contingent negative variation. In: W.C. McCallum and J. Knott (Bds.), The Responsive Brain, John Wright & Sons, Bristol, pp. 126-131. Trimmel, M., Groll-Knapp, E., Streicher, F. and Haider, M. (1989) DC potentials during and after cued, sustained motor activity (muscle tension). In: EPIC IX, Vol. 2, No. 28, Noordwijk, The Netherlands. Van Boxtel, G.J.M., Van den Boogaart. B. and Brunia, C.H.M.
44
B. Dimitrov
( 1989) The effects of precueing
et ol./lnternational
Journal of Psychophysiology 22 (1996) 35-44
isometric contraction speed on the contingent negative variation and reaction time. In: EPIC IX, Vol. 2, No. 23, Noordwijk, The Netherlands. Vaughan, H.B., Jr., Costa, L.D. and Ritter, W. (1968) Topography of human motor potential. Electroenceph. Chn. Neurophysiol., 25: I-10. Wait&erg, H. (1980) Slow potentials related to initiation and inhibition of proprioceptively guided movements. In: H.H.
Komhuber and L. Dee&e (Eds.), Motivation, Motor and Sensory Processes of the Brain: Electrical Potentials, Behaviour and Clinical Use. Progress in Brain Ressearch, Vol. 54, Elsevier, Amsterdam, pp. 183- 186. Wiesendanger. M. (1986) Recent developments in studies of the supplementary motor area of primates. Rev. Physiol. B&hem. Pharmacol., 103: 1-59.