Event-related beta synchronization after wrist, finger and thumb movement

Electroencephalography and clinical Neurophysiology 109 (1998) 154–160

Event-related beta synchronization after wrist, finger and thumb movement Gert Pfurtscheller a , b ,*, Karin Zalaudek b, Christa Neuper b a

Department of Medical Informatics, Institute for Biomedical Engineering, University of Technology, Brockmanng. 41, A-8010 Graz, Austria b Ludwig Boltzmann-Institute for Medical Informatics and Neuroinformatics, Brockmanng. 41, A-8010 Graz, Austria Accepted for publication: 8 October 1997

Abstract Pre-movement event-related desynchronization (ERD) and post-movement event-related synchronization (ERS) were studied in a group of normal subjects during voluntary thumb, index finger and wrist movement. The band power time courses were computed for the upper alpha band (10–12 Hz) and for two frequency bands in the range of beta (16–20 Hz and 20–24 Hz). While a similar mu ERD was found during motor preparation for the 3 movement tasks, significant differences concerning beta synchronization were observed after movement off set. The contralateral percentage beta increase (ERS) was significantly larger in gross movements of the wrist as compared to index finger and thumb movements, which is discussed under the assumption of a cumulative effect. Summarizing, pre-movement desynchronization seems relatively independent of the forthcoming type of movement, whereas the post-movement beta synchronization might depend on the activated muscle mass.  1998 Elsevier Science Ireland Ltd. Keywords: Event-related desynchronization (ERD); Event-related synchronization (ERS); Voluntary movement; Beta oscillations

1. Introduction Besides the Bereitschaftspotential (Kornhuber and Deecke, 1965), two other phenomena in the EEG are characteristic for self-paced movement. One is the event-related desynchronization (ERD) of mu and central beta rhythms starting about 2 s prior to movement onset (Jasper and Penfield, 1949; Gastaut, 1952; Chatrian et al., 1959; Pfurtscheller, 1989), the other is the event-related synchronization (ERS) after termination of movement (Pfurtscheller, 1981; Pfurtscheller et al., 1996). The post-movement beta ERS is an especially interesting phenomenon because of its high task-specificity and its relatively strict localization to primary motor areas (Salmelin and Hari, 1994; Salmelin et al., 1995; Stanca´k Jr. and Pfurtscheller, 1996a; Pfurtscheller et al., 1997). Both phenomena have already been studied with voluntary finger and hand movement (Pfurtscheller, 1981; Toro et al., 1994b; Pfurtscheller et al., 1996, 1997; Stanca´k Jr. and Pfurtscheller, 1996a), though they were not explicitly investigated in one study. Compared to movement of the wrist, finger and thumb movements are quite different not only * Corresponding author. Tel.: +43 316 8735311; fax: +43 316 812964; e-mail: [email protected]

0924-980X/98/$19.00  1998 Elsevier Science Ireland Ltd. All rights reserved PII S0924-980X (97)0007 0-2

concerning moved mass and involved muscle force, but also concerning the afferent activity. The postcentral representation of proximal joints might be relatively large and more pronounced and thus might involve a larger area than the representation of distal joints (Mountcastle and Powell, 1959). Therefore, differences in the beta oscillations can be expected with different types of movement. The purpose of this paper was to study the pre-movement ERD and the post-movement ERS in a group of normal subjects during self-paced voluntary finger, thumb and wrist movements. The results of this study should (i) give a better understanding of cortical networks involved in the generation of beta oscillations and (ii) also help to compare movement studies in patients with Parkinson’s disease where thumb or wrist movements have already been investigated (Defebvre et al., 1993, 1994, 1996; Diez et al., 1996).

2. Methods and subjects 2.1. Subjects Eleven healthy subjects (mean age 24.4 years, SD = 3.3) participated in the experiment. Due to artifacts caused by

EEM 97665

G. Pfurtscheller et al. / Electroencephalography and clinical Neurophysiology 109 (1998) 154–160

muscular activity during the course of the recording, the data of two subjects had to be excluded from further analysis. ERD was missing in the data of one subject, thus the effective sample consisted of data from 8 subjects for calculation of ERD and 9 subjects for studying beta ERS. According to self-report, they were all right-handed. Subjects were paid for their participation. 2.2. Experimental paradigm Prior to the EEG measurement the subjects were informed about the procedure and purpose of the experiment. The subjects were sitting in a comfortable semireclining armchair, that was positioned in a darkened and electrically isolated room. During the EEG recording, the subjects kept their eyes closed. They were trained to perform self-paced brisk movements in intervals of 12–15 s before the experimental sessions. In each subject’s session, the 3 following types of movement were investigated: (i) a brisk extension and flexion of the right index finger, (ii) a brisk pressing of a button on a joystick with the right thumb, and (iii) a brisk 45° flexion of the right wrist with brisk return to the resting position. Therefore, the hand was vertically positioned in a hand-splint and the forearm was placed on an arm rest (a similar type of wrist movement as used by Defebvre et al., 1996 in their clinical studies). Each session comprised 70–80 movements. After each session, the subjects were given a break of about a quarter of an hour for relaxation and a training for the subsequent task. 2.3. EEG recording and data processing The EEG was recorded with 23 sintered Ag/AgCl electrodes, using an extended electrode montage (Fig. 1A). The electrodes were placed according to sites of the international 10–20 system, and additional positions according to the American Electroencephalographic Society (Niedermeyer

155

and Lopes da Silva, 1993). The EEG data were recorded with the right mastoid as reference. The EEG signals were amplified by a BEST system (Grossegger) with a time constant of 0.3 s and an upper cut-off frequency of 50 Hz, whereby electrode impedances were kept below 5 kQ. The surface electromyogram (EMG) was recorded bipolarly with sintered Ag/AgCl electrodes (7 mm diameter). For index finger movement, the electrodes were placed distal at about one third of the distance between the elbow and wrist on the m. digitorum profundus of the right ventral forearm. For thumb movement, the m. flexor pollicis brevis, caput superficiale served as point of recording, and the m. brachioradialis for wrist movements with the hand-splint. EMG signals were amplified by a Neurofax (Nihon Kohden) EEG apparatus with a time constant of 0.1 s and an upper cut-off frequency of 1000 Hz. The EMG was rectified and full-wave integrated by a contour follower. EEG and integrated EMG as well as rectangular trigger signals were digitized at 128 Hz and stored on optical disk. To obtain reference-free EEG data, orthogonal source derivations were calculated (Hjorth, 1975). For each movement two 8 s periods, one starting 5 s before movement onset (registered by the trigger-flank) and the other starting 5 s before movement offset were analyzed. The first interval was used to quantify the premovement desynchronization (ERD), the second interval related to movement offset was used to measure the postmovement EEG changes. The raw EEG data was visually controlled for artifacts, before it was digitally band pass filtered, squared and averaged across trials and consecutive samples to obtain 8 band power values per second. Details on data processing are reported elsewhere (Kalcher and Pfurtscheller, 1995). The percentage band power changes for each sample, relative to band power in the reference interval (0.5–1.5 s; R in Fig. 1B and C), which is assigned to 100%, were calculated. A power decrease is represented as an ERD, while power increase results in an ERS. Percentage power changes are displayed in the form of time

Fig. 1. Electrode montage (A), time course for movement onset and calculation of ERD (B), and time course for movement offset and calculation of ERS (C).

156

G. Pfurtscheller et al. / Electroencephalography and clinical Neurophysiology 109 (1998) 154–160

the repeated measures, the Greenhouse-Geisser epsilon correction of degrees of freedom was applied if required (Vasey and Thayer, 1987).

3. Results 3.1. Duration of movement

Fig. 2. Integrated EMG for the 3 movement tasks of one subject. EMG for gross movements with the wrist shows larger amplitudes compared to finger and thumb movements indicating the activation of a larger muscle mass. The trigger is schematically displayed below the EMG.

courses. The comparison of the above reported movement tasks (finger, thumb and wrist) was carried out for the following 3 frequency bands: upper mu rhythm (10–12 Hz) and two bands in the range of beta (16–20 Hz and 20–24 Hz). The 10–12 Hz band was chosen because of its task specificity (Klimesch et al., 1992), while between 16 and 24 Hz, the largest post-movement beta oscillations were reported (Pfurtscheller et al., 1996; Stanca´k Jr. and Pfurtscheller, 1996a). As movements were only performed with the right hand, and since electrode C3 was expected to show maximal ERD and ERS (Pfurtscheller et al., 1997), statistical analysis was carried out for this electrode. As a control, the corresponding position over the right hemisphere (C4) was included in the analysis. 2.4. Statistical analysis The main focus of the statistical analysis was to compare pre-movement mu desynchronization and post-movement beta synchronization during and after different kinds of movement, respectively. Absolute as well as relative band-power changes (ERD/ERS) in the 3 frequency bands were studied using analysis of variance for repeated measures (ANOVA). Two intervals in the time course of ERD and ERS, each averaged over 1 s, were used as variables for the 3 movement tasks. For the study of pre-movement mu ERD, two 1 s periods before movement onset (t1: 3–4 s and t2: 4–5 s; Fig. 1B) were analyzed, while two 1 s periods after termination of movement (t1: 5.5–6.5 s; Fig. 1C) were analyzed with regard to beta ERS. The factors (i) Movement (finger versus thumb versus wrist), (ii) Hemisphere (C3 versus C4) and (iii) Period (two levels in the actual time course of ERD/ERS) as repeated measures variables were analyzed separately for the mu rhythm and the two beta bands. Main effects as well as interactions between factors were analyzed using Newman-Keuls post-test. According to

According to the mean duration of the different kinds of movement a one-way ANOVA for repeated measures indicated significant differences between the 3 tasks (F(2,16) = 37.76, P , 0.01). As expected, the movement time for wrist movements (686 ± 102 ms) lasted significantly longer than movements with the thumb (194 ± 29 ms) or finger (330 ± 192 ms). Wrist flexions took more than twice the time of movements with the index finger (P , 0.01) and about three times the time of thumb movements (P , 0.01). However, finger and thumb movements also differed significantly with regard to movement time (P , 0.05). An example of the integrated EMG activity for the 3 movement tasks of one subject is shown in Fig. 2. 3.2. Band power in the reference interval A two-way ANOVA for repeated measures (Movement × Hemisphere) was computed separately in each of the 3 frequency bands with regard to values during the reference period (0.5–1.5 s). Regarding power values in the 10–12 Hz band, no significant main effects or interactions between the variables were observed, indicating similar means of absolute power values for the 3 movement tasks throughout the reference interval. In both of the analyzed beta bands (16–20 Hz and 20–24 Hz) the same results were observed, showing again comparable values throughout the reference period for the 3 movement tasks and electrode positions. 3.3. Differences during movement preparation For the comparison of the movement tasks concerning differences in pre-movement ERD, a three-way ANOVA (Movement × Hemisphere × Period) was performed in the 10–12 Hz band. Significant main effects were observed for the variables Hemisphere and Period, indicating significantly larger ERD over the left as compared to the right Table 1 Results of the 3 way ANOVA in the 10–12 Hz band Results of the three way ANOVA

Hemisphere

Period

Hemisphere × Period

10–12 Hz

F(1,7) = 11.01*

F(1,7) = 24.97** F(1,7) = 31.59**

F-values and significance level for the main effects and interactions. *P , 0.05; **P , 0.01.

157

G. Pfurtscheller et al. / Electroencephalography and clinical Neurophysiology 109 (1998) 154–160

Table 2). Referring to these results the variables Period and Hemisphere showed significant effects as expected, while in contrast, pre-movement ERD showed no significant differences depending on movement task. Thus motor preparation is similar for the 3 evaluated movements in the 10– 12 Hz band. Grand average ERD curves for all 3 types of movement evaluated in the 10–12 Hz band are displayed in Fig. 3. As can be seen, the ERD is most pronounced on electrode C3 (contralateral) and starts immediately before movement onset on electrode C4 (ipsilateral). 3.4. Differences in post-movement beta synchronization

Fig. 3. Grand average ERD curves (thick line) in the on-triggered 10–12 Hz band were superimposed on the plot of the individual ERD curves (thin lines) of 8 subjects. Data recorded at electrodes C3 and C4 are displayed for the 3 movement tasks (index finger, thumb and wrist). The horizontal line indicates 0% and the vertical line movement onset.

hemisphere (P , 0.05) and stronger desynchronization at t2 (P , 0.01) as compared to t1 (3–4 s), thus 1 s before movement onset (4–5 s). This result was also qualified by the significant interaction between Hemisphere × Period. Fvalues for the main effects and interactions are shown in Table 1. Concerning the analyzed periods, a larger ERD was found 1 s before movement onset. Post-hoc comparisons indicated significant differences between both intervals (t1 and t2) over C3 (P , 0.05) and C4 (P , 0.01) as well as differences between C3 and C4 at the analyzed intervals t1 (P , 0.01) and t2 (P , 0.05). Overall, the largest ERD was found within finger movement, followed by movement of the thumb and wrist, though there were no significant differences concerning desynchronization during movement preparation (Fig. 3,

According to the results of the 3-way ANOVA (Movement × Period × Hemisphere) in the 16–20 Hz range, significant main effects for Movement and for Hemisphere as well as significant interactions between Movement × Hemisphere and Hemisphere × Period were found. F-values for main effects and interactions are shown in Table 3. Posttests of the interaction Hemisphere × Period showed similar results as those found in the analyzed pre-movement mu band, although these concern synchronization (larger ERS over C3 as compared to C4; P , 0.05). The positions C3 and C4 differed at both of the analyzed intervals (t1: 5.5–6.5 s and t2: 6.5–7.5 s) as well as the periods on both of the electrodes (for all comparisons: P , 0.01). A larger power increase is found after movement of the wrist compared to movements of the thumb and index finger (Table 2). According to the interaction of Movement × Hemisphere, post-movement power increase shows no difference between movements of the index finger and thumb on either electrode, while both of these tasks differed significantly from movements of the wrist (P , 0.01) over C3 (Table 3, Fig. 4). For the 20–24 Hz band comparable results were observed with significant main effects for the variables Movement and Hemisphere and a significant interaction between Movement × Hemisphere (see also Tables 2 and 3). Hence, independent of the analyzed period (t1 and t2), post-movement beta synchronization is remarkably larger in movements of the wrist as compared to finger and thumb movements over the contralateral hemisphere (Fig. 5). The grand average time courses in Fig. 4 not only display the largest ERS with hand movement, but also the clear contralateral dominance of the post-movement beta oscillations on electrode C3.

Table 2 Percentage decrease (ERD) for the 10–12 Hz band and percentage increase (ERS) for the 16–20 and 20–24 Hz bands of the 3 movement tasks for electrodes C3 and C4 Percentage power change

Decrease (ERD) 10–12 Hz Increase (ERS) 16–20 Hz Increase (ERS) 20–24 Hz

Wrist, mean (±SE)

Thumb, mean (±SE)

Finger, mean (±SE)

C3

C4

C3

C4

C3

C4

55 (8) 282 (52) 250 (50)

26 (17) 51 (24) 46 (31)

63 (7) 64 (19) 43 (18)

24 (11) 13 (10) 5 (11)

66 (6) 98 (26) 51 (24)

32 (10) 24 (13) 12 (17)

Values are averaged across the two analyzed periods in the time course of ERD (3–4 s and 4–5 s) and ERS (5.5–6.5 s and 6.5–7.5 s).

158

G. Pfurtscheller et al. / Electroencephalography and clinical Neurophysiology 109 (1998) 154–160

Table 3 Results of the 3 way ANOVA in the 16–20 Hz and 20–24 Hz bands Results of the three-way ANOVA

Movement

Hemisphere

Movement × Hemisphere

Hemisphere × Period

16–20 Hz 20–24 Hz

F(2,16) = 11.03** e = 0.55 F(2,16) = 9.32* e = 0.60

F(1,8) = 17.37** F(1,8) = 20.91**

F(2,16) = 15.26**e = 0.67 F(2,16) = 14.77** e = 0.78

F(1,8) = 11.47** –

F-values and significance level for the main effects and interactions.

4. Discussion Two main results were found: (i) similar pre-movement ERD with wrist, finger and thumb movement and (ii) significantly increased post-movement beta ERS with wrist as compared to finger and thumb movement. Given the relationship between scalp EEG amplitudes and synchronized neural activity on the one hand and the size of the primary motor upper limb area on the other hand, the similar time courses of desynchronization before movement onset during different kinds of movement can be expected. The excited cortical area is of about the same size in movements of a single finger and movements of the whole hand. Large mu amplitudes on the scalp require the cooperative activation of cortical neurons in an area of at least several square centimeters (Cooper et al., 1965). An

Fig. 4. Grand average ERS curves (thick line) in the off-triggered 16–20 Hz band were superimposed on the plot of the individual ERS curves (thin lines) of 9 subjects. Data recorded at electrodes C3 and C4 are displayed for the 3 movement tasks (index finger, thumb and wrist). The horizontal line indicates 0% and the vertical line movement offset.

area of similar size (about 5.5 cm2) was found to be representative for finger, wrist and arm movement. These various movements were triggered by electrical stimulation from a cortical area of around 5.5 cm along the Rolandic fissure in a band of 1 cm (Penfield and Boldrey, 1937). This finding indicates that the majority of neurons in the hand area may become excited during preparation for single finger as well as wrist movement. However, the existence of only one hand area mu rhythm in each hemisphere is questionable, taking the results of Toro et al. (1994a) into account. They found, in cortical recordings, that the direction and amplitude of arm movement was coded in the 8–12 Hz activity. In addition to the hand area mu rhythm, which exists independently in both hemispheres (Storm van Leeuwen et al., 1978), there are other types of mu rhythms locally blocked by foot or face movement (Arroyo et al., 1993; Pfurtscheller and Neuper, 1994).

Fig. 5. Plot of the two-way interactions Movement × Hemisphere in the 10–12 Hz, 16–20 Hz and 20–24 Hz band. ERS after wrist movement is significantly larger as compared to finger and thumb movement on electrode C3 while there are no differences concerning pre-movement ERD.

G. Pfurtscheller et al. / Electroencephalography and clinical Neurophysiology 109 (1998) 154–160

The relative non-specificity of the mu rhythm ERD in scalp recordings of finger and wrist movement is supported by two other observations. Stanca´k Jr. and Pfurtscheller (1996b) investigated the effects of brisk and slow finger extensions on sensorimotor rhythms. They found a similar pre-movement ERD pattern with both types of movement although the efferent output for a brisk movement is concentrated whereas a slow movement involves a sustained control during the motor act. Stanca´k Jr. et al. (1997) also investigated the influence of external loads on index finger movement and found no significant change of mu rhythm ERD with increasing load (in contrast to the mu rhythm, the central beta rhythm was significantly affected by increasing loads). The pre-movement mu ERD, starting more than 2 s prior to voluntary movement onset, may reflect a type of general readiness or presetting of sensorimotor neurons, needed to execute a forthcoming movement. Different movement properties such as type (finger versus wrist), speed (brisk versus slow) and force are supposedly not coded in detail in the mu ERD. After the termination of movement, significant differences were found between wrist and finger movement. The beta rhythm showed larger amplitudes (more pronounced synchronization) after wrist as compared to index finger and thumb movement. The most evident interpretation of this finding is that the differences between the 3 movement tasks in post-movement ERS are related to the movement duration. Indeed, the movement time was significantly different among the 3 types of movement, with the shortest movement duration being the thumb and the longest movement duration being the wrist movement. However, as with slow (movement time of about 1.7 s) and brisk (movement time of about 0.2 s) finger flexions a similar beta ERS was already reported (Pfurtscheller et al., 1997), the enhanced beta ERS with wrist movement can not be explained by the longer movement time. The control of finger movement involves a large number of muscle spindles, whereas for the movement of the wrist, in particular, muscle force is necessary. Therefore more mass of muscular fibers has to be activated, which can be seen in the EMG (Fig. 2). Finger movement is accompanied by cutaneous, but also proprioceptive afferences, whereas wrist movement results in more proprioceptive activity from the joints. For the activation of a larger muscle mass, a relatively larger population of cortical neurons is required. Our finding of larger beta oscillations with wrist as compared to finger or thumb movement can be understood as the change of a larger population of motor cortex neurons from an increased neural discharge during the motor act to a state of cortical disfascilitation or cortical idling. In this ‘idling’ state pyramidal tract neurons are not only ‘reset’ and centrally generated motor programs are cancelled, but perhaps also reafferent activity is processed and consolidated. Large amplitudes of rhythms in the alpha band on the scalp require a synchronized, or nearly synchronized, activ-

159

ity over a cortical area of at least several square centimeters (Cooper et al., 1965). However, not all of the cortical elements need to be involved in the coherent activity, small fractions of cortical neurons distributed over some square centimeters are sufficient. Amplitudes of beta rhythms are about 10 times smaller than amplitudes of the mu rhythm. This means that cortical neurons displaying coherent beta activity are organized in smaller patches, as compared to mu rhythms generating neural elements. As a first approximation, a 10 times smaller amplitude can be related to a 10 times smaller cortical area of coherent activity. Thus, a cortical area of, for example, 5 cm2 responsible for the mu rhythm generation may correspond to about 50 mm2 for the generation of beta waves. About 50 mm2 of the cortical area could be a realistic estimation for the sensorimotor control of one finger, while approximately 5.5 cm2 in the Rolandic fissure is estimated for the control of the total upper limb area (Penfield and Boldrey, 1937). Therefore, we can speculate that along with the mu rhythm, a number of beta rhythms with different reactivity patterns exist in each hand area. Considering, for example, each finger has its own specific beta generating network, the simultaneous movement of two or more fingers is expected to result in a larger beta ERS than the movement of only one finger. The large beta ERS with wrist movement may therefore be explained as the result of a cumulative effect. The differentiation between the postulated different beta rhythms during the preparatory period is not always possible because of the superposition of ‘real’ beta rhythms and beta rhythms related to the first harmonic mu components (Pfurtscheller et al., 1997). This differentiation is, however, likely in the post-movement period, when the mu rhythm is still desynchronized and recovers only slowly from desynchronization, whereas the beta rhythm recovers fast and becomes maximally synchronized approximately 0.6 s after termination of the motor act. A comparison between self-paced flexion of the index finger and of the digits 2–5 (4-finger flexion) was reported by Salmelin et al. (1995). They observed not only a similar pre-movement ERD, but also a similar post-movement beta increase with one finger as well as 4-finger flexion. In contrast to our study, they recorded derivates of the magnetic field and the intervals between finger movements were relatively short, approximately 3 s. It is of interest to note, however, that the maximum of the beta field rebound was found 0.8–1.1 s after movement onset and the contralateral field amplitude increase was approximately 40% (this amplitude increase corresponds to a power increase of 96%). When from the latency of 0.8–1.1 s, the movement time of about 0.2 s is subtracted, the beta peak is comparable to the latency observed in our data of approximately 0.6 s after movement offset. Compared to the EMG study, the maximal beta power increase with one finger movement in our study was nearly of double size (around 200%). To determine whether these amplitude differences are due to the different intervals between movements or to differences

160

G. Pfurtscheller et al. / Electroencephalography and clinical Neurophysiology 109 (1998) 154–160

in the measurements of magnetic field and electrical potentials needs further research. Summarizing, we can state that beta ERS is relatively independent of duration and speed of movement, yet it significantly depends on which part of the hand (finger, wrist, etc.) is moved and thus might be related to the mass of muscles involved.

Acknowledgements We would like to thank Britta Ortmayr for the layout of the figures and Sonja Ebner for help with manuscript preparation. This work was made possible through the financial support of the Austrian ‘Fonds zur Fo¨rderung der wissenschaftlichen Forschung (FWF)’, project P11571.

References Arroyo, S., Lesser, R.P., Gordon, B., Uematsu, S., Jackson, D. and Webber, R. Functional significance of the mu rhythm of human cortex: an electrophysiological study with subdural electrodes. Electroenceph. clin. Neurophysiol., 1993, 87: 76–87. Chatrian, G.E., Petersen, M.C. and Lazarte, J.A. The blocking of the rolandic wicket rhythm and some central changes related to movement. Electroenceph. clin. Neurophysiol., 1959, 11: 497–510. Cooper, R., Winter, A.L., Crow, H.J. and Grey, W.W. Comparison of subcortical, cortical and scalp activity using chronically indwelling electrodes in man. Electroenceph. clin. Neurophysiol., 1965, 18: 217–228. Defebvre, L., Derambure, P., Bourriez, J.L., Jacquesson, J.M., Dujardin, K., Destee, A. and Guieu, J.D. Spatiotemporal study of event-related desynchronization in idiopathic Parkinson’s disease. Adv. Neurol., 1993, 60: 422–428. Defebvre, L., Bourriez, J.L., Dujardin, K., Derambure, P., Destee, A. and Guieu, J.D. Spatiotemporal study of Bereitschaftspotential and eventrelated desynchronization during voluntary movement in Parkinson’s disease. Brain Topogr., 1994, 6: 237–244. Defebvre, L., Bourriez, J.L., Destee, A. and Guieu, J.D. Movement-related desynchronization pattern preceding voluntary movement in untreated Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry, 1996, 60: 307– 312. Diez, J., Pfurtscheller, G., Reisecker, F., Holzner, B., Zalaudek, K. and Kalcher, J. Event-related desynchronization in idiopathic Parkinson’s disease. Third International Hans Berger Congress, Friedrich Schiller University, Jena, Germany, October 3–6, 1996. Gastaut, H. Etude electrocorticographique de la reactivite des rhythmes rolandiques. Rev. Neurol., 1952, 87: 176–182. Hjorth, B. An on-line transformation of EEG scalp potentials into orthogonal source derivations. Electroenceph. clin. Neurophysiol., 1975, 39: 526–530. Jasper, H.H. and Penfield, W. Electrocorticograms in man: effect of the voluntary movement upon the electrical activity of the precentral gyrus. Arch. Psychiat. Z. Neurol., 1949, 183: 163–174. Kalcher, J. and Pfurtscheller, G. Discrimination between phase-locked and non-phase-locked event-related EEG activity. Electroenceph. clin. Neurophysiol., 1995, 94: 381–384.

Klimesch, W., Pfurtscheller, G. and Schimke, H. Pre- and poststimulus processes in category judgement tasks as measured by event-related desynchronization (ERD). J. Psychophysiol., 1992, 6: 186–203. Kornhuber, H.H. and Deecke, L. Hirnpotentiala¨nderungen bei Willku¨rbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale. Pflu¨gers Arch., 1965, 284: 1–17. Mountcastle, V.B. and Powell, T.B. Central nervous mechanisms subserving position sense and kinesthesis. Bull. John Hopkins Hosp., 1959, 105: 173–200. Niedermeyer, E. and Lopes da Silva, F. (Eds.) Electroencephalography: Basic Principles, Clinical Applications and Related Fields. Williams and Wilkins, Baltimore, 1993, p. 105. Penfield, W. and Boldrey, E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain, 1937, 60: 389–443. Pfurtscheller, G. Central beta rhythm during sensory motor activities in man. Electroenceph. clin. Neurophysiol., 1981, 51: 253–264. Pfurtscheller, G. Functional topography during sensorimotor activation studied with event-related desynchronization mapping. J. Clin. Neurophysiol., 1989, 6 (1): 75–84. Pfurtscheller, G. and Neuper, C. Event-related synchronization of mu rhythm in the EEG over the cortical hand area in man. Neurosci. Lett., 1994, 174: 93–96. Pfurtscheller, G., Stanca´k, A. Jr. and Neuper, C. Post-movement beta synchronization. A correlate of an idling motor area?. Electroenceph. clin. Neurophysiol., 1996, 98: 281–293. Pfurtscheller, G., Stanca´k, A. Jr. and Edlinger, G. On the existence of different types of central beta rhythms below 30 Hz. Electroenceph. clin. Neurophysiol., 1997, 102: 316–325. Salmelin, R. and Hari, R. Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement. Neuroscience, 1994, 60: 537–550. Salmelin, R., Ha¨ma¨la¨inen, M., Kajola, M. and Hari, R. Functional segregation of movement-related rhythmic activity in the human brain. Neuroimage, 1995, 2: 237–243. Stanca´k Jr., A. and Pfurtscheller, G. Event-related desynchronization of central beta rhythms during brisk and slow self-paced finger movements of dominant and non-dominant hand. Cogn. Brain Res., 1996a, 4: 171– 183. Stanca´k, Jr. A. and Pfurtscheller, G. The effect of handedness and type of movement on the contralateral preponderance of mu-rhythm desynchronization. Electroenceph. clin. Neurophysiol., 1996b, 99: 174–182. Stanca´k, Jr. A., Riml, A. and Pfurtscheller, G. The effects of external load on movement-related changes of the sensorimotor EEG rhythms. Electroenceph. clin. Neurophysiol., 1997 (in press). Storm van Leeuwen, W., Wieneke, G., Apoelstra, P. and Versteeg, H. Lack of bilateral coherence of mu rhythm. Electroenceph. clin. Neurophysiol., 1978, 44: 140–146. Toro, C., Cox, C., Frichs, G., Ojakangas, C., Maxwell, R., Gates, J.R., Gumnit, R.J. and Ebner, T.J. 8–12 Hz rhythmic oscillations in human motor cortex during two-dimensional arm movements: evidence for representation of kinematic parameters. Electroenceph. clin. Neurophysiol., 1994a, 93: 390–403. Toro, C., Deuschl, G., Thatcher, R., Sato, S., Kufta, C. and Hallett, M. Event-related desynchronization and movement-related cortical potentials on the ECoG and EEG. Electroenceph. clin. Neurophysiol., 1994b, 93: 380–389. Vasey, M. and Thayer, J. The continuing problem of false positives in repeated measures ANOVA in psychophysiology. Psychophysiology, 1987, 24: 85–93.