CHA

Neuper & Klimesch (Eds.)

Progress in Brain Research, Vol. 159

ISSN 0079-6123

Copyright r 2006 Elsevier B.V. All rights reserved

PTER 14

ERD/ERS patterns reflecting sensorimotor activationand deactivation

Christa Neuper1,�, Michael Wortz2 and Gert Pfurtscheller3

1Institute of Psychology, University of Graz, Universitatsplatz 2/III, A-8010 Graz, Austria2Austrian Research Institute for Artificial Intelligence (OFAI), Freyung 6/6, A-1010 Vienna, Austria

3Laboratory of Brain–Computer Interfaces, Institute of Knowledge Discovery, Graz University of Technology,Krenngasse 37, A-8010 Graz, Austria

Abstract: Oscillations in the alpha and beta band (o35Hz) show characteristic spatiotemporal patternsduring sensorimotor processing. Whereas event-related desynchronization (ERD) during motor prepara-tion, execution, and imagery can be seen as a correlate of an activated cortical area, event-related syn-chronization (ERS) of frequency components between 10 and 13Hz may represent a deactivated corticalarea or inhibited cortical network, at least under certain conditions. Induced beta rhythms (13–35Hz, betaERS) can be found in sensorimotor areas following both voluntary movement and somatosensory stim-ulation. In a recent study we used different tasks involving execution and imagery of movements of theupper and lower limb to produce activation vs. deactivation/inhibition of the sensorimotor hand area.Sensorimotor interference, as a function of the activation level of the motor cortex, was studied by the useof repetitive median nerve stimulation (MNS) (ISI 1.5 s) in 12 healthy volunteers during the following taskconditions: (i) cube manipulation between thumb and fingers of one hand, (ii) imagined cube manipulation,(iii) continuous foot rotation movements, and (iv) imagined foot movements. EEG was recorded from handand foot representation areas and processed time-locked to MNS (ERD/ERS). In addition, task-relatedband power changes (TRPD/TRPI) were analyzed. We found a clear-cut suppression of the stimulation-induced beta ERS (indicating an enhanced activity state of the sensorimotor areas) during active cubemanipulation and a weaker suppression during cube imagery. Mental imagination of foot movement led toan increase of the hand area mu rhythm, but did not interfere with stimulation-related effects on beta ERS.These findings support that interfering sensorimotor activation and deactivation is reflected in graduatedchanges of induced mu and beta oscillations.

Keywords: mu rhythm; beta oscillations; event-related desynchronization (ERD); event-relatedsynchronization (ERS); voluntary movement; motor imagery; median nerve stimulation

Mu synchronization and desynchronization in

voluntary movement and motor imagery

Voluntary movement is the overt basis of humanbehavior: without movement we cannot walk,communicate, or interact with others. According

�Corresponding author. E-mail: christa.neuper@uni-graz.at

DOI: 10.1016/S0079-6123(06)59014-4 211

to the present view, the brain processes involved ingenerating and controlling movements are accom-plished through parallel distributed processing inmultiple motor areas (for a review, see Dum andStrick, 2005). The study of oscillatory EEG signalsin the sensorimotor and related cortical areas pro-vides a window to how the information processingin multiple neuronal networks may be realized.

212

It is well established that preparation, execution,and also imagination of movement produce anevent-related desynchronization (ERD) over thesensorimotor areas, with maxima in the alphaband (mu rhythm, �10Hz) and beta band(�20Hz) (Jasper and Penfield, 1949; Chatrian etal., 1959; Pfurtscheller and Aranibar, 1977; Neu-per and Pfurtscheller, 1999). The mu ERD is mostprominent over the contralateral sensorimotor ar-eas during motor preparation and extends bilater-ally with movement initiation. ERD during handmotor imagery is very similar to the pre-movementERD, i.e., it is locally restricted to the contralat-eral sensorimotor areas (Neuper and Pfurtscheller,1999). Since ERD of alpha band and beta(o30Hz) frequency components can be viewedas an electrophysiological correlate of an activatedcortical network, prepared to process informationwith an increased excitability of cortical neurons(Lopes da Silva and Pfurtscheller, 1999;Pfurtscheller and Lopes da Silva, 1999), the pre-movement ERD and the ERD during motor im-agery may reflect a similar type of readiness orpresetting of neural networks in sensorimotor ar-eas (Neuper and Pfurtscheller, 2001a).

During movement preparation and execution,desynchronization of alpha band (mu) activity at aspecific cortical location may be accompanied byan increase of synchronization (ERS) in the 10-Hzband over areas not engaged in the task(Pfurtscheller and Neuper, 1994; Pfurtscheller etal., 1996b, 2006). ERS can also be observed afterthe movement, over the same areas that had dis-played ERD earlier (Toro et al., 1994). Because themu rhythm typically occurs in the absence ofprocessing sensory information or motor output, itwas conceived to reflect a cortical ‘‘idling’’ or ‘‘nil-work’’ state (Mulholland, 1995). Therefore, it hasbeen hypothesized that the 10-Hz ERS is producedby deactivated cortical areas and may representidling or inhibitory cortical activity (Pfurtschelleret al., 1996b). This may be the case in cortical areasrepresentative for another modality and in neigh-boring areas that correspond to the same modalityas well. For example, in a movement task a centralERD is accompanied by an occipital ERS and in avisual task an occipital ERD is found in parallelwith a central ERS (Pfurtscheller and Neuper,

1994). Other examples are execution and imagina-tion of foot movement; in both cases very oftenan ERD close to the foot representation area isaccompanied by a synchronization of the handarea mu rhythm (Neuper and Pfurtscheller,2001a). This observation, ERD and ERS occur-ring at the same moment in time in differentscalp locations, was named ‘‘focal ERD/surroundERS’’ (Suffczynski et al., 1999) and interpretedas a type of lateral cortical inhibition of networksnot directly involved in a specific task (see alsoChapter 2, this volume). More recently, it hasbeen shown that mu ERS likely reflects more thanan idling state (for a review, see Pineda, 2005).Exemplarily, a task-related alpha power increase(TRPI) has been found to be related to context-dependent inhibition of extended sensorimotornetworks (Hummel et al., 2002; see also Chapter15, this volume).

Beta rebound following movement and

somatosensory stimulation

Besides the mu rhythm, the central beta rhythmsmay be indicative for the activity state of neuralnetworks in the sensorimotor cortex. The generalfinding is that beta oscillations are desynchronizedduring preparation, execution, and imagination ofa motor act (Pfurtscheller, 1981; Stancak andPfurtscheller, 1996; Neuper and Pfurtscheller,1999). After movement offset, the beta band ac-tivity recovers very fast (o1 s) and short-lastingbeta bursts appear. These beta oscillations, de-scribed also as post-movement beta ERS or ‘‘betarebound’’ (Pfurtscheller et al., 1996a), display ahigh degree in somatotopical specificity (Salmelinet al., 1995; Neuper and Pfurtscheller, 1996; Brov-elli et al., 2002). Recently, Pfurtscheller et al.(2005) reported a distinct spatial distribution ofbeta ERS after different types of motor imagery.The occurrence of a beta rebound related to men-tal motor imagery implies that this activity doesnot necessarily depend on motor cortex outputand muscle activation.

A number of experiments have also shown betaoscillations to be sensitive to somatosensory stim-ulation (Salmelin and Hari, 1994; Salenius et al.,

213

1997; Neuper and Pfurtscheller, 2001b) andpassive movement (Cassim et al., 2001). Resem-bling to voluntary hand movement, stimulation ofthe median nerve can elicit short-lasting bursts ofbeta oscillations that are localized predominantlyin the contralateral hand sensorimotor cortex(Salenius et al., 1997). In general, electrical me-dian nerve stimulation (MNS) above the sensorythreshold can generate two types of cortical re-sponses, a phase-locked (evoked) response local-ized in the postcentral somatosensory cortex(Baumgartner et al., 1991) and a non-phase-locked(induced) response in the form of beta oscillationsin the precentral motor cortex. The latter appearswithin 1 s after the delivery of the stimulusand follows a short-lasting ERD immediatelyafter stimulation. Beta ERS has been reportedin response to median/tibial nerve stimulation(Hari et al., 1996; Neuper and Pfurtscheller,

Fig. 1. (A) Topographical display (nose on top) of grand average ER

(mean frequency band: 15–20Hz). The horizontal line marks the le

stimulation. Band power increase (beta ERS) is indicated by upwa

deflection. (B) Topographical maps of one subject, each representing

(16–20Hz) following tactile stimulation of the index fingertip (electro

finger movement. ‘‘Black’’ indicates beta power increase (ERS). (C)

2001b).

2001b; Brovelli et al., 2002), functional electricalstimulation (FES) producing wrist extension(Muller et al., 2003), and even mere tactile stim-ulation of the finger tip (Pfurtscheller et al., 2001;Cheyne et al., 2003; Gaetz and Cheyne, 2006).

Figure 1(A) shows the topographical display ofbeta band ERD/ERS time courses comparing vol-untary index finger movement and MNS (Neuperand Pfurtscheller, 2001b) and Fig. 1(B) showstopographic maps of one representative subjectwith beta ERS obtained in three different condi-tions: mechanical finger stimulation, electricalnerve stimulation, and voluntary finger movement.In all the conditions the focus of beta ERS wasfound over the contralateral primary sensorimotorcortex. Of interest is the observation that sen-sory stimulation can elicit short-lasting bursts ofbeta oscillations, irrespectively whether it is ac-companied by a visible motor response or not

D/ERS curves comparing movement vs. stimulation of the hand

vel of reference power and the vertical line movement-offset/

rd deflection, band power decrease (beta ERD) by downward

an interval of 125 ms, showing the distribution of beta ERS

de positions are marked), median nerve stimulation, and index

Electrode montage (modified from Neuper and Pfurtscheller,

214

(Pfurtscheller et al., 2001; Stancak et al., 2003).This means that sensory stimulation alone canchange the ongoing activity of beta oscillatorynetworks in the motor cortex (see also Chapter 16,this volume).

The stimulation-related beta ERS can be sup-pressed by various tasks involving motor cortexactivation, e.g., exploratory finger movements(Salenius et al., 1997; Pfurtscheller et al., 2002),motor imagery (Schnitzler et al., 1997) or evenmovement observation (Hari et al., 1998). Fromthese studies we can conclude that not only thepost-movement beta ERS, but also the beta ERSinduced by somatosensory stimulation, reflects as-pects of the functional state of the primary motorcortex. More specifically, these central 20-Hz os-cillations have been interpreted to reflect a short-lasting state of deactivation or inhibition of motorcortex networks (Salmelin et al., 1995). Furthersupport for this assumption comes from studiesusing transcranial magnetic stimulation (TMS), inwhich it was shown that the excitability level ofmotor cortex neurons was significantly reducedwithin the first second after termination of fingermovement (Chen et al., 1998) and after MNS aswell (Chen et al., 1999).

Effects of interfering sensorimotor activation and

deactivation on mu ERD and beta ERS

In a recent study we used repetitive peripheralnerve stimulation to investigate the activity state ofmotor cortex networks during sensorimotor inter-ference. Starting from the hypothesis that the ex-citability of motor cortex circuitry is modulated bymovement execution and motor imagery, the aimof this study was twofold: first, we sought to cor-roborate previous magnetoencephalographic(MEG) findings that activation of the motor cor-tex, by performing or imagining manipulatory fin-ger movements, desynchronizes the central murhythm and suppresses stimulus-induced beta os-cillations (cf. Salenius et al., 1997; Schnitzler et al.,1997). Second, we wanted to extend the previouslyreported results and evaluate the hypothesis thatinhibition of the hand area network, assumedlyproduced by foot movement or foot motor

imagery (Pfurtscheller and Neuper, 1994; Neuperand Pfurtscheller, 2001b), results in a synchroni-zation of the mu rhythm and an enhancement ofthe beta ERS. The idea was to utilize overt motorbehavior and motor imagery of upper vs. lowerlimb to produce a state of activation vs. deactiva-tion/inhibition, respectively, of neuronal networksin the sensorimotor cortex.

In order to evaluate how the activation of thesensorimotor hand area depends on concomitantshort-lasting (i.e., stimulation-induced) vs. long-lasting processes (i.e., movement execution andmotor imagery), we used in this study a combinedapproach of (i) ERD/ERS time frequency analysis(Graimann et al., 2002) and (ii) analyses of task-related power decreases/increases (TRPD/TRPI;Gerloff and Hallett, 1999). Even though ERD/ERS and TRPD/TRPI follow the same rationale,i.e., the analysis of regional changes in oscillatorybrain activity in relation to a certain event, theydiffer in that ERD/ERS focuses on spectral powerchanges time-locked to a single stimulus, whereasTRPD/TRPI concentrates on changes with steady-state processes related to continuous movementexecution or mental imagery (for a discussion of‘‘event-related’’ vs. ‘‘task-related’’ analysis of os-cillatory activity, see Chapter 15, this volume).

Subjects and experimental paradigm

Twelve healthy right-handed volunteers (six menand six women, aged 19–32 years) participated inthe study. Periodic MNS was delivered at the rightwrist in four different experimental conditions,each of which lasted about 3min:

CUBE

MNS and cubemanipulation: The subjectsperformed continuous fingermovements by manipulatinga small cube between thumband fingers of the right hand.

I-CUBE

MNS and cubemanipulation imagination:Participants were instructedto imagine continuously themovement of conditionCUBE.

215

FOOT

MNS and foot movement:The subjects performed acontinuous movement of theright foot in form of a circlewith the heel resting on thefloor.

I-FOOT

MNS and foot movementimagery: Subjects wereinstructed to imagine thefoot movement they had toperform in condition FOOT.

Bipolar ball electrodes with 2.5 cm interelec-trode distance were used for stimulation of theright median nerve. Stimulation was performedwith constant current pulses of 0.2ms durationevery 1.5 s. Before the experiment started, the ad-equate stimulation intensity for stimulating themedian nerve (at the wrist) was adjusted to evoke aslight visible thumb twitch without causing dis-comfort. Each experimental condition was pre-ceded by a 3-min resting period, during whichMNS was repetitively applied without any addi-tional task. Besides the specific task instructions,the participants were asked to sit relaxed with eyesopen and resting arms, and to avoid any move-ments other than requested.

Data recording and processing

The EEG (bandpass between 0.5 and 30Hz) wasrecorded with four electrodes positioned at positions2.5 cm anterior and posterior to C3 and Cz, respec-tively (C3a, C3p, Cza, and Czp), sampled at 2kHz,and converted into bipolar by calculating the differ-ence for the electrode of interest (C3 ¼ C3a–C3p,Cz ¼ Cza–Czp). All data were visually controlledfor artifacts before further processing.

Figure 2 illustrates the influence of periodic me-dian nerve stimulation on rhythmic EEG activities(single EEG trials) in the contralateral hemisphere(C3) during a rest condition. The mu rhythm isattenuated following the stimuli and resynchro-nizes slowly. Examples of post-stimulus betabursts (ERS) can be observed within a few hun-dred milliseconds after stimulation.

Because of interindividual variability in reactivefrequencies, subject-specific frequency bands were

used for subsequent analysis. To this end, ERD/ERS time–frequency maps were calculated for allconditions (for a description of ERD/ERS mapcalculation, see Graimann et al., 2002), and on thebasis of the stimulation-related ERD/ERS valuesobtained for electrode position C3 the reactivefrequency bands were determined for each partic-ipant. In the alpha range, the mean center fre-quency displaying the largest ERD was11.4Hz70.8 (mean7SD); in the beta range, thelargest ERS was found about 19.3Hz71.9(mean7SD).

ERD/ERS time curves were calculated for both,the subject-specific alpha and beta bands, using theintertrial variance method (Kalcher andPfurtscheller, 1995). In the subject-specific alphaband, the maximum alpha ERD with respect tothe reference interval (250–0ms before the trigger)was measured; in the beta band, maximum syn-chronization (ERS) was quantified for furtheranalysis.

Task related power decrease/increase (TRPD/TRPI) for the different task conditions was deter-mined by calculating the variance. For this pur-pose the trials of each condition were bandpassfiltered in the two subject-specific frequency bands,and the overall variance of each condition wascalculated from these filtered data. In order to es-timate the task-related power increase/decrease,each condition with motor or mental task was re-lated to the preceding resting condition.

Stimulation-related band power changes

In Fig. 3 the averaged (thick line) and subject-spe-cific (thin lines) ERD/ERS curves are displayed forall subjects and conditions. Comparing the alphaband (upper panel) and the beta band (lowerpanel) activity, it can be noticed that the beta bandshows a faster time behavior than the alpha band(mu rhythm) and results in a clear beta reboundthat declines back to the baseline before the nextstimulus is delivered (o1.5 s).

We evaluated whether the stimulation-relatedERD/ERS response during the investigated motorand imagery tasks differed significantly from thecorresponding (preceding) rest conditions. Inter-estingly, the mu rhythm ERD yielded significant

Fig. 2. Alpha and beta oscillations as a function of median nerve stimulation during rest (channel C3, one subject). Topmost plot: Raw

EEG signal. 2nd plot: Bandpass filtered signal in the selected alpha range (10–13Hz). It can be seen that the mu rhythm is shortly

attenuated following the stimulus. 3rd plot: Bandpass filtered signal in the selected beta frequency band (15–20Hz). Note that the

stimuli are followed by beta bursts that appear approximately 500 ms after stimulus offset. Bottom plot: stimulation trigger.

216

results only for the cube manipulation task atelectrode position C3 (paired t-test, t ¼ –3.346,df ¼ 11, po0.01). No significance was foundfor the other conditions (see box plots in Fig. 4,upper panel) or for the electrode position Cz.This result indicates that continuous hand move-ment (cube manipulation) significantly reducedthe stimulation-induced mu rhythm changes, spe-cifically over the corresponding hand sensorimo-tor area.

Analysis of the post-stimulus beta ERS showeda highly significant power suppression during cubemanipulation (t ¼ 3.091, df ¼ 11, po0.01) overelectrode C3. A tendency was detected in the datafor cube manipulation imagination (t ¼ 1.967,df ¼ 11, po0.075), whereas both foot-related con-ditions did not alter the beta ERS (compare boxplots in Fig. 3, lower panel).

Task-related power decrease/increase

The task-related band power (TRPD/TRPI)changes of the mu rhythm, referenced to the pre-ceding resting condition, yielded a highly signifi-cant band power decrease for both the cubemanipulation (t ¼ 6.795, df ¼ 11, po0.01) andthe cube movement imagination task (t ¼ 4.608,df ¼ 11, po0.01). Foot movement imagination, incontrast, led to a significant mu power increase(t ¼ –2.215, df ¼ 11, po0.05). Unexpectedly, theperformed foot movement apparently did notchange the alpha power over C3 (Fig. 5, upperpanel).

Figure 5, lower panel, shows the box plots forreferenced beta band power measurement, whichyielded a highly significant decrease for cube ma-nipulation (t ¼ 8.496, df ¼ 11, po0.01) and foot

Fig. 3. Individual (thin lines) and grand average normalized band power changes (thick lines) recorded over C3 and calculated for the

alpha (upper panel) and beta band (lower panels) for all conditions (from left to right: rest 1, cube movement; rest 2, foot movement;

rest 3, cube manipulation imagination; rest 4, foot movement imagination). At time zero the stimulation takes place, reference interval

is from –250 to 0 ms before stimulation.

217

movement (t ¼ 5.241, df ¼ 11, po0.01). Still asignificant difference was found for cube manipu-lation imagination (t ¼ 2.370, df ¼ 11, po0.05).Only foot movement imagination failed to pro-duce a statistically noteworthy result over C3.

Correlation of mu rhythm ERD and beta ERS

The analysis of the relationship between the mag-nitude of the mu ERD and the beta ERS acrosssubjects and conditions gave significant results forcube manipulation (r ¼ 0.6, po0.05) and footmovement (r ¼ –0.654, po0.01) over electrodeC3. The positive correlation between alpha bandERD and beta ERS in the cube manipulation taskindicates that a stronger mu rhythm ERD is as-sociated with a smaller beta ERS. With foot move-ment, in contrast, a negative relationship emerged,in the sense that a stronger mu rhythm ERD

appeared in connection with an enhanced betaERS. Over Cz, no significant correlation betweenmu rhythm ERD and beta ERS could be found.

Discussion and conclusions

Suppression of stimulation-related ERD/ERS bycube manipulation

In agreement with previous findings (cf. Salenius etal., 1997; Neuper and Pfurtscheller, 2001b), theoscillatory brain activity with components in the10- and 20-Hz bands showed the characteristic re-activity pattern to periodic median nerve stimula-tion (during rest), i.e., each stimulus was followedby a transient desynchronization (ERD) and asubsequent rebound (ERS). As noted before, itwas anticipated that complex finger manipulation

Fig. 4. Box plots indicating the distribution of the obtained

values for the maximum mu ERD (upper panels) and the max-

imum post-stimulus beta ERS (lower panels) for electrode po-

sition C3 for all conditions (from left to right: rest 1, cube

movement; rest 2, foot movement; rest 3, cube manipulation

imagination; rest 4, foot movement imagination). Each box

represents the mean 50% between the lower and upper quartile

values; the median is indicated by a line. Significant differences

are marked by a double arrow.

Fig. 5. Box plots indicating the distribution of the obtained

values for the referenced band power of mu (upper panels) and

the referenced task-specific beta band power change (lower

panels) for electrode position C3 for all conditions (from left to

right: rest 1, cube movement; rest 2, foot movement; rest 3, cube

manipulation imagination; rest 4, foot movement imagination).

Each box represents the mean 50% between the lower and up-

per quartile values; the median is indicated by a line. Significant

differences are marked by a double arrow.

218

as well as the mental simulation of this task wouldresult in activation of the hand motor cortex and,therewith, desynchronize the central mu rhythmand suppress stimulus-induced beta bursts. In fact,continuous finger movement, in comparison to theresting condition, reduced the stimulus-related muERD. The beta ERS was completely abolishedduring cube manipulation, and there was also atendency found for the cube imagination task.

This is in line with previously reported MEG datashowing that imagination of manipulatory fingermovements attenuates the 20-Hz activity to alesser extent than actually executed finger move-ments (Schnitzler et al., 1997).

The picture of sensorimotor interference be-comes even clearer when changes of steady-stateprocesses also are considered, i.e., based on theband power decreases/increases during the wholetime periods of task performance (TRPD/TRPI;Gerloff and Hallett, 1999). Compared to the

219

preceding resting condition, the band power in thereactive alpha and beta bands decreased substan-tially during active cube manipulation, but also, toa smaller degree, in the cube movement imagina-tion task. This observation confirms that the men-tioned task conditions resulted in a long-lastingactivation (i.e., enhanced activity state) of neuron-al networks in sensorimotor areas, especially in thecase of active cube manipulation. Furthermore,the ongoing desynchronization (blocking) of alphaband activity gives an explanation for the reducedstimulus-related mu-rhythm ERD during cubemanipulation. Similarly, the reduced level of on-going beta band activity during task performancemay facilitate the suppression of the stimulation-induced beta ERS.

The clear-cut suppression of the stimulation-in-duced beta ERS during sensorimotor interferenceindicates that at least two processes may playa role for the magnitude of the beta ERS (elic-ited by median nerve stimulation of constant in-tensity): a central mechanism increasing the levelof activation in the primary motor cortex (e.g., thegeneration of a motor command, and the involve-ment of cortico-cortical or cortico-subcortical cir-cuits) and the modulation of the afferent inputfrom the limb (e.g., by a gating mechanism at thethalamocortical level, e.g., Brunia, 1993, or Fu etal., 2001). The former is expected to result in ac-tivation of the motor cortex, irrespective ofwhether the motor behavior is really executed oronly imagined. The latter may account for thecomplete suppression of the beta ERS duringactive movement (cube manipulation). Gatingof attention during the active motor task can re-duce the sensory input from the peripheral nervestimulation or the awareness thereof (cf. Cheronand Borenstein, 1987; Brunia, 1993; Mima et al.,1998;) and, thereby, further attenuate the betaERS (Pfurtscheller et al., 2002).

Enhancement of the hand area mu rhythm by footmotor imagery

Starting from the concept termed ‘‘focal ERD/surround ERS’’ (Suffczynski et al., 1999, 2001),which emphasizes the idea of simultaneous ac-tivation and deactivation/inhibition of locally

restricted cortical regions, the present study con-trasted the effects of directing the focus of atten-tion onto the upper vs. lower limb, thus drawingon distinct sensorimotor cortical areas. Concen-tration on foot movement as well as foot motorimagery was expected to activate the cortical footarea along with a deactivation/inhibition of thehand area network, since the latter is presumablynot involved to perform the task (Pfurtscheller andNeuper, 1994; Neuper and Pfurtscheller, 2001a).Consequently, we expected a synchronization ofthe mu rhythm over the hand area, while subjectsconcentrated on the foot.

Although neither foot movements nor foot mo-tor imagery had an impact on the reactivity pat-terns of ERD/ERS computed time-locked tomedian nerve stimulation, in the task-related bandpower significant changes occurred. The foot im-agery task led to a significant increase of the handarea mu rhythm, but the actually performed footmovements did not change the alpha band powerover the hand area. Of interest is, that the 10-Hzsynchronization during foot motor imagery wasonly significant for the hand area (C3), but notfound for the midline scalp location (Cz), whichprobably overlies the foot area localized in themesial cortex.

The distinct reactivity patterns, i.e., decrease(ERD) vs. increase in synchrony (ERS), associatedwith (mental) concentration on the hand vs. foot,respectively, provide further support for the ‘‘focalERD/surround ERS’’ phenomenon (Suffczynski etal., 1999, 2001), which was simulated by an ex-tended version of the lumped model initially pro-posed by Lopes da Silva et al. (1974). Theantagonistic ERD/ERS pattern may be interpretedin the light of a thalamocortical mechanism tofacilitate focal cortical activation (‘‘focal ERD’’)by a simultaneous deactivation or inhibition ofsurrounding cortical areas, which are outside thefocus of attention (‘‘surround ERS’’). In this re-spect the demands of the task may be of im-portance. It can be assumed, for instance, that ac-tual executed foot movements became habitualover time during task performance and, therefore,required less attention than the motor imagerytask. Given the distractive input from the repeti-tive stimulation of the median nerve, foot motor

220

imagery probably requires more mental effort toavoid disturbance. As a result, stronger mu en-hancement, as expression of top–down processes,is more likely.

A very interesting aspect is that the reactive al-pha (mu) components are found in the upper alphaband with a center mean frequency above 11Hz.Upper alpha or mu components typically show amovement-specific and locally restricted desyn-chronization during voluntary limb movement(Pfurtscheller et al., 2000), in contrast to the morewidespread ERD of lower alpha components. Itwas reasoned that the upper alpha frequency com-ponents reflect a mechanism responsible for selec-tive attention to a motor subnetwork. This effectof selective attention to one motor subnetwork(e.g., foot area) may be accentuated when othermotor subnetworks (e.g., hand area) are ‘‘inhib-ited.’’ This is in agreement with more recent stud-ies showing that especially the frequency band11–13Hz displays ERS in the hand area, when thesubject is engaged in another motor task (i.e., ex-ecution or imagination of foot or tongue move-ments; see Pfurtscheller et al., 2006), or withholdspre-learned finger movements (Hummel et al.,2002). On the basis of a combined approach ofEEG task-related power and TMS cortical excit-ability analysis, Hummel et al. (2002) substanti-ated that the enhanced 11–13Hz mu componentsin the hand representation area are instrumentalfor inhibitory control at the cortical level (see alsoChapter 15, this volume).

Both mu and beta responses showed in principlethe same patterns with an initial ERD followed bya rebound in the form of an ERS. The mu ERDhad the greatest magnitude about 400 ms afterstimulation, whereas the beta ERS displayed amaximum about 600 ms after stimulation. Thedegree of reactivity of mu and beta rhythms (mag-nitudes of the mu ERD and beta ERS to somato-sensory stimulation) was correlated, but showeddifferential effects dependent on the task. In thecube manipulation task (focus of attention ontocube manipulation and therewith activation of thehand motor cortex), a stronger mu rhythm ERDwas associated with a smaller beta ERS. Whenthe stimulus-induced beta ERS is associated witha short-latency deactivation (inhibition) of the

motor cortex, it can be expected that a long-lastingactivation of the motor cortex should not onlydesynchronize the mu rhythm, but also counter-balance the short-lasting inhibition and suppressthe beta ERS (Hari et al., 1998; Pfurtscheller et al.,2002).

During foot movement, however, a stronger murhythm ERD was correlated with an enhancedbeta ERS. Since alpha and beta power changesusually have the same direction, this finding re-quires an explanation. One reason could be thatthe foot movement task in this study presumablydid not implicate deactivation of the hand area.Previous studies reported, on the one hand, a rel-atively widespread mu rhythm ERD during self-paced foot movement, covering also the hand rep-resentation area (Arroyo et al., 1993; Toro et al.,1994; Pfurtscheller et al., 2000). On the other hand,an increase (ERS) of the upper alpha band(10–13Hz) or mu activity over the hand areawas observed, when foot movement was only onepossible behavioral response, to be executed in de-pendence of a cue stimulus, indicating the re-quested type of movement (Pfurtscheller andNeuper, 1994). Comparable effects, in terms ofhand area mu rhythm enhancement, have beenreported, when the subjects imagined foot move-ments and ‘‘suppressed’’ imagery of hand move-ments, respectively (Neuper and Pfurtscheller,2001a). This task-related aspect may further ex-plain that in the present study, only the more de-manding foot motor imagery task, but not theexecution of continuous foot movements, resultedin an increase of the hand area mu rhythm. An-other point to consider is that beta ERS over themotor cortex hand area was not only found relatedto movement, imagery, or stimulation of the cont-ralateral hand, but was further observed to be co-activated during toe and lip stimulation (Gaetz andCheyne, 2006). These examples raise the possibilitythat, independent of the somatotopic representa-tion, the hand area of the precentral gyrus playsalso a more general role in sensorimotor control.

From the present and former results we sum-marize that there is evidence for an inhibition ofneuronal networks in the hand representationarea during imagination of foot movement. Thisinhibition results in a divergent behavior of mu and

221

beta activities, i.e., in an enhanced synchronizationof the hand area mu rhythm, but not, as expected,in enlarged stimulus-induced beta oscillations.

Acknowledgments

This study is part of the ongoing PhD thesis of oneof the authors (M.W.) and has been supported bythe ‘‘Fonds zur Forderung der wissenschaftlichenForschung’’, project P14831.

References

Arroyo, S., Lesser, R.P., Gordon, B., Uematsu, S., Jackson, D.

and Webber, R. (1993) Functional significance of the mu

rhythm of human cortex: an electrophysiological study with

subdural electrodes. Electroencephalogr. Clin. Ne-

urophysiol., 87: 76–87.

Baumgartner, C., Doppelbauer, A., Deecke, L., Barth, D.S.,

Zeitlhofer, J., Lindinger, G. and Sutherling, W.W. (1991)

Neuromagnetic investigation of somatotopy of human hand

somatosensory cortex. Exp. Brain Res., 87: 641–648.

Brovelli, A., Battaglini, P., Naranjo, J. and Budal, R. (2002)

Medium-range oscillatory network and the 20-Hz sensori-

motor induced potential. NeuroImage, 16: 130–141.

Brunia, C.H.M. (1993) Waiting in readiness: gating of attention

and motor preparation. Psychophysiology, 30: 327–339.

Cassim, F., Monaca, C., Szurhaj, W., Bourriez, J.L., Defebvre,

L., Derambure, P. and Guieu, J.D. (2001). Does post-move-

ment beta synchronization reflect an idling motor cortex?

Neuroreport, 12: 3859–3863.

Chatrian, G., Petersen, M. and Lazarete, J. (1959) The blocking

of the rolandic wicket rhythm and some central changes related

to movement. Electroenceph Clin. Neurophysiol., 11: 497–510.

Chen, R., Corwell, B. and Hallett, M. (1999) Modulation of

motor cortex excitability by median nerve and digit stimu-

lation. Exp. Brain Res., 129: 77–86.

Chen, R., Yaseen, Z., Cohen, L.G. and Hallett, M. (1998) Time

course of corticospinal excitability in reaction time and self-

paced movements. Ann. Neurol., 44: 317–325.

Cheron, G. and Borenstein, S. (1987) Specific gating of the early

somatosensory evoked potentials during active movement.

Electroenceph. Clin. Neurophysiol., 67: 537.

Cheyne, D., Gaetz, W., Garnero, L., Lachaux, J.P., Ducorps,

A., Schwartz, D. and Varela, F.J. (2003) Neuromagnetic im-

aging of cortical oscillations accompanying tactile stimula-

tion. Brain Res. Cogn. Brain Res., 17: 599–611.

Dum, R.P. and Strick, P.L. (2005) Motor areas in the frontal

lobe: the anatomical substrate for the central control of

movement. In: Vaadia, E. and Riehle, A. (Eds.) Motor Cor-

tex in Voluntary Movements: A Distributed System for Dis-

tributed Functions. Series: Boca Ration, Methods and New

Frontiers in Neuroscience. CRC Press, Boca Raton, pp. 3–47.

Fu, K.M., Foxe, J., Murray, M., Higgins, B., Javitt, D. and

Schroeder, C. (2001) Attention-dependent suppression of

distracter visual input can be cross-modally cued as indexed

by anticipatory parieto-occipital alpha-band oscillations.

Cogn. Brain Res., 12: 145–152.

Gaetz, W. and Cheyne, D. (2006) Localization of sensorimotor

cortical rhythms induced by tactile stimulation using spatially

filtered MEG. Neiuroimage, 30: 899–908.

Gerloff, C. and Hallett, M. (1999) ERD and coherence of

sequential movements and motor learning. In: Pfurtscheller,

G., Lopes da Silva, F.H. (Eds.), Event-Related Desyn-

chronization. Handbook of Electroencephalography and

Clinical Neurophysiology. Vol. 6. Elsevier, Amsterdam, pp.

327–339.

Graimann, B., Huggins, J.E., Levine, S.P. and Pfurtscheller, G.

(2002) Visualization of significant ERD/ERS patterns in

multichannel EEG and ECoG data. Clin. Neurophysiol.,

113: 43–47.

Hari, R., Forss, N., Avikainen, E., Salenius, S. and Rizzolatti,

G. (1998) Activation of human primary motor cortex during

action observation: a neuromagnetic study. Proc. Natl. Acad.

Sci. USA,, 95: 15061–15065.

Hari, R., Nagamine, T., Nishitani, N., Mikuni, N., Sato, T.,

Tarkiainen, A. and Shibasaki, H. (1996) Time-varying acti-

vation of different cytoarchitectonic areas of the human SI

cortex after tibial nerve stimulation. NeuroImage, 4:

111–118.

Hummel, F., Andres, F., Altenmuller, E., Dichgans, J. and

Gerloff, Ch. (2002) Inhibitory control of acquired motor

programmes in the human brain. Brain, 125: 404–420.

Jasper, H. and Penfield, W. (1949) Electrocorticograms in man:

effect of the voluntary movement upon the electrical activity

of the precentral gyrus. Arch. Psychiatr. Z Neural., 183:

163–174.

Kalcher, J. and Pfurtscheller, G. (1995) Discrimination between

phase-locked and non-phase-locked event-related EEG ac-

tivity. Electroenceph. Clin. Neurophysiol., 94: 381–384.

Lopes da Silva, F.H., Hoeks, A., Smits, H. and Zetterberg,

L.H. (1974) Model of brain rhythmic activity. the alpha-

rhythm of the thalamus. Kybernetic,, 15: 27–37.

Lopes da Silva, F.H. and Pfurtscheller, G. (1999) Basic con-

cepts on EEG synchronization and desynchronization. In:

Pfurtscheller G. and Lopes da Silva F.H. (Eds.), Event-Re-

lated Desynchronization. Handbook of Electroencephalo-

graphy and Clinical Neurophysiology. Revised Edition Vol.

6. Elsevier, Amsterdam, pp. 3–11.

Mima, T., Nagamine, T., Nakamura, K. and Shibasaki, H.

(1998) Attention modulates both primary and second so-

matosensory cortical activities in humans: a magnetoencep-

halographic study. J. Neurophysiol., 80: 2215.

Mulholland, T. (1995) Human EEG, behavioral stillness and

biofeedback. Int. J. Psychophysiol., 19: 263–279.

Muller, G., Neuper, C., Rupp, R., Keinrath, C., Gerner, H. and

Pfurtscheller, G. (2003) Event-related beta EEG changes

during wrist movements induced by functional electrical

stimulation of forearm muscles in man. Neurosci. Lett., 340:

143–147.

222

Neuper, C. and Pfurtscheller, G. (1996) Post-movement syn-

chronization of beta rhythms in the EEG over the cortical

foot area in man. Neurosci. Lett., 216: 17–20.

Neuper, C. and Pfurtscheller, G. (1999) Motor imagery and

ERD. In: Pfurtscheller G. and Lopes da Silva F.H. (Eds.),

Event-Related Desynchronization. Handbook of Electroen-

cephalography and Clinical Neurophysiology. Revised Edi-

tion Vol. 6. Elsevier, Amsterdam, pp. 303–325.

Neuper, C. and Pfurtscheller, G. (2001a) Event-related dynam-

ics of cortical rhythms: frequency-specific features and func-

tional correlates. Int. J. Psychophysiol., 43: 41–58.

Neuper, C. and Pfurtscheller, G. (2001b) Evidence for distinct

beta resonance frequencies in human EEG related to specific

sensorimotor cortical areas. Clin. Neurophysiol., 112:

2084–2097.

Pfurtscheller, G. (1981) Central beta rhythm during sensory

motor activities in man. Electroenceph. Clin. Neurophysiol.,

51: 253–264.

Pfurtscheller, G. and Aranibar, A. (1977) Event-related

cortical desynchronization detected by power measurements

of scalp EEG. Electroenceph. Clin. Neurophysiol., 42:

817–826.

Pfurtscheller, G., Brunner, C., Schlogl, A. and Lopes da Silva,

F.H. (2006) Mu rhythm (de)synchronization and EEG single-

trial classification of different motor imagery tasks. Neuro-

Image, 31: 153–159.

Pfurtscheller, G., Krausz, G. and Neuper, C. (2001) Mechanical

stimulation of the fingertip can induce bursts of beta oscil-

lations in sensorimotor areas. J. Clin. Neurophysiol., 18:

559–564.

Pfurtscheller, G. and Lopes da Silva, F.H. (1999) Functional

meaning of event-related desynchronization (ERD) and syn-

chronization (ERS). In: Pfurtscheller, G. and Lopes da Silva,

F.H. (Eds.) Event-Related Desynchronization. Handbook of

Electroencephalography and Clinical Neurophysiology, Vol.

6. Elsevier, Amsterdam, pp. 51–65.

Pfurtscheller, G. and Neuper, C. (1994) Event-related synchro-

nization of mu rhythm in the EEG over the cortical hand

area in man. Neurosci. Lett., 174: 93–96.

Pfurtscheller, G., Neuper, C., Brunner, C. and da Silva, F.H.

(2005) Beta rebound after different types of motor imagery in

man. Neurosci. Lett., 378: 156–159.

Pfurtscheller, G., Neuper, C. and Krausz, G. (2000) Functional

dissociation of lower and upper frequency mu rhythms in

relation to voluntary limb movement. Clin. Neurophysiol.,

111: 1873–1879.

Pfurtscheller, G., Stancak, A. and Neuper, C. (1996a) Post-

movement beta synchronization. A correlate of an idling

motor area? Electroenceph. Clin. Neurophysiol., 98: 281–293.

Pfurtscheller, G., Stancak, A. and Neuper, C. (1996b) Event-

related synchronization (ERS) in the alpha band — an elect-

rophysiological correlate of cortical idling: a review. Int. J.

Psychophysiol., 24: 39–46.

Pfurtscheller, G., Woertz, M., Muller, G., Wriessnegger, S. and

Pfurtscheller, K. (2002) Contrasting behavior of beta event-

related synchronization and somatosensory evoked poten-

tials after median nerve stimulation during finger manipula-

tion in man. Neurosci. Lett., 323: 113–116.

Pineda, J.A. (2005) The functional significance of mu rhythm:

translating ‘‘seeing’’ and ‘‘hearing’’ into ‘‘doing’’. Behav. Res.

Rev., 50: 57–68.

Salenius, S., Schnitzler, A., Salmelin, R., Jousmaki, V. and

Hari, R. (1997) Modulation of human cortical rolandic rhythms

during natural sensorimotor tasks. Neuroimage, 5: 221–228.

Salmelin, R. and Hari, R. (1994) Characterization of sponta-

neous MEG rhythms in healthy adults. Electroenceph. Clin.

Neurophysiol., 91: 237–248.

Salmelin, R., Hamalainen, M., Kajola, M. and Hari, R. (1995)

Functional segregation of movement related rhythmic activ-

ity in the human brain. Neuroimage, 2: 237–243.

Schnitzler, A., Salenius, S., Salmelin, R., Jousmaki, V. and

Hari, R. (1997) Involvement of primary motor cortex in mo-

tor imagery: a neuromagnetic study. Neuroimage, 6:

201–208.

Stancak Jr, A. and Pfurtscheller, G. (1996) Event-related de-

synchronisation of central beta rhythms during brisk and

slow self-paced finger movements of dominant and nondom-

inant hand. Cogn. Brain Res., 4: 171–183.

Stancak, A., Svoboda, J., Rachmanova, R., Vrana, J., Kralik,

J. and Tintera, J. (2003) Desynchronization of cortical

rhythms following cutaneous stimulation: effects of stimulus

repetition and intensity, and of the size of corpus callosum.

Clin. Neurophysiol., 114: 1936–1947.

Suffczynski, P., Kalitzin, S., Pfurtscheller, G. and Lopes da

Silva, F.H. (2001) Computational model of thalamo-cortical

networks: dynamical control of alpha rhythms in relation to

focal attention. Int. J. Psychophysiol., 43(1): 25–40.

Suffczynski, P., Pijn, J.P., Pfurtscheller, G. and Lopes da Silva,

F.H. (1999) Event-related dynamics of alpha band rhythms: a

neuronal network model of focal ERD/surround ERS. In:

Pfurtscheller, G. and Lopes da Silva, F.H. (Eds.) Event-Re-

lated Desynchronization. Handbook of Electroencephalo-

graphy and Clinical Neurophysiology, Vol. 6. Elsevier,

Amsterdam, pp. 67–85.

Toro, C., Deuschl, G., Thatcher, R., Sato, S., Kufta, C. and

Hallett, M. (1994) Event-related desynchronization and

movement-related cortical potentials on the ECoG and

EEG. Electroenceph. Clin. Neurophysiol., 93: 380–389.