Behavioural Brain Research - Semantic Scholar to a twelve-items version of the Oldfield Edinburgh handedness inventory [26]. They all provided written, informed consent to participate

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Behavioural Brain Research 271 (2014) 365–373

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Behavioural Brain Research

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esearch report

ost-switching beta synchronization reveals concomitant sensoryeafferences and active inhibition processes

tienne Sallarda,∗, Jessica Talletb, Gregor Thutc, Marie-Pierre Deiberd,e, Jérôme Barrala

Research Group of Institute of Sport Sciences University of Lausanne (GRISSUL), University of Lausanne, Lausanne, SwitzerlandPRISSMH-LAPMA, University of Toulouse3, Toulouse, FranceInstitute of Neuroscience and Psychology, University of Glasgow, Glasgow, United-KingdomINSERM U1039, Faculty of Medicine, La Tronche, FranceClinical Neurophysiology and Neuroimaging Unit, Division of Neuropsychiatry, Department of Psychiatry, University Hospitals of Geneva, Geneva,witzerland

i g h l i g h t s

Electrical neuroimaging shows beta synchronization after selective inhibition.Beta synchronization in a restricted-band (22–26 Hz) within left parietal cortex.Beta synchronization in a broad-band (14–30 Hz) within right pre-frontal cortex.Beta synchronization is related to active inhibition and sensory reafferences.

r t i c l e i n f o

rticle history:eceived 13 May 2014eceived in revised form 28 May 2014ccepted 29 May 2014vailable online 24 June 2014

eywords:nhibitory controllectroencephalographyime-frequency analysisource estimations

a b s t r a c t

It is known that post-movement beta synchronization (PMBS) is involved both in active inhibition and insensory reafferences processes. The aim of this study was examine the temporal and spatial dynamics ofthe PMBS involved during multi-limb coordination task. We investigated post-switching beta synchro-nization (assigned PMBS) using time-frequency and source estimations analyzes. Participants (n = 17)initiated an auditory-paced bimanual tapping. After a 1500 ms preparatory period, an imperative stim-ulus required to either selectively stop the left while maintaining the right unimanual tapping (Switchcondition: SWIT) or to continue the bimanual tapping (Continue condition: CONT). PMBS significantlyincreased in SWIT compared to CONT with maximal difference within right central region in broad-band14–30 Hz and within left central region in restricted-band 22–26 Hz. Source estimations localized theseeffects within right pre-frontal cortex and left parietal cortex, respectively. A negative correlation showedthat participants with a low percentage of errors in SWIT had a large PMBS amplitude within right pari-etal and frontal cortices. This study shows for the first time simultaneous PMBS with distinct functions in

different brain regions and frequency ranges. The left parietal PMBS restricted to 22–26 Hz could reflectthe sensory reafferences of the right hand tapping disrupted by the switching. In contrast, the right pre-frontal PMBS in a broad-band 14–30 Hz is likely reflecting the active inhibition of the left hand stopped.Finally, correlations between behavioral performance and the magnitude of the PMBS suggest that betaoscillations can be viewed as a marker of successful active inhibition.

© 2014 Elsevier B.V. All rights reserved.

. Introduction

Electro-cortical recordings in normal human adults show thatmplitudes of alpha and beta rhythms are modulated over theensorimotor cortex before, during and following the execution

∗ Corresponding author. Tel.: +41 21 692 36 23; fax: +41 21 692 32 93.E-mail address: [email protected] (E. Sallard).

ttp://dx.doi.org/10.1016/j.bbr.2014.05.070166-4328/© 2014 Elsevier B.V. All rights reserved.

of voluntary movement [1–4]. During unilateral limb movement,these modulations are characterized by a reduction of ampli-tude during the preparation and execution phases (event-relateddesynchronization, ERD) followed by an increase of amplitudesynchronization once the movement is completed (event-related

synchronization, ERS; also called post-movement beta synchro-nization, PMBS). More specifically, alpha and beta ERD start about2 s before the voluntary movement over the contralateral sensor-imotor areas and extends bilaterally with movement initiation.

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66 E. Sallard et al. / Behavioural B

he PMBS occurs approximately 1 s after movement terminationver the contralateral sensorimotor areas [2,5–8]. While converg-ng studies confirm that alpha and beta ERD are related to corticalctivations [6,9,10], the significance of the PMBS is unclear. It isroposed that the PMBS could reflect cortical inhibition [4,9,11,12]nd/or sensory reafference processing [1,13–15].

The hypothesis of sensory reafferences processing emergesecause large PMBS is observed after median nerve stimulation oractile stimulations of the finger [13,16,17]. Houdayer et al. [13]sed a task in which participants either performed right index fin-er extension or received electrical stimulation on the index fingerr on the median nerve. A PMBS (13–25 Hz) was observed in all con-itions, with more intensity for finger extension and median nervetimulation than for index finger stimulation. Authors concludedhat the PMBS is related to reafference information and dependsn the type and quantity of the afferent inputs. The work of Cas-im and collaborators [1] illustrated the relation between PMBS andensory reafferences during active and passive movements (involv-ng no motor cortex activity) as well as during passive movementsollowing deafferentation by ischemic nerve block. They reportedimilar magnitude of PMBS (13–25 Hz) after active and passiveovements and the suppression of PMBS after passive movementsith deafferentation. Authors concluded that the PMBS cannot

olely be related to pure motor deactivation but may involve therocessing of sensory reafferences. However, Alegre and colleagues18] showed that during a sequence of right hand movements, theMBS emerged in left central region only once the whole actionas finished and not after each sequential movement. This result

ndicates that the PMBS might be more closely related to the ter-ination of the motor plan (inhibition process) than to the sensory

eafferences processes.In line with the conclusion of Alegre and colleagues [18], oth-

rs studies suggest that the PMBS is related to inhibitory processes.recisely, PMBS has been related to deactivation (also called idlingtate or resting state) or active inhibition processes. Despite a clearistinctness between these processes, PMBS related to active inhi-ition has been suggested during motor imagery or execution ofoordination tasks [11,19,20] and Go/No-go task [12] while PMBSelated to deactivation has been observed during discrete voluntaryovements task [3,4,9,21].The PMBS related to deactivation processes have been observed

fter movement termination. Pfurtscheller and collaborators [9]howed that the PMBS (around 20 Hz) was maximal over theontralateral hemisphere after voluntary self-paced right manualovements and hypothesized to a deactivation processes. Using

ranscranial magnetic stimulation (TMS) on hand area, Chen et al.22] corroborates the deactivation hypothesis by showing a reduc-ion of excitability of the contralateral motor cortex within the firstecond after termination of a finger movement. A more recent studynvestigates the PMBS in a Go/No-go task in which participants

ere required to respond with a brisk foot movement at a Go stim-lus or to withhold foot movement at a No-go stimulus [12]. Theesults reveal a PMBS in both conditions suggesting that the PMBSs not exclusively observed after the termination of movement butlso during the withholding of prepared action. In the No-go con-ition, the PMBS is likely to stand for a more active processing

nvolved in the inhibitory control of human motor behavior.The PMBS associated to active inhibition processes have been

bserved during execution of alternated movements betweeneveral limbs. Pfurtscheller and collaborators [11] reported simul-aneous alpha/beta ERD and PMBS in a task where participantsave been invited to perform either a hand or a foot movement

n response to visual stimulation. During foot movements, an ERD10–12 Hz) occurred in the foot area with a concomitant PMBSaround 20 Hz) in the hand area. All occurs as if the PMBS refers ton active inhibition of the effector that does not move. In another

esearch 271 (2014) 365–373

study, Pfurtscheller and Neuper [19] instructed the participantsto imagine movements with the right or the left hand accord-ing to a visual stimuli. Again, these authors found an ipsilateralPMBS (around 20 Hz) during the imagined movement. The ipsilat-eral PMBS was interpreted as an active inhibition of motor areato prevent any movement from the resting hand. TMS studiesalso evidenced active inhibition processes during repetitive manualmovements [23,24]. In the study from Stinear and Byblow [24], par-ticipants performed index movements auditory paced (1 Hz) withthe dominant hand while TMS is applied over the ipsilateral pri-mary motor cortex (M1) not involved in the movement. Resultsshowed an increase of intracortical inhibition in the ipsilateral M1during the unilateral index movements. Authors concluded thatthe increased intracortical inhibition in the ipsilateral M1 mightactively prevent unwanted homologous muscle activation in orderto prevent motor interference. More recently, active inhibition wasevidenced in a motor switching task [20]. Using task-related spec-tral power measures, authors showed an increase of beta power(13–30 Hz) over the frontal area during switching from anti-phaseto in-phase bimanual coordination, supporting the occurrence ofan intentional inhibition of the more complex anti-phase to theless complex in-phase coordination. Finally, in Cremoux et al. [25],decreased PMBS (13–31 Hz) amplitude in participants with spinalcord injury was associated to longer time to inhibit voluntary con-tractions.

All in all, according to the two inhibitory processes describeabove, one can view the neural deactivation as a closed door (weaccompany someone to leave the room and we close the door) whileactive inhibition might refer to a door being kept closed (we accom-pany someone to leave the room and we stay behind the door toprevent the person to come in again).

Up to now, there are several evidences that the PMBS repre-sents both sensory reafferences and motor inhibition processes.The present study proposes to examine the temporal and spatialdynamics of PMBS associated with sensory reafferences and activeinhibition processes during a switching task from a bimanual in-phase to an unimanual tapping. The switching task involves theselective stopping of one hand’s tapping while maintaining theactivation of the tapping of the other hand. The switching signalwas presented during the ongoing bimanual tapping movement,ensuring that motor responses were initiated before being selec-tively inhibited. We hypothesize that sensory reafference processesmay be evidenced after switching by the presence of a PMBS inthe sensorimotor region contralateral to the hand continuing theunimanual tapping [4,13] while active inhibition processes maytake place in relation to the stopping hand, producing an ipsilateralPMBS in the motor regions [11].

2. Materials and methods

2.1. Participants

Seventeen young adults (9 males; aged 25 ± 3 years,mean ± standard deviation (SD)) participated in the study. Allparticipants had normal or corrected-to-normal vision, werefree of medication and none reported a history of major medicaldisorders, sustained head injury, psychiatric or neurological dis-orders, alcohol or drug abuse. They were all right-handed (90 ± 8)according to a twelve-items version of the Oldfield Edinburghhandedness inventory [26]. They all provided written, informed

Code of Ethics of the World Medical Association (Declaration ofHelsinki, 18 July 1964) and the Ethics Committee of the canton ofVaud (University of Lausanne) for research on human participantsapproved all experimental procedures.

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.2. Stimuli

Visual stimuli were presented at the center of the screen with gray background at 60 cm from the participants. Two loudspeak-rs placed at 50 cm from the participants delivered the tones of theuditory metronome (2 Hz; high-pitched tones: 4000 Hz) for thehole duration of each trial (10 s). A trial consisted in presenta-

ion of a visual start stimulus (white cross fixation) displayed for aandom duration between 4500 ms and 6000 ms, followed by theresentation of a visual preparatory stimulus (displayed until thend of the trial, 4000 ms to 5500 ms duration). An imperative audi-ory stimulus (low-pitched tone 500 Hz; 80 dB), which replaced theigh-pitched tones of the metronome, occurred at a fixed interval of500 ms after the preparatory stimulus. The preparatory stimulusas either a green cross (Switch condition: “SWIT”; 70 trials) or a

ed cross (Continue condition: “CONT”; 70 trials. Fig. 1). We ensuredhat each participant was able to easily discriminate the imperativetimulus tone from the metronome beats. Stimulus delivery andesponse recording were controlled by Presentation 14.4 softwareNeurobehavioral System, Albany, CA).

.3. Procedure and task

The switching paradigm was designed to assess the PMBSuring a selective inhibition in a tapping task. At the beginningf each trial, participants produced a bimanual (BM) in-phasendex fingers’ tapping on a keyboard in synchronization with theuditory metronome. Each trial engaged BM tapping at the starttimulus following by a preparatory period. During the prepara-ory period, participants had either to prepare to selectively stophe left index while continuing the tapping with the right indexSWIT condition), or to maintain the bimanual tapping (CONTondition). Thus, participants switched from BM to unimanualUM) tapping in the SWIT condition, whereas they continuedhe BM tapping in the CONT condition. The action of switchingr continuing had to be executed after the imperative stimulusFig. 1).

Participants performed a familiarization block of eight trialsfour trials in each condition) before starting the proper exper-

ment, which included 5 blocks of 28 trials (70 trials in eachondition). Conditions were randomly assigned. A rest period ofpproximately 60 s was proposed to the participants between eachlock. The whole experiment lasted approximately 40 min.

ig. 1. Switching paradigm. Stimuli were a 2 Hz metronome (high-pitched tone) during thross fixation) following by a preparatory stimulus (green or red cross fixation accordingtimulus (low-pitched tone). The electroencephalographic time period analyzed is underliFor interpretation of the references to color in this figure legend, the reader is referred to

esearch 271 (2014) 365–373 367

2.4. Electrophysiological recordings and data pre-processing

Continuous EEG was recorded at a sampling rate of 2048 Hzthough 64-channels Biosemi ActiveTwo amplifier system (Biosemi,Amsterdam, Netherlands). This system is referenced to the Com-mon Mode Sense (CMS; active electrode) and the Driven Right Leg(DRL; passive electrode) which replace the ground electrodes con-ventionally used. The CMS-DRL electrodes form a feedback loopwhich drive the average reference potential of the subject as closeas possible to amplifier zero. Electrode impedances were keptbelow 5 k�. Eye blinks were recorded by two electrodes placedabove and below the right eye.

Offline analyses were performed with BESA software (MEGISSoftware, Inc., Gräfelfing, Munich). Continuous EEG data were cor-rected for eye blinks and artifacts through an automatic correctionof artifacts accounting for EOG activities. Bad electrodes were inter-polated using spherical spline interpolation. On average, 8.7% ofthe 64 electrodes were interpolated. Raw EEG was band pass fil-tered (0.3–40 Hz with slope 6–24 db/oct, forward—phase). For eachtrial in each condition, epochs of interest were time-locked on theimperative stimulus (−2500/+2500 ms) with a baseline from −2500to −1500 ms. Epochs containing artifacts were rejected (amplitude120 �V, gradient 75 �V/sample). After transformation to averagereference, we performed a time-frequency (TF) analysis of single-trial EEG data using complex demodulation method. The TF analysiswas set to a frequency resolution of 1 Hz and temporal resolutionof 50 ms in the frequency range 5–30 Hz. The mean power of the–2500 to –1500 ms interval preceding the imperative stimulus wasconsidered as baseline, providing single-trial measure of relativepower at each frequency. Using such a TF computation on each sin-gle trial and averaging the energy across single trials preserves bothevoked and induced activities [27]. The ERD/ERS measures wereobtained in a second step by simply averaging the energy acrossfrequency bins of interest (i.e. beta band within 14 and 30 Hz),and contain both evoked and induced information. This approachavoids any a priori hypothesis on the nature of the beta response,which is likely to be a mixture of phase-locked and non phase-locked activities. For more details about the BESA power spectrumanalysis, see a previous publication [28].

Only correct trials were considered (mean ± SD: 58 ± 4 in SWIT

and 61 ± 5 in CONT condition). On average, the number of epochsincluded for analysis was 55 ± 5 (rejection: 6.6%) in the SWIT condi-tion and 56 ± 6 (rejection: 8.1%) in the CONT condition. There was

e whole trial. Each trial engaged bimanual (BM) tapping at the start stimulus (white to the condition). The SWIT and the CONT had to be executed after the imperativene in purple for each condition (from 0 to 2500 ms after imperative stimulus onset).

the web version of this article.)

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o difference in the percentage of rejection between conditionst(16) = 1.01, p > 0.3). Participants were included when a minimumf 44 trials were accepted by condition, leading to the exclusion of

participants. Two more participants were excluded due to abun-ant EEG artifacts. Seventeen out the 21 recorded participants werehus eventually included in the study.

.5. Statistical analyses

.5.1. BehaviorInter-tap interval (ITI) between each button press of the right

ndex was measured. ITI was considered as correct (1) if the instruc-ion (SWIT/CONT) was respected and (2) if the delay between theeft and right button presses did not exceed 50 ms during theimanual tapping. The non-respect of (1) and/or (2) from 0 to00 ms after imperative stimulus onset have been recognized asrror. Mean, SD and percentage of errors of the ITI from 0 to 500 msfter stimulus imperative onset in SWIT and CONT conditions wereompared using paired t-test.

.5.2. Time-frequencyA paired sampled t-test was performed to compare the time-

requency signals between SWIT and CONT conditions with BESAtatistics 1.0. Statistics were performed in beta range 14–30 Hz on

2500 ms time window time-locked to imperative stimulus onset.ermutation test was fixed at 1000 for a p-value <0.05. Permu-ation test systematically interchanges the data of subjects andvoids significant effect found by chance. The result of the compar-son between SWIT and CONT condition was interpreted in termsf synchronization (PMBS) phenomenon. Thus, PMBS reflects theifference between SWIT and CONT. Using the CONT condition as

control task seems well appropriated to evaluate efficiently theMBS since it eliminates a large amount of effects attributed to per-eptual and attentional processes due to the subtraction betweenonditions.

.5.3. Electrical source estimationsElectrical source estimations were computed with Cartool

https://sites.google.com/site/fbmlab/cartool; [29]]. We estimatedlectric sources underlying scalp-recorded data using a distributedinear inverse solution based on a local autoregressive averageLAURA) regularization approach [30–32]. LAURA selects the sourceonfiguration that better mimics the biophysical behavior of elec-ric fields (i.e. activity at one point depends on the activity ateighboring points according to electromagnetic laws). The solu-ion space is based on a realistic head model and included 3005olution points homogeneously distributed within the gray matterf the average brain of the Montreal Neurological Institute (cour-esy of R. Grave de Peralta Menendez and S. Gonzalez Andino,niversity Hospital of Geneva, Geneva, Switzerland). Intracranial

ources were estimated for each participant across the whole epochn a beta frequency-band (14–30 Hz) averaged and then statisticallyompared using paired-sample t-tests at each time-frame and eachode between the SWIT and CONT conditions.

Correction was made for temporal autocorrelation through thepplication of a >1 contiguous data point temporal criterion (50 ms)or the persistence of significant differential effects [33]. The resultsf this analysis of source estimations are presented as plot depictinghe percentage of solution nodes showing a significant (p < 0.01)ifference as a function of peri-stimulus time [34,35].

.5.4. Behavioral-brain correlations

The brain activity at each time-frame (from 0 to 2500 ms after

mperative stimulus onset) in SWIT was correlated with the per-entage of errors in SWIT using Pearson correlation tests. First,olution points significantly different in the paired t-test between

esearch 271 (2014) 365–373

SWIT and CONT conditions (p < 0.01) were used to select the brainactivity (�V/mm3) at each time-frame for each subject. Second, cor-relations between the brain activities at each time frame in SWITwere correlated with the percentage of errors in SWIT. Finally, allthe correlations with a p-value <0.05 were exported in a 3005 solu-tion points head model.

2.5.5. Global considerations about statistical analysesThe normality of all data was assessed with the

Kolmogorov–Smirnov test, ensuring that all variables werenormal (all p-values >0.05) except the percentage of error in theCONT condition (p-value <0.05). Hence, values of the percentageof error in CONT and SWIT condition were normalized using log10data transformation.

In view of the large number and complexity of results obtainedin this task, the analysis of the preparatory period will be addressedin another report.

3. Results

3.1. Behavioral data

Mean, SD (516 ± 27 ms and 513 ± 25 ms in SWIT and CONT,respectively) and percentage of errors (9% and 8% in SWIT andCONT, respectively) of the ITI were not different between SWIT andCONT condition (all p-values >0.1).

3.2. EEG data

3.2.1. Time-frequency analysesA PMBS is observed in a broad beta frequency-band (14–30 Hz)

in medial fronto-central (Fz, FCz and Cz), right fronto-central (F2,F4, FC2, FC4, C2, C4 and C6) and right centro-parietal (CP2, CP4,CP6, P4 and P6) regions during the whole post-switching period(from 500 ms to 2500 ms after imperative stimulus onset; dura-tion: 2000 ms). The maximal magnitude of the broad-band PMBS(14–30 Hz) is observed in electrode C4 (Fig. 2). Another PMBSappeared in a restricted beta frequency-band (22–26 Hz) in leftfronto-central (F1, FC1 and FC3; from 500 ms to 1500 ms afterimperative stimulus onset; duration: ∼1000 ms), left central (C1and C3; duration: ∼1500 ms) and left medio-parietal (CPz andCP1; duration: ∼1500 ms) regions. The maximal magnitude ofthe restricted-band PMBS (22–26 Hz) was observed in electrodeC1 (Fig. 2). The variability inter-subject was larger in SWIT thanCONT for the electrodes C4 (t(51) = 12.5, p < 0.05; 14–30 Hz) and C1(t(51) = 6.6, p < 0.05; 22–26 Hz).

3.2.2. Electrical source estimationDuring the PMBS (14–30 Hz), the time frame-wise analysis of the

source estimation revealed periods of widespread significant dif-ferences between the SWIT vs. CONT conditions peaking at 750 msand 1300 ms. The significant solution points are represented on atemplate brain at the time-frames when the number of solutionpoints showing a significant difference was maximal (Fig. 3).

The first peak of the PMBS (14–30 Hz) showed significant(p < 0.01) difference at 750 ms after imperative stimulus onsetwithin bilateral frontal (pre-central, middle, superior and medialfrontal gyri), right frontal (inferior frontal gyrus), right temporal(superior and middle temporal gyri), bilateral parietal (post-centralgyrus, inferior and superior parietal lobules) and right parietal (pre-cuneus) cortices. Solution points with maximal difference (SP MAX)were located within right pre-frontal cortex (superior frontal gyrus;

Fig. 3). The second peak showed significant (p < 0.01) difference at1300 ms after imperative stimulus onset within bilateral frontal(pre-central, middle and superior frontal gyri), right temporal (mid-dle and superior temporal gyri), bilateral parietal (post-central

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Fig. 2. Time-frequency results. Topography (at the center) representing the clusters significantly different (p < 0.05) between SWIT and CONT conditions in each electrode(n = 64) throughout the time (x-axis: from 0 to 2500 ms after imperative stimulus onset) and the frequency-band (y-axis: from 14 to 30 Hz). Electrodes with a broad significantfrequency range (i.e. 14–30 Hz) are noted in cyan while electrodes with restricted significant frequency range (i.e. 22–26 Hz) are noted in purple. The electrodes with maximaldifference (left and right panels) in the broad (14–30 Hz; C4) and restricted (22–26 Hz; C1) beta range are displays for the SWIT and the CONT condition. Oscillations ofelectrodes with maximal difference in the broad (14–30 Hz; C4) and restricted (22–26 Hz; C1) beta range are represented in the bottom panels. The representation depictedthe oscillations of the SWIT (in green) and the CONT (in red) conditions throughout microvolt (left y-axis) and time (x-axis: from 0 to 2500 ms after imperative stimulusonset). Gray background represent the difference between the SWIT and the CONT conditions obtained with paired t-test (right y-axis: 1—p-value) at each time point in theaveraged beta frequency-range (14–30 Hz and 22–26 Hz). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of thisa

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yrus, superior parietal lobule and precuneus), right parietal (infe-ior parietal lobule) and right occipital (cuneus) cortices. Solutionoints with maximal difference (SP MAX) were located within rightarietal cortex (inferior parietal lobule; Fig. 3).

.2.3. CorrelationThe solution points significantly correlated (Pearson p-value

0.05) with behavioral performance are represented on a templaterain at the time-frames when the number of solution points show-

ng a significant difference was maximal (Fig. 4).The percentage of errors in SWIT and the solution nodes signifi-

antly different in SWIT during the PMBS (14–30 Hz) was negativelyorrelated (p < 0.05) at 450 ms, 800 ms and 1300 ms after impera-ive stimulus onset. At 450 ms, brain activity was located withinight parietal (inferior parietal lobule and post-central gyrus) andight frontal (pre-central gyrus) cortices with a maximal correla-ion within the right parietal cortex (SP MAX: post-central gyrus;

= −0.67, p < 0.01, Fig. 4). At 800 ms, brain activity was located

ithin right pre-frontal (superior and middle frontal gyri), rightarietal (post-central gyrus and superior parietal lobules) and rightccipital (middle occipital gyrus) cortices with a maximal differ-nce within right pre-frontal cortex (SP MAX: middle frontal gyrus;

r = −0.69, p < 0.01, Fig. 4). At 1300 ms, brain activity was locatedwithin right pre-frontal (middle frontal gyrus), right parietal (post-central gyrus, inferior and superior parietal lobules and precuneus)and right temporal (superior temporal gyrus) cortices with max-imal difference within right pre-frontal cortex (SP MAX: middlefrontal gyrus; r = −0.63, p < 0.01, Fig. 4).

4. Discussion

Using a switching motor task, our results distinguish for thefirst time the temporal dynamics and spatial localization of PMBSassociated with (i) sensory reafferences and (ii) active inhibitionprocesses. Behavioral variables (mean, variability and percent-age of errors) showed no difference between the switch andcontinue conditions. This suggested that in a context of audi-tory paced tapping (2 Hz), selective stopping of a movement isas easy as continued bimanual tapping movements when theparticipants know beforehand the stopping hand. These results

showed that both conditions were performed in the same way andallowed to match precisely the movements between conditionsfor a better comparison at an electrical level. Electrophysiolog-ically, we observed large PMBS in SWIT compared to CONT in

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Fig. 3. Time-wise t-tests on the source estimations. The total number of solution nodes showing a significant (p < 0.01) difference at each time-frame is plotted (right panel).The dashed lines indicate the two time-frames with the maximal number of solution points showing a significant difference in the beta frequency (750 ms and 1300 ms afterimperative stimulus onset in 14–30 Hz). The results of the t-tests (significant t-values) are projected on a template brain for these time-frames (left panels). The negativet-values (purple color) indicate the regions more activated in the CONT than in the SWIT condition; the red values indicate the regions more activated in the SWIT than CONTc maxi( in th

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ondition. Two supplementary template brains showed the solution point with thered color) accompanied each SP MAX. (For interpretation of the references to color

broad-band (14–30 Hz) in right fronto-centro-parietal regionsith maximal difference within right central region (sensorimotor

egions) during the whole post-switching period. A concomitantMBS appeared in a more restricted-band (22–26 Hz), limitedo left fronto-centro-parietal regions with maximal differenceithin left central region (sensorimotor regions) during mostart of the post-switching period. Electrical source analyses local-

zed the broad-band PMBS (14–30 Hz) within bilateral frontalnd parietal and right temporal cortices at 750 ms and withinilateral frontal and parietal, right temporal and right occipi-al cortices at 1300 ms. Solution points with maximal differenceere located within right pre-frontal cortex (superior frontal

yrus) at 750 ms and within right parietal cortex (inferior pari-tal lobule) at 1300 ms. Finally, we evidenced negative correlationsetween the percentage of errors in SWIT and the magnitude ofhe PMBS (14–30 Hz) in SWIT within right parietal and frontal cor-ices.

To note that the PMBS modulations might be affected by cog-itive processes. Indeed, the behavioral response is determinedy bottom up factors (i.e. preparatory and imperative stimuli)hat might induce an elevation of beta band activity (i.e. ampli-ude increase [36]). We suppose, however, that cognitive processeselated to beta ERS modulations are light because the large part of

he cognitive processing takes place during the preparatory period.n addition, the fact that the SWIT and CONT conditions were com-ared should cancel the residual cognitive processes evoked by the

mperative stimulus.

mal difference (SP MAX). Oscillations across time in SWIT (green color) and CONTis figure legend, the reader is referred to the web version of this article.)

4.1. Active inhibition processes.

At the sensor level, we observed a broad-band 14–30 Hz PMBSduring the whole post-switching period (from 500 ms to 2500 ms:duration 2000 ms) within the right hemisphere with a dominancein the right motor region. We suggest that the broad-band and thecontinuous duration of the ipsilateral PMBS is related to active inhi-bition processes (top–down control) involved in the stopping of theleft index movement during the whole post-switching tapping. Ourresults corroborate previous studies supporting that PMBS relatesto an active inhibition involved discrete hand-foot movement [11]and motor imagery of right–left hand movement [19]. Because TMSstudies evidenced active inhibition after repetitive thumb [23] orindex movements [24] auditory-paced (1 Hz) in the brain area notinvolved in the movement, we suggest that, after the switching,the active inhibition set up in the regions representation of theirrelevant movement (i.e. left index selectively stopped) allowing toprevent any unwanted movement of this index previously involvedin the task. We provide here additional information about the PMBSduration. Indeed, it was evidenced that PMBS triggering was relatedto the end of the whole motor process, and not to the end of eachmotor program [18]. Our results allow to precise that PMBS trigger-ing is related to the end of a partial part of the motor process (i.e.

when a part of the movement is selectively stopped while otherpart of the movement continue the action).

Source estimation analyses further support the assumptionof active inhibition within the right hemisphere. Brain activity

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Fig. 4. Pearson correlation between the percentage of errors in SWIT and the brain activity in SWIT at each time-frame (from 0 to 2500 ms after imperative stimulus onset).Solution points with a Pearson correlation p < 0.05 were represented on a 3005 solution points head model (upper left panel). The dashed lines indicate the three time-frames(450 ms, 800 ms and 1300 ms after imperative stimulus onset) with the maximal number of solution points showing a significant difference. The results of the Pearsoncorrelation (significant r-values) are projected on a template brain for these time-frames (right panels). The negative r-values (purple color) indicate a negative correlation;the red values indicate a positive correlation. The template brains displayed for the three time periods are entitled by the brain region with the maximal difference (SP MAX).G solutif re leg

diavmtaTiBcacmrti

pblfttb

raphical representation (bottom panel) displays the average of brain activity of all

or each subject (i.e. n = 17). (For interpretation of the references to color in this figu

ifference indeed stemmed within regions involved in selectivenhibition, including the right pre-frontal (superior frontal gyrus)nd the right parietal (inferior parietal lobule) cortices [37,38]. Con-erging evidences support that inhibition processes of a selectiveovement involves a wide network including the pre-frontal cor-

ex (inferior and superior frontal gyri), the supplementary motorrea (SMA), the pre-SMA and the inferior parietal cortex [39–41].hese regions were shown responsible of selective inhibition dur-ng reactive paradigm such as stop signal or Go/No-go tasks.ecause the selective stopping in reactive paradigm requires a dis-rete response, the inhibitory processes should be activated during

short period. In our study, where the subject prepared (proactiveontrol) a selective stopping of the left index while maintainingovements with the right index, we show that the same cortical

egions are actively inhibited that in the reactive paradigm and thathis network stays inhibited during the whole stopping of the leftndex movement.

Hypothesis of active inhibition during the post-switchingeriod was strengthened by the negative correlation betweenehavioral and neurophysiological data. Maximal correlation was

ocated within right parietal (post-central gyrus) and right pre-

rontal (middle frontal gyrus) cortices. This result indicates thathe larger the PMBS, the lower the level of error rate, suggestinghat the magnitude of the PMBS is related to the selective inhi-ition efficiency. Relationship between beta synchronization and

on points (�V2/mm3) significantly correlated with the percentage of errors in SWITend, the reader is referred to the web version of this article.)

behavioral performance has been recently reported during avisuomotor task [42]. These authors showed a negative correlationbetween the amplitude of the PMBS and the size of the precedingangular error. We suggest here that the PMBS could be an electro-cortical marker of the efficiency of active inhibition processesduring selective hand movement.

Taken together, these observations point out the involvementof the active inhibition processes within right pre-frontal and rightparietal network during selective inhibition and raise the possibil-ity that this is mediated, at least in part, by the dynamic modulationof the degree of beta synchronization.

4.2. Sensory reafferences processes

Time-frequency analysis at the sensor level revealed a contralat-eral (left) PMBS concomitant to the ipsilateral (right) PMBS. Thiscontralateral PMBS appeared in a more restricted beta frequency-band (22–26 Hz) with a dominance in the left sensorimotor regionsduring a shorter time period (from 500 ms to 2000 ms after imper-ative stimulus onset; duration: 1500 ms). The link between PMBSand motor inhibitory processes cannot be evoked here since the

right index is engaged in both conditions. Instead of the inhibitoryhypothesis, the contralateral PMBS could emerge to the largeipsilateral PMBS (i.e. overflow) due to massive transcallosal con-nections of both hemispheres. It is of interest, however, that the

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72 E. Sallard et al. / Behavioural B

agnitude of the contralateral PMBS is less large and that itsuration is shorter than in the ipsilateral hemisphere. This resultorroborates with previous evidences showing that PMBS inducedy the movement had a greater magnitude and lasted longer thanMBS related to cutaneous stimulation [8,13,43]. Another hypothe-is concerned the involvement of sensory reafference processes (i.e.ottom–up control) related to the right index tapping movement.upporting this hypothesis, previous studies showed a PMBS withinensorimotor regions after nerve stimulation on thumb and fin-er movement [13,17]. In our task, once the switching to unilateralight tapping was performed, we assume that sensory reafferencesoming from the right index finger are sent to the sensorimotoregions. We suggest that the duration of the left PMBS could beelied to the need to stabilize the regularity of the tapping with theetronome beat in the post-switching phase. These results could

onfirm our hypothesis about the existence of reafferences pro-esses in the contralateral hemisphere in relation to continuingapping of the right hand.

The contralateral PMBS found in a restricted band (22–26 Hz) athe sensor level was localized within the left parietal cortex (supe-ior and inferior parietal lobules) at the brain space level. This brainctivation was reduced in magnitude and time duration comparedo the ipsilateral brain activity. This result is in accordance with theypothesis of sensory reafferences processes involved in continu-us hand tapping since the parietal lobe is known to play a majorole in the integration of sensorimotor information in motor skilluring grip force task [44] or bimanual coordination task [45]. Morerecisely, the inferior and superior parietal lobules were shown toe activated when subjects covertly prepare movements or switch

ntended movements [see also [46]]. Finally, we suggested that sen-ory reafferences constitute an important source of informationn our switching paradigm in order to produce efficient regularapping movements.

. Conclusion

This study shows for the first time simultaneous PMBS withinistinct brain regions, latencies and frequency ranges during aotor switching task. We suggest that the PMBS correspond to

oncomitant active inhibition and sensory reafferences processes.he PMBS within left parietal cortex might reflect the sensory reaf-erences (bottom–up control) of the right hand tapping disruptedy the switching in order to maintain a regular rhythm. The PMBSithin right frontal and right parietal cortices might reflect the con-

inued active inhibition (top–down control) of the recently stoppedeft hand in order to prevent interference with the right handapping. Furthermore, we evidenced a marker of active inhibitionhrough the magnitude of the PMBS. Overall, we conclude that aimanual switching task is a suitable paradigm to reveal distinctunctional aspects of post-movement beta synchronization.

cknowledgements

Cartool software has been programmed by Denis Brunet, fromhe Functional Brain Mapping Laboratory, Geneva, Switzerland, andupported by the Center for Biomedical Imaging (CIBM) of Genevand Lausanne. We thank Fabio Borrani for his help in treatment ofata.

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