Stability-dependent behavioural and electro-cortical reorganizations during intentional switching between bimanual tapping modes

Neuroscience Letters 483 (2010) 118–122

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Stability-dependent behavioural and electro-cortical reorganizations during intentional switching between bimanual tapping modes Jessica Tallet a,∗ , Jérôme Barral b , Clara James c,d , Claude-Alain Hauert c,d a

Université de Toulouse, UPS, LAPMA, Toulouse, France Institut des Sciences du Sport de l’Université de Lausanne, Switzerland Faculté de Psychologie et des Sciences de l’Education, Université de Genève, Switzerland d Geneva Neuroscience Center, University of Geneva, Switzerland b c

a r t i c l e

i n f o

Article history: Received 30 June 2010 Received in revised form 21 July 2010 Accepted 26 July 2010 Keywords: Motor intention Inhibition Coordination Electroencephalography Functional coupling

a b s t r a c t This study investigated behavioural and electro-cortical reorganizations accompanying intentional switching between two distinct bimanual coordination tapping modes (In-phase and Anti-phase) that differ in stability when produced at the same movement rate. We expected that switching to a less stable tapping mode (In-to-Anti switching) would lead to larger behavioural perturbations and require supplementary neural resources than switching to a more stable tapping mode (Anti-to-In switching). Behavioural results confirmed that the In-to-Anti switching lasted longer than the Anti-to-In switching. A general increase in attention-related neural activity was found at the moment of switching for both conditions. Additionally, two condition-dependent EEG reorganizations were observed. First, a specific increase in cortico-cortical coherence appeared exclusively during the In-to-Anti switching. This result may reflect a strengthening in inter-regional communication in order to engage in the subsequent, less stable, tapping mode. Second, a decrease in motor-related neural activity (increased beta spectral power) was found for the Anti-to-In switching only. The latter effect may reflect the interruption of the previous, less stable, tapping mode. Given that previous results on spontaneous Anti-to-In switching revealing an inverse pattern of EEG reorganization (decreased beta spectral power), present findings give new insight on the stability-dependent neural correlates of intentional motor switching. © 2010 Elsevier Ireland Ltd. All rights reserved.

Behavioural flexibility depends in part on the capacity to rapidly change the ongoing behaviour in order to meet new environmental constraints. This capacity may require switching between two behaviours that is interrupting or reorganizing the ongoing behaviour in order to engage in a subsequent one. Rhythmical coordination with index fingers tapping in synchronization with a metronome is an appropriate paradigm to investigate motor switching because it is well established that switching between two tapping modes depends on their stability [17,18,33,34]. Bimanual finger tapping modes are characterized by their relative phase (RP), which is the relative timing between the fingers’ movements [17]. At an identical moderate movement rate, both In-phase (synchronous) and Anti-phase (alternate) tapping modes are produced stably, but the RP of In-phase is characterized by a higher stability than the RP of Anti-phase [e.g., 8]. When the movement rate increases beyond a critical point, the RP of the less stable Antiphase tapping mode destabilizes, leading to spontaneous switching to the more stable In-phase tapping mode (Anti-to-In switch-

∗ Corresponding author. Tel.: +33 0 561556465; fax: +33 0 561558280. E-mail address: [email protected] (J. Tallet). 0304-3940/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2010.07.074

ing) [17,18,34]. The inverse switching, from more to less stable tapping mode (In-to-Anti switching), does never occur spontaneously, suggesting that switching is stability-dependent. Several neuroimaging studies (fMRI, EEG/MEG) demonstrated that the spontaneous Anti-to-In switching induces cerebral reorganizations in the premotor cortex, the Supplementary Motor Area (SMA) and the cerebellum ([14,20,21,22]; for reviews [4,15,24]). However, much less is known regarding the cerebral changes accompanying the intentional switching between two required tapping modes differing in stability. Intentional switching driven by environmental constraints requires inhibition of a stable coordination, in combination with the stabilization of a more or less stable subsequent coordination mode. At a behavioural level, the intentional In-to-Anti switching takes more time than the Anti-to-In switching [18,33]. At a neural level, studies using fMRI revealed a stability-dependent increased activation of the basal ganglia during intentional switching [9,15]. Here, we investigated the fundamentally different question: how cortical regions communicate to ensure intentional switching between tapping modes of different stability, when produced an identical movement rate?. EEG is the most appropriate technique to investigate this issue because it captures the synchronized oscillations within

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and between brain regions, which are assumed to represent a basic form of communication between cortical assemblies [6,35]. Task-Related spectral Power (TRPow) measures the level of (de)synchronization within local cortical neuronal populations and captures the level of neural activity or excitability [3,11,12,25,36]. A decrease in TRPow reflects local desynchronization of cortical activity exhibiting an increase in neural activity whereas an increase in TRPow reflects synchronization exhibiting a decrease in neural activity [11,25]. Task-Related Coherence (TRCoh) measures the strength of inter-regional (de)coupling and reflects the dynamic functional communication between distributed cortical regions [3,11,12,35,36]. Task-Related changes in the alpha frequency band (8–12 Hz) are predominantly associated with attentional processes whereas changes in the beta band (13–30 Hz) reflect motor processes [13,26,32]. Using TRPow and TRCoh analyses in alpha and beta bands, we recently investigated the correlates of intentional In-to-Anti switching [40]. Behavioural results revealed an increased inter-trial temporal variability accompanying the initiation of the Anti-phase tapping. Meanwhile, EEG results showed a decrease of TRPow in the alpha band over the left sensorimotor and the mesio-parietal areas in combination with an increase of TRCoh in the beta band between inter- and intra-hemispheric cortical regions. These EEG results suggest that interrupting a more stable tapping mode in order to engage in a less stable one (In-to-Anti switching) induces an increase in cortical activity related to attentional resources and an increase in inter-regional communication related to motor information. The inverse (Anti-to-In) switching has not been investigated. Given that the Anti-to-In switching requires interrupting a less stable tapping mode in order to engage in a more stable one, we expect the inverse pattern of behavioural and EEG results, namely (a) less increase in tempo variability at the moment of the transition, (b) an increase of TRPow in the alpha band and (c) a decrease in the inter-regional TRCoh (i.e., a decoupling) in the beta band. To test these hypotheses, seven right-handed and non-musician volunteers (2 women) participated in the study (mean age: 26 ± 4 years). The procedure was approved by the local ethics committee and the experiment was conducted in agreement with the University guidelines and the ethical standards of the declaration of Helsinki. The experiment was conducted in a sound-treated and dimly lit shielded room. Visual instructions and auditory tones of a metronome were delivered by a computer with Presentation software (Neurobehavioral System, Albany, CA). The same computer recorded movements of the index fingers that consisted in pressing two red-colored “Ctrl” keys on a keyboard. EEG was continuously recorded at 64 electrode sites (BioSemi Active-Two, V.O.F., Amsterdam, the Netherlands), equally distributed over the scalp, at a sampling rate of 2048 Hz. Prior to analysis, data were offline recomputed against average reference. The participants were asked to produce iso-frequency bimanual fingers tapping movements in synchronisation with the auditory metronome at a moderate fixed tempo (700 ms) and intensity (80 dB). In-phase tapping required to synchronize both fingers on the beat while Anti-phase tapping required to synchronize the right index on the beat and to alternate (syncopate) the left index of the beat. In consequence, the required tempo (period of the right index) remained the same for In-phase and Anti-phase tapping modes. Each trial lasted 20 s. First, the metronome produced low-pitched tones (500 Hz) and the participant started the trial either with the In-phase tapping or with the Anti-phase tapping. After varying delays (9, 11 or 13 low-pitched tones), the metronome changed to high-pitched tones (4000 Hz), prompting the participant to switch to the other bimanual tapping mode. The experiment comprised two experimental conditions: the In-to-Anti condition and the Anti-to-In condition. In an additional

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control condition participants listened to the metronome that changed from low-pitched to high-pitched tones without moving. The experiment was preceded by familiarization trials in the two experimental conditions. Each experimental condition and control condition included 24 trials performed in two separate sessions, to avoid fatigue effects. Hence, the experimental design comprised a total of 6 sessions (144 trials) pseudo-randomized across participants. We processed the behavioural data as follows. Mean period right index finger tapping (Tright (mean)) and corresponding standard deviations (Tright (sd)) were computed for each participant and each tapping mode (In-phase and Anti-phase). Tright (mean) reflects the Tempo adopted by the right index finger and Tright (sd) its variability, expressed in milliseconds. Additionally the relative phase (RP) of the tapping was calculated. RP was a measure of the Inter-Tapping temporal delay between the tapping of the right and left index (ITright-left), divided by the period of the corresponding right-leading hand tapping (Tright), multiplied by 360◦ (RP = (ITright-left/Tright) × 360). RP is expressed in degrees and gives theoretically 0◦ for In-phase and 180◦ for Anti-phase. The mean of the produced RP (RPmean) informs on the accuracy of the produced tapping mode and SD of RP (RPsd) on its stability [17]. Theoretically, RP = 0◦ with Tright = 700 ms and ITright-left = 0 ms for In-phase tapping and RP = 180◦ with Tright = 700 ms and ITrightleft = 350 ms for Anti-phase tapping. The moment of switching (S) was identified by a change in RP, exceeding 90◦ for the In-to-Anti condition and going below 90◦ for the Anti-to-In condition, after the change of the metronome from low- to high-pitched tone. Behavioural analyses were performed (a) on RPmean and RPsd before and after switching, in order to ensure that participants actually performed the required In-phase and Anti-phase tapping and (b) on Tright (mean) and Tright (sd) during a random selection from the pre-switching tapping (PS) and the moment of switching (S), in order to evaluate the changes at the very moment of the switching. We processed the raw EEG data as follows. Continuous EEG was segmented into two non-overlapping epochs of 1024 ms (512 ms before and after the switching tap), corresponding, respectively to PS and S. Neural activation and functional coupling were quantified from the raw EEG by computing power and coherence by means of a spectral analysis of brain oscillatory activities. Power and Coherence were calculated in the alpha (8–12 Hz) and beta (13–30 Hz) frequency bands for the time epochs of PS and S. EEG power data were transformed using a logarithmic function in order to reduce the effects of inter-participant and inter-electrode variability in absolute power values. Coherences were transformed using an inverse hyperbolic tangent to stabilize variances [31]. Final values for TRPow and TRCoh were obtained by subtracting the control condition from each experimental condition, hence reducing the effects of volume conduction, between-subject differences and between-electrode variability [e.g., 3,12,36,37]. TRPow was calculated for four regions of interest (ROIs) that consisted each of two grouped electrodes over the sensorimotor cortical areas. Left and right latero-central ROIs consisted, respectively, in C3-CP3 and C4CP4, anterior and posterior ROIs in FCz-Cz and CPz-Pz (cf. Fig. 1). The TRCoh was analyzed between three pairs of interest (POIs) located over the left-central (C3-Cz), right-central (C4-Cz) and left-right (C3-C4) sensorimotor regions. With regard to behavioural results, a paired-samples t-test revealed that the RPsd was larger for Anti-phase than for In-phase produced at P1 (t(6) = −9.421; p < 0.0001), confirming that the Antiphase was less stable than the In-phase tapping (RPsd = 4.5 ± 0.5◦ vs RPsd = 12.8 ± 1.3◦ , respectively). Another paired-samples t-test revealed that the Tright (mean) and the Tright (sd) did not differ significantly between the In-phase and the Anti-phase produced at P1 (respectively, t(6) = −2.424; ns and t(6) = 0.587; ns), confirming

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Table 1 Mean tempo of the right index finger (Tright (mean)) and its variability (Tright (sd)) during the pre-switching (PS) and during the switching (S) in the In-to-Anti and Anti-to-In conditions. In-to-Anti

Tright (mean) ± SD (ms) Tright (sd) ± SD (ms)

Anti-to-In

PS

S

PS

S

690 ± 2 8±1

716 ± 9 43 ± 9

695 ± 3 7±2

686 ± 7 38 ± 10

that the movement rate and its variability did not differ for both tapping modes. The Condition (2) × Epoch (2) repeated measures ANOVA performed on RPmean revealed a significant Condition × Epoch interaction (F(1,6) = 11840.59; p < 0.0001). RPmean increased for the In-to-Anti switching condition (from 9 ± 0.5◦ to 178 ± 2◦ ) and decreased for the Anti-to-In switching condition (from 179 ± 1.5◦ to 9 ± 1◦ ). A significant Condition × Epoch interaction on RPsd (F(1,6) = 362.71; p < 0.0001) attested that the RP stability decreased for the In-to-Anti condition (from 4.5 ± 0.5◦ to 11.5 ± 1.2◦ ) and increased for the Anti-to-In condition (from 12.8 ± 1.3◦ to 5.5 ± 1.4◦ ). Finally, the Condition (2) × Epoch (2) repeated measures ANOVA demonstrated a main effect of Epoch on Tright (sd) (F(1,6) = 24.13; p < 0.005), indicating that the tempo variability increased at the moment of switching whatever the condition (cf. Table 1). A main effect of Epoch (F(1,6) = 6.75; p < 0.05) and a significant Condition × Epoch (F(1,6) = 6.05; p < 0.05) interaction on Tright (mean) indicated that the In-to-Anti condition induced a greater tempo deceleration than the Anti-to-In condition. With regard to EEG results, the Condition (2) × ROI (4) or POI (3) repeated measures ANOVA revealed that, whatever the ROI

Fig. 1. Histogram and topographic maps of the grand average of the TRPow (= TRPow at S – TRPow at PS) for the four ROIs (C3-CP3, C4-CP4, FCz-Cz and CPz-Pz) in the beta band (13–30 Hz) according to the In-to-Anti (left panel) and the Anti-to-In (right panel) conditions. In the histogram, positive values mean TRPow increase (synchronization = deactivation) and negative values mean a TRPow decrease (desynchronization = activation) between PS and P. In the topographic maps, the color scale represents the TRPow increase (red) and TRPow decrease (blue). The dots indicate electrode positions. Vertical bars represent the standard error. *** p < 0.001. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)

or POI, In-phase and Anti-phase produced at PS differed neither for alpha and beta TRPow (F(1,6) = 0.324; ns and F(1,6) = 4.079; ns, respectively), nor for beta TRCoh (F(1,6) = 0.129; ns). The Condition (2) × Epoch (2) × ROI (4) repeated measures ANOVA performed on TRPow in the alpha band indicated main effects of ROI (F(1.572,9.434) = 6.16; p < 0.05) and Epoch (F(1,6) = 6.59; p < 0.05). Values of alpha TRPow of C3-CP3 and C4-CP4 were significantly lower than those of FCz-Cz and CPzPz (C3-CP3: −0.242 ± 0.07 ␮V; C4-CP4: −0.248 ± 0.05 ␮V; FCz-Cz: −0.129 ± 0.04 ␮V and CPz-Pz: −0.108 ± 0.03 ␮V) and alpha TRPow decreased from PS to S whatever the ROI and the Condition (from −0.142 ± 0.04 to −0.222 ± 0.05 ␮V). An ANOVA with the same design performed on beta TRPow indicated a significant Condition × Epoch × ROI interaction (F(3,18) = 3.28; p = 0.045). Post hoc analyses (t-tests with Bonferroni–Dunn corrections) revealed that the values of beta TRPow increased from PS to S only in the anterior group of electrodes (FCz-Cz) in the Anti-to-In condition (p < 0.001) (cf. Fig. 1). The Condition (2) × Epoch (2) × POI (3) repeated measures ANOVA performed on beta TRCoh indicated a significant Condition × Epoch interaction (F(1,6) = 10.08; p = 0.019). Whatever the POI, only the In-to-Anti condition was associated with an increase of the beta TRCoh (from 0.01 ± 0.06 at PS to 0.024 ± 0.04 at P (TRCoh = 0.014) for the In-to-Anti condition and from 0.011 ± 0.07 at PS to 0.017 ± 0.05 at P (TRCoh = 0.006) for the Anti-to-In condition). To sum up, the behavioural results support our hypothesis: an increase in the tapping variability occurred at the actual moment of switching whatever the condition, but the Anti-to-In switching induced a larger tempo deceleration associated with the increase in variability. These results corroborate previous findings showing that In-to-Anti switching takes more time than the Anti-to-In switching [33]. The EEG results partially support our hypotheses. Globally, the reorganizations in the alpha band were not specific to the switching tasks, whereas the reorganizations in the beta band differed for the In-to-Anti and the Anti-to-In switching. Concerning the alpha band, both switching conditions induced a general increase in neural desynchronization (TRPow decrease) over all the regions of interest. Contrary to our hypothesis, the Anti-to-In switching did not demand less attentional resources than the In-to-Anti switching. The non-specific alpha desynchronization can be attributed to enhanced attentional resources necessary to switch from an ongoing tapping mode to another one, whatever its stability. This interpretation is in accordance with Chen et al. [7], who proposed that an Event- or Task-Related Desynchronization in the alpha band over sensorimotor and parietal areas reflects a general state of large-scale neural activation and may designate switching to more ‘active’ information processing required to change the motor state. Concerning the beta band, two specific EEG reorganizations depended on the stability of the required tapping modes. First, only the In-to-Anti switching induced an increase in the inter-regional couplings in the beta band over sensorimotor regions. This result supports the previous findings of Tallet et al. [40] who attributed this effect to a strengthening in inter-regional communication accompanying the engagement in a more complex Anti-phase coordination [see also 3,5,12,19,37,42]. The greater complexity of the Anti-phase tapping could refer to the need of syncopating the left index finger’s tapping off the beat of the metronome, which may require mentally subdividing the tempo of the metronome in order to create a more stable tempo to synchronize their left hand with [30]. It follows that the increase in inter-regional couplings would pertain to switching from synchronization to syncopation [7,14,20,21]. However this hypothesis is doubtful given that, when produced at PS, Anti-phase did not require supplementary inter-regional coupling (or neural activity) compared to In-phase,

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although Anti-phase already required syncopation.1 An alternative hypothesis is that the greater complexity of the Anti-phase tapping mode refers to the “effort of coordination” needed to integrate the movements of both limbs in a single coordination mode [35,40,43]. Thus, the increase in inter-regional couplings during the In-to-Anti switching would reflect an increase in sensorimotor information communication to stabilize the less stable tapping mode. On this basis, we can assume the novel finding that the increase in beta TRCoh found in the In-to-Anti switching is stability-dependent and reflects the engagement in a subsequent less stable Anti-phase tapping mode. Second, an increase in beta TRPow occurred in the Anti-to-In condition only (yellow colour in the topographic map of Fig. 1). This novel finding reflects an increased neural synchronization in the beta band over the frontal region (FCz-Cz) that is a decrease in neural activity related to motor processes. To our knowledge, it is the first time that an increase in beta synchronization was found during the intentional switching between two movements. To date, an increased beta Event-Related Synchronization over precentral regions is known to accompany the termination of a voluntary movement or a sequence of two movements [1], probably manifesting the “idling”/“active immobilization” [27,32] or the deactivation/inhibition/resetting/recovery of the motor network controlling the limb movements [23,25,28]. This interpretation is in line with recent findings showing that an increase in beta synchronization reflects intentional motor inhibition [41]. It also supports results showing reduced post-movement beta synchronization in patients with Parkinson disease who exhibit intentional inhibition disorder (motor perseverations and switching difficulties) [e.g., 2,29,39]. Moreover, given that both spontaneous and intentional Anti-to-In switching induce neural reorganizations over (pre)central regions, our results support previous fMRI results by suggesting the crucial role of SMA and premotor cortex in motor switching [14,16,22]. Interestingly, switching-related beta synchronization only occurs during the transition from a less stable to a more stable movement (Anti-to-In condition). This original finding suggests a transient deactivation/inhibition to intentionally interrupt the Anti-phase tapping, despite the fact that In-phase is subsequently required. According to Stancàk [38], the amplitude of the postmovement beta synchronization over the motor cortex depends on the “complexity” of the movement to-be-interrupted. More precisely, our results suggest that the beta synchronization over central regions depends on the stability of the movement tobe-interrupted. In this perspective, we can assume that the beta synchronization found in the Anti-to-In switching is stabilitydependent and evidences a deactivation of motor areas in order to interrupt the less stable Anti-phase tapping. This proposition is in line with results regarding the spontaneous Anti-to-In switching, which induces an opposite pattern of TRPow results, that is a desynchronization in the beta band over central regions associated to the destabilization of the Anti-phase tapping [21,24]. Thus, it seems that the intentional Anti-to-In switching induced beta synchronization increase, allowing interrupting the less stable Anti-phase, whereas the spontaneous Anti-to-In switching induced a beta synchronization decrease, to maintain the stability of the Anti-phase tapping despite increase in movement rate. Even if this assumption needs further investigations, it suggests that the modulation of the beta synchronization over (pre)central regions represents a signature of motor intention to interrupt or maintain a less stable coordination when the environmental constraints call for switching.

1 Previous studies [37,10] also revealed similar EEG correlates in the beta and alpha bands for In-phase and Anti-phase when produced at moderate movement rate (T = 700 ms).

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