Relationship between intracerebral gamma oscillations and slow potentials in the human sensorimotor cortex

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1 European Journal of Neuroscience, Vol. 24, pp , 2006 doi: /j x Relationship between intracerebral gamma oscillations and slow potentials in the human sensorimotor cortex William Szurhaj, 1 Etienne Labyt, 1 Jean-Louis Bourriez, 1 Philippe Kahane, 2 Patrick Chauvel, 3 François Mauguière, 4 and Philippe Derambure 1 1 EA 2683, Service de Neurophysiologie Clinique, CHRU Lille, France 2 Neurophysiopathologie de l Epilepsie, Clinique Neurologique, CHU Grenoble, France 3 Service de Neurophysiologie Clinique, Hôpital de la Timone, Marseille, France 4 Service de Neurologie Fonctionnelle et d Epileptologie, Hôpital Neurologique, Lyon, France Keywords: cortical rhythms, event-related synchronization, intracerebral recording, motor cortex, movement-related cortical potentials Abstract Changes in sensorimotor rhythms (mu, beta and gamma) and movement-related cortical potentials (MRCPs) are both generated principally by the contralateral sensorimotor areas during the execution of self-paced movement. They appear to reflect movement control mechanisms, which remain partially unclear. With the aim of better understanding their sources and significance, we recorded MRCPs and sensorimotor rhythms during and after self-paced movement using intracerebral electrodes in eight epileptic subjects investigated by stereoelectroencephalography. The results showed that: (i) there is a strong spatial relationship between the late components of movement ) the so-called motor potential (MP) and post-movement complex (PMc) and gamma event-related synchronization (ERS) within the Hz band, as the MP PMc always occurred in contacts displaying gamma ERS (the primary sensorimotor areas), whereas mu and beta reactivities were more diffuse; and (ii) MPs and PMc are both generated by the primary motor and somatosensory areas, but with distinct sources. Hence, this could mean that kinesthesic sensory afferences project to neurons other than those firing during the pyramidal tract volley. The PMc and low gamma ERS represent two electrophysiological facets of kinesthesic feedback from the joints and muscles involved in the movement to the sensorimotor cortex. It could be suggested that gamma oscillations within the Hz band could serve to synchronize the activities of the various neuronal populations involved in control of the ongoing movement. Introduction Two types of cortical activity react to self-paced movement: movement-related cortical potentials (MRCPs) and changes in sensorimotor cortical rhythms (mu, beta and gamma rhythms). MRCPs consist of four main components: (i) BereitschaftPotential (BP) (Kornhuber & Deecke, 1965); (ii) negative slope (NS ) (Shibasaki et al., 1980); (iii) motor potential (MP) (Deecke et al., 1969); (iv) post-movement positive complex (PMc), also called the reafferent potential (RAP) (Kornhuber & Deecke, 1965; Shibasaki et al., 1980). In terms of rhythmic activity, movement is preceded by an event-related desynchronization (ERD) of mu and beta rhythms over the contralateral central region (Pfurtscheller & Berghold, 1989; Derambure et al., 1993). Mu ERD is followed by a slow return to the baseline, whereas beta rhythms synchronize rapidly. Reactivity within the gamma band (> 30 Hz) has also been detected (Pfurtscheller & Neuper, 1992). Intracerebral studies (Neshige et al., 1988a,b; Ikeda & Shibasaki, 1992; Ikeda et al., 1992; Rektor et al., 1994; Toro et al., 1994; Crone et al., 1998; Ohara et al., 2000; Matsumoto et al., 2003; Szurhaj et al., 2003, 2005; Kunieda et al., 2004) have confirmed that MRCPs and cortical rhythm reactivity are related to activity of the supplementary motor area (SMA), the premotor cortex and the primary sensorimotor Correspondence: Dr W. Szurhaj, as above. w-szurhaj@chru-lille.fr Received 5 January 2006, revised 1 April 2006, accepted 5 April 2006 cortex. A few studies have recorded MRCPs and ERD synchronisation (S) simultaneously (Defebvre et al., 1994; Toro et al., 1994; Babiloni et al., 1999; Guieu et al., 1999; Stancak et al., 2000; Leocani et al., 2001; Paradiso et al., 2004). However, these works failed to establish strong relationships between the two phenomena. Hence, these studies concluded that MRCPs and ERD S may represent different aspects of sensorimotor cortex activation. Nevertheless, most of the work concerned the early MRCP components (BP and NS ), and used scalp recordings. Only one study compared MRCPs and ERD S in intracerebral recordings using subdural electrodes (Toro et al., 1994). However, in this latter case, the authors did not explore rhythms above 30 Hz. Recently, several studies have suggested that gamma rhythms may be related to the efferent drive to the muscles (Salenius et al., 1996) and to somatosensory integration (Aoki et al., 1999; Ihara et al., 2003) during and after movement (Szurhaj et al., 2005). It is generally accepted that MP and late MRCP components (the so-called RAP), respectively, reflect motor cortex firing and kinesthesic sensory input from the peripheral nervous system (Deecke et al., 1976; Tarkka & Hallett, 1991). If these hypotheses are correct, then there should be a close temporo-spatial correlation between MP, PMc and gamma ERS. With the aim of exploring the temporo-spatial relationships between these components and sensorimotor rhythm changes (especially gamma ERS), we directly recorded cortical, electrical activity before, during and after movement using intracerebral electrodes in eight

2 948 W. Szurhaj et al. epileptic subjects investigated by stereoelectroencephalography (SEEG). Materials and methods Subjects Eight epileptic subjects (five males, three females; age range years) were recorded. They were explored using SEEG in order to localize the epileptic focus and to perform functional mapping prior to surgical treatment. Intracerebral electrodes were implanted orthogonally, according to Talairach s methodology (Talairach & Bancaud., 1973). Each electrode had 10 or 15 2-mm contacts with a 1.5-mm intercontact spacing. The eight subjects were selected because their electrodes were located in all the sensorimotor areas: the precentral and postcentral gyri, the frontal lateral cortex and the frontal medial cortex. Only recordings obtained from contacts located in healthy, cortical regions were analysed in the present study. SEEG confirmed that the epileptogenic focus did not coincide with the selected sensorimotor areas. Positions of selected contacts of all subjects are reported in Fig. 1. Neurological examination results were normal for all subjects. The subjects were fully informed of the aims of the study and had given their informed consent. The study has been approved by the local ethical committee of Lyon. Methods Data collection SEEG activity was recorded from 62 or 96 deep electrode contacts, with a sampling rate of 512 Hz and an analogue filter bandpass of Hz. As reference electrode, we always selected a relatively inactive contact that was in the white matter and outside the sensorimotor pathways. The subjects were half-sitting in their beds, in a quiet room and with their forearms resting on a table. Subjects were instructed to remain motionless, to stare at a fixed point and to perform a self-paced movement contralateral to the investigated sensorimotor areas. All the subjects performed a brief extension of the index finger, except for subject n 6 who performed an extension of the wrist. Movements had to be brisk, and were separated from one other by an interval of up to 10 s. In order to detect movement onset and offset, electromyogram (EMG) was recorded using two surface electrodes placed over the belly of the extensor indicis proprius for the index finger movement and the extensor carpi radialis for the wrist movement. Recordings were performed under video surveillance in Fig. 1. Positions of all electrodes in the eight subjects are reported on a sagittal section of the Talairach and Tournoux atlas (AC PC +41 mm). order to exclude epochs with erratic movements. Subjects performed at least 50 movements. Selection of recording sites Depending on each subject s set of intracerebral electrodes, we selected contacts located in sensorimotor areas. It was impossible to perform magnetic resonance imagery (MRI) with stainless steel electrodes in place. The stereotactic coordinates of electrode positions were those preoperatively calculated on MRI for each target using scale 1 skull radiography data superimposed on scale 1 angiography results. A post-implantation, frontal X-ray was performed to check the final position of each electrode. The contacts of each electrode were then plotted onto the appropriate frontal MRI slices of each patient, and we were able to localize each contact on the MRI by calculating three coordinates: for the lateral medial axis, x ¼ the distance between the contact and the median sagittal plane; for the rostro-caudal axis, y ¼ the distance between the contact and the vertical anterior commissure frontal plane; and for the vertical axis, z ¼ the distance between the contact and the horizontal anterior commissure posterior commissure (AC PC) plane. In order to pool the data across subjects, these coordinates were used to localize each contact site in the Talairach and Tournoux atlas (Talairach & Tournoux, 1988). In some subjects (n 3, 4 and 6), the location of the recording electrodes was confirmed by MRI performed after their removal. To localize precisely the central sulcus and in addition to the anatomical method, we used functional data from cortical stimulation studies previously performed for functional mapping of the central cortex. We only analysed contacts for which the anatomical and functional methods were in agreement. Data analysis: MRCP analysis Each of the selected trials was aligned at the onset and offset of the EMG burst. MRCPs were generated by averaging more than 40 4-s periods (from )2 s to +2 s). Due to the time constant used here, we were not able to accurately study the first, slow MRCP components (BP and NS ). We studied only the late MRCP components, which were not altered by the selected high-bypass filtering. For definition of the late MRCP components, we decided to use criteria similar to those employed in scalp studies: we refer to potentials starting before the movement onset and with a clearly defined peak less than 100 ms after movement onset as MP components. We refer to potentials with a clearly defined peak later than 100 ms after movement onset or starting after movement onset as PMc components. Only potentials with a steep slope were considered as MP or PMc. Polarity and potential s location (pre- or postcentral) were not taken into account in its definition. Data analysis: ERD S analysis ERD was computed according to the method proposed by Pfurtscheller (Pfurtscheller & Aranibar, 1977). Electroencephalography (EEG) data were analysed from 4 s before to 4 s after movement onset. Epochs containing spikes or erratic movements of the patient were omitted from the analysis. Only trials containing a well-defined EMG burst onset were analysed. In order to minimize bias from MRCPs, the full set of EEG samples was averaged and the resulting signal was subtracted from each individual EEG sample. Each 8-s, artefact-free EEG epoch was digitally filtered with three bandpasses: (i) a narrow band in the 5 11 Hz band, chosen on the basis of spectral analysis and which

3 Intracerebral study of human sensorimotor rhythms 949 corresponds to the subject s mu rhythm; (ii) a Hz band, which corresponds to beta rhythms; and (iii) a Hz band, which corresponds to low gamma rhythms. Filtered EEG samples were then squared and averaged over all trials to calculate the mean power change. In order to reduce the variance, temporal resolution was reduced so as to obtain one power value every 32.5 ms, so that 256 values of ERD represented the temporal change in desynchronization from 4 s before to 4 s after movement onset. Each of these 256 mean power values (P) was then expressed as a percentage of a reference power value (R) computed within the time interval from 3.5 to 2.5 s before movement onset: ((R ) P R) 100). Negative and positive values indicate desynchronization and synchronization, respectively. The significance of the differences in mean power between the reference period and subsequent 32.5-ms intervals was also expressed as a probability value (P), using non-parametric statistics (Wilcoxon s signed ranks test). We decided to define the onset of ERD S as the onset of a deflection comprising at least three successive, statistically significant ERS values. Results The onset latencies and maximal amplitudes of recorded MRCPs, mu ERD, beta ERS and gamma ERS are given in Table 1. MRCPs MRCPs were recorded in seven out of the eight subjects. Different components were observed, sometimes in a given subject. Examples of MP and PMc are given in Fig. 2. A MP was observed in four subjects (1, 3, 6, 7) and in 11 contacts out of the 126 exploring the pre- and postcentral gyri in the subjects as a whole. It was located in the precentral gyrus in three subjects (3, 6, 7) (in eight out of 86 contacts) and in the postcentral gyrus in subject 1 (in three out of 40 contacts exploring the postcentral gyrus in the subjects as a whole). The MP began just before movement ()55 ± 21 ms) and peaked just after movement onset (27 ± 11 ms): it had a positive polarity in all subjects. Figure 2 illustrates MP in subjects 6, 7 and 1. Table 1. Latencies and amplitudes of MP, PMc, mu ERD, beta ERS and gamma ERS recorded within each of sensorimotor areas MRCPs Latency to peak (ms) Mu ERD Beta ERS Gamma ERS Subjects and locations of electrodes MP PMc Latency (ms) Amplitude (lv) Latency (ms) Amplitude (lv) Latency (ms) Amplitude (lv) (1) M, 19 y, R-handed Precentral gyrus )2000 )96% % % Postcentral gyrus )625 )90% % % Frontal lateral cortex +250 )42% Frontal medial cortex )250 )40% (2) F, 36 y, L-handed Precentral gyrus )1125 )81% Postcentral gyrus +375 )72% % Frontal lateral cortex Frontal medial cortex )375 )46% (3) F, 14 y, R-handed Precentral gyrus 23 )500 )55% % % Postcentral gyrus 80 )750 )80% % Frontal dorsal lateral cortex )375 )80% Frontal medial cortex )500 )75% (4) M, 37 y, R-handed Precentral gyrus 156 )125 )85% % % Postcentral gyrus 133 )125 )95% % % Frontal lateral cortex +375 )50% % Frontal medial cortex +375 )50% (5) M, 23 y, R-handed Precentral gyrus % Postcentral gyrus 0 50% % % Frontal lateral cortex )250 45% % % Frontal medial cortex % (6) F, 33 y, R-handed Precentral gyrus )625 )80% % % Postcentral gyrus 100 )500 )95% % % Frontal lateral cortex )375 )85% % Frontal medial cortex )250 )65% % (7) M, 31 y, R-handed Precentral gyrus )125 )90% % % Postcentral gyrus 0 )85% % Frontal lateral cortex 0 )70% Frontal medial cortex 0 )80% % (8) M, 23 y, R-handed Precentral gyrus )125 )80% % Postcentral gyrus )250 )85% % Frontal lateral cortex 0 )80% Frontal medial cortex +375 )35%

4 950 W. Szurhaj et al. Fig. 2. MRCPs recorded in subjects 1 (A), 6 (B) and 7(C). Motor potentials (MPs) and postmovement complexes (PMcs) are emphasized. All the contacts were located within the cortex. Note that their respective maximum amplitudes are observed in different, but adjacent, contacts. A PMc was observed in five subjects. It was located in the precentral gyrus in four subjects (3, 4, 6, 7) and in the postcentral gyrus in a slightly different set of four subjects (1, 3, 4, 6), i.e. three individuals displayed a PMc in both the pre- and postcentral gyri. The PMc was sometimes polyphasic (subjects 1, 4, 6) (Fig. 3A, subject 6; Fig. 5A, subject 1). The latencies given in the text below concern the first peak. In the precentral gyrus, the PMc began with variable latency but was generally around the movement onset (from )170 to +40 ms). However, onset was sometimes difficult to determine accurately because of a possible overlap between the initial MP and PMc slopes, and perhaps also the pre-movement slow potential, such as NS. The potential peaked at about +130 ms (± 43 ms). In three subjects (3, 6, 7), we recorded both MP and PMc in the same electrode, although the respective maximum amplitudes were observed in different (but adjacent) contacts (see Fig. 2). The MP was located more deeply than the PMc, i.e. in contacts located more internally than those displaying a PMc. A PMc was observed in the postcentral gyrus in four subjects (1, 3, 4, 6), and in 12 contacts out of the 40 exploring this area for the subjects as a whole (see Figs 2B and 3A for subject 6; and Figs 2A and 4A for subject 1). It began just after movement onset (37 ± 8 ms) and peaked at 112 ± 26 ms, with a mean amplitude that varied from 30 lv to 180 lv. In subjects 2, 4 and 5, potentials were indeed recorded in other contacts located in the postcentral gyrus, but the latency was too great (in fact, it followed the movement in subject n 4) and or the slope was not steep enough for the signal to be considered as a PMc. We recorded other slow potentials in the parietal opercula area (subject n 3, starting just before the movement onset) and the frontal, lateral (three contacts) and medial (two contacts) cortex (subject n 5, starting during movement). The amplitudes were moderate (between 12 and 30 lv). ERD S responses Mu and beta ERD were recorded very broadly across the whole sensorimotor cortex in each subject, except for subjects 2 and 5 in whom mu or beta ERD were absent in one or more areas (see Table 1 for the mu ERD). ERD generally began before or at movement onset (latencies from )2000 ms to 0 ms). The maximal amplitudes were

5 Intracerebral study of human sensorimotor rhythms 951 Fig. 3. MRCPs (A) and mu, beta, gamma changes (B) in subject 6. The reconstructed electrode M, superimposed upon the post-implantation MRI slice showing its track, is displayed on axial views (C). M 11 and more internal contacts are located in the precentral gyrus. The contact M 12 is located in the postcentral gyrus. Note that mu ERD, beta ERD and beta ERS are recorded widely. Gamma ERS is focused. It is only recorded from contacts displaying a PMc. reached during movement. Mu and beta ERD were predominant in the pre- and postcentral gyri in all subjects. Desynchronization lasted throughout the movement, with a slow return to baseline for the mu rhythm and a steep return for the beta rhythms. In six subjects, beta ERD was followed by ERS in the precentral gyrus (all six subjects), postcentral gyrus (five subjects), frontal lateral cortex (three subjects) and frontal medial cortex (three subjects). When present, this ERS never occurred before movement offset. A mu ERS was recorded in one subject (n 1) from just a single contact in the postcentral gyrus. Gamma ERS was observed in the central region (precentral gyrus, postcentral gyrus and opercular area) in all subjects. We recorded it from 23 out of a total of 86 contacts exploring the precentral gyrus (six out of eight subjects). Seventeen contacts were located in the hand motor area, three in the opercular part of the precentral gyrus and three in the anterior part of the paracentral lobulus. We found postcentral gamma ERS in all subjects, and in 20 out of 40 contacts exploring the postcentral gyrus. Seventeen contacts explored the hand somatosensory area, and three explored the opercular part of the postcentral gyrus. We also observed gamma ERS in the frontal, lateral cortex in one subject (n 5), and in the SMA in two subjects (5 and 6). It occurred either at movement onset or after movement offset. Correlation between ERD S and MRCPs Even though MRCPs always occurred in regions where we observed mu and beta ERD, the latter were more diffuse than the MRCPs. Beta ERS was more focused than mu and beta ERD but was nevertheless more diffuse than the MRCPs. Moreover, beta ERS occurred later than the late MRCP components and always after movement offset. The highest spatial correlation was found with gamma ERS: we only recorded MPs and PMcs from contacts where we had also observed gamma ERS (see Figs 3 5). In the pre- and postcentral gyri, MPs and PMcs were detected in 24 contacts out of the 34 where we found gamma ERS. However, MPs started before the movement and the onset of the gamma ERS, whereas PMc peaks always occurred during gamma ERS in the pre- and postcentral gyri (except in subject 1). PMc onset was more variable: in the precentral gyrus, it occurred with the gamma ERS in one case, after it in another case and before it in two cases. In the postcentral gyrus, PMc started after the gamma ERS (again with the exception of subject 1). In subject n 5, slow MRCPs were recorded in the medial and lateral frontal cortex. We also detected gamma ERS in the same contacts. In subject n 2, we recorded a MRCP and gamma ERS in the parietal opercular area from different (but adjacent) contacts.

6 952 W. Szurhaj et al. Fig. 4. MRCPs (A) and mu, beta, gamma changes (B) in subject 7. (C) Diagram of implantation. The electrode M is located in the precentral gyrus. Mu ERD, beta ERD and beta ERS are recorded widely. Note the spatial overlap between MP PMc and gamma ERS locations. Discussion We observed two kinds of potentials (MP and PMc) in the pre- and postcentral gyri, sometimes in adjacent contacts. There was a spatial overlap between MP PMc and gamma ERS locations, whereas mu and beta reactivities were more diffuse: MP PMc only occurred in contacts having also displayed a gamma ERS. MPs always began earlier than gamma ERS but, in most cases, the PMc peaks occurred during the gamma ERS. Contribution to our knowledge of the sources of MPs PMcs Late MRCP components were predominantly observed in the primary sensorimotor areas. We observed a slow potential in the SMA in only one subject, and the slope was not steep enough for it to be considered as an MP. It was similar to the movement-accompanying slow potentials reported by Rektor et al. (1998). Absence of MPs in the SMA agrees with the observations of Neshige et al. (1988a,b). Furthermore, the lack of MPs argues against an executive role of SMA during simple finger movements. However, we acknowledge that our spatial sampling was limited by use of the SEEG technique. Moreover, the SMA was only explored by a few contacts. It is possible that potentials did occur but were too far from our electrodes to be detected. We show here that the MP has its source in both the pre- and postcentral gyri. MP is considered as reflecting the activation of the cortex during the latter s generation of the pyramidal tract volley. Lee et al. (1986) previously recorded a similar activity over the postcentral gyrus. These findings argue in favour of a role of the primary somatosensory area (S1) in movement execution in the human brain, as already demonstrated in the monkey brain (Soso & Fetz, 1980). It can be argued that MPs recorded in the postcentral gyrus may be due to spreading of the electrical activity from the precentral gyrus into the adjacent tissue. Nevertheless, this is unlikely because depth electrodes record electrical activity that is generated in close proximity to the contact, in a volume of just a few cubic millimetres. Moreover, as can be seen from the figures, two adjacent contacts may display very different potentials. Hence, the electrical activity that is recorded from one contact has only a moderate influence on the adjacent contact. Because the PMc peaks at about ms after movement onset, it is likely to be a component of the RAP described in scalp recording. RAP supposedly reflects the kinesthesic sensory projections to the S1 (Lee et al., 1986; Tarkka & Hallett, 1991). Our data confirm that both S1 and primary motor area (M1) participate in generation of the RAPs. We note with interest that MP and PMc are detected in different but adjacent contacts in the three subjects in whom we recorded both potentials. This finding may suggest that they are generated by different neuronal populations. In other words, this could mean that kinesthesic sensory afferences project to neurons other than those firing during the pyramidal tract volley. Contacts where we observed PMc were located more externally on the electrode, i.e. closer to the central sulcus (due to the electrode s orientation) than those displaying

7 Intracerebral study of human sensorimotor rhythms 953 Fig. 5. MRCPs (A) and mu, beta, gamma changes (B) in subject 1. (C) Diagram of implantation. The electrode N is located in the postcentral gyrus. Mu ERD, beta ERD and beta ERS are recorded widely. Note the spatial overlap between MP PMc and gamma ERS locations. MP. This finding argues in favour of different functional maps within M1, with a posterior part receiving kinesthesic inputs from joints and muscles involved in the movement and an anterior part with an executive function. This proposal may concord with the study of Geyer et al. (1996) in which positron emission tomography revealed greater activation of the posterior part of area 4 during a roughness discrimination task than during a movement task. Relationships between MRCPs and oscillation changes Basic mechanisms (and thus their respective meanings) of MRCPs and rhythms changes are almost certainly different: extracellular and intracellular recordings have revealed postsynaptic potentials to be the main factors underlying cortical potentials, whereas rhythm reactivity reflects changes in functional connectivity within the cortex (Lopes da Silva & Pfurtscheller, 1999). However, we can suppose that some of their components are linked and reflect two electrophysiological facets of a similar process. As is already known from scalp recordings and electrocorticography, our SEEG results confirmed that there is no strong correlation between MRCPs and mu beta rhythm changes. Mu and beta ERDs are spread out across the whole sensorimotor cortex, and the exact significance of these events remains unclear. However, we show here that there is a strong relationship between PMcs and gamma ERS, thus suggesting that they are related to the same phenomenon. This also suggests a relationship between gamma ERS in the sensorimotor cortex and somesthesic integration during movement, as suggested by a few previous studies (Aoki et al., 1999; Ihara et al., 2003; Szurhaj et al., 2005). Gamma ERS in the primary sensorimotor areas may support afferent sensory feedback from the joints and muscles involved in movement. Certain studies have demonstrated that gamma oscillations were strongly associated with ongoing movement (Salenius et al., 1996; Donoghue et al., 1998), and that they were clearly correlated with EMG rhythmicity in the extensor muscles (Mima et al., 2000). Hence, it has been suggested that the 40 Hz rhythm reflects communication between the sensorimotor cortex and the motor units. Our data do not permit us to confirm this hypothesis, as gamma ERS was recorded at or after movement onset and after the onset of the MP s initial slope. However, in the present work, we only explored the Hz band and thus cannot rule out the possibility that gamma rhythms of higher frequency may play such a role. The significance of the gamma ERS seen here remains unclear. The main rationale behind gamma rhythms seems to be a binding function between different neuronal populations involved in parallel processing (Singer, 1993). Hence, it could be suggested that gamma oscillations within the Hz band serve to functionally link the different neuronal populations involved in the movement, i.e. the cortico-spinal cells driving the muscles and the somatosensory neurons receiving kinesthesic sensory feedback. Synchronization of the neuronal populations activities may serve to facilitate afferences from the muscles and joints involved in the movement to the motor cortico-spinal cells, which would be necessary for controlling the ongoing movement.

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