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1Department of Neurology, the Neurological Institute, Taipei Veterans General Hospital, Taipei; 2Department of Neurology, National Yang-Ming University, Taipei; 3Department of Neurology, Cathay General Hospital, Taipei, Taiwan; and 4National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland
Submitted 3 November 2003; accepted in final form 23 August 2004
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ABSTRACT |
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INTRODUCTION |
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). Rhythmic movements can be modulated by sensory input and descending influences from the brain stem or higher motor centers (Elble and Koller 1990).
Hemispheric dominance for motor control in humans is suggested by multiple lines of evidence. For example, in right-handers the transcallosal inhibition after transcranial magnetic stimulation (TMS) of the dominant left hemisphere was more marked than after stimulation of the nondominant right hemisphere (Netz et al. 1995). Using TMS to investigate corticospinal excitability in right-handed subjects, contralateral inhibition was more efficient for left hemisphere stimulation than for right (Leocani et al. 2000).
Interhemispheric connections appear to be important for bimanual coordination. Acallosal patients commit more errors in bimanual tapping tasks than normal subjects (Leonard et al. 1988). Interhemispheric EEG alpha coherence is increased during bimanual rhythmic tasks in children (Knyazeva et al. 1994). Interhemispheric EEG coherence increases in initial training but then decreases in a well-trained bimanual coordination task (Andres et al. 1999).
To test the influence of different inputs on an oscillation generator, the technique of phase resetting can assess whether a given input can reset the pacemaker to a fixed phase in its cycle; if it does so, then the input exerts a significant influence over the oscillator (Winfree 1980). Phase resetting can be quantified with the method of "resetting index" (RI). Using this method, the afferent influence on Parkinson tremor and essential tremor has been measured (Lee and Stein 1981). The measure is also potentially applicable to study any input on any type of repetitive activity including voluntary rhythmic movements (Wagener and Colebatch 1996). Unilateral TMS exerts both excitatory and inhibitory effects. By applying TMS to the motor cortex, it may reset Parkinson tremor, essential tremor (Britton et al. 1993; Pascual-Leone et al. 1994), orthostatic tremor (Tsai et al. 1998), palatal tremor (Chen et al. 2000), and regular voluntary muscle contraction of contralateral upper limb (Britton et al. 1993; Wagener and Colebatch 1996). The rhythm resetting is closely related to the silent period provoked by TMS (Pascual-Leone et al. 1994). This indicates that TMS modulates activity through an inhibitory effect on the neural network from the oscillator to the execution system (Britton et al. 1993; Wagener and Colebatch 1996). Here, we studied: 1) whether TMS applied to one hemisphere resets the rhythmic movements of bimanual tasks; 2) whether there is any difference between TMS disruption to ipsilateral and contralateral finger tapping; 3) whether the TMS effect differs between unimanual and bimanual rhythmic tasks; 4) whether there is any difference of the TMS effect between bimanual in-phase and antiphase tasks; and 5) whether there is hemispheric dominance of the TMS effect on bimanual rhythmic task.
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METHODS |
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Six healthy right-handed volunteers (5 males, 1 female; age: 26–36 yr) were studied. Experiments were approved by the IRB and informed consent was obtained.
Electromyographic (EMG) recording
Each subject sat in front of a table and kept his/her arms on the table. Two surface electrodes, 1 cm apart, were put on the muscle belly of the extensor digitorum communis of both forearms with ground lead on one wrist. EMG activity was fully rectified and recorded 4 s before and 6 s after TMS with a band-pass 20–3K Hz and was stored in an EMG machine (Nihon Kohden, Neuropack 8). After the procedure, EMG recordings could be recalled, digitally smoothed using a 5-point running mean, and averaged for further analysis.
TMS
TMS was delivered with a figure-of-eight coil (Magstim 200, Camarthenshire, UK) placed over the motor cortex, with the handle held posteriorly and oriented sagittally for focal stimulation. The precise coil position was adjusted to yield a maximal response in the target muscle at a given stimulus intensity. The appropriate coil position was marked. Motor threshold (MT) was defined in the relaxed forearm muscle as the intensity to elicit 
5 motor-evoked potentials (MEPs) with peak-to-peak amplitude more than 100 µV in 10 consecutive stimuli. In checking for MT, we used stimulus intensities beginning at 70% of maximal output and then gradually decreased the intensity in 2% steps until appropriate MEP amplitudes were obtained. Respective MTs of the right and left forearm muscles were defined in each subject. The interval between 2 stimuli was 30 s.
UNILATERAL TMS TO CONTRALATERAL AND IPSILATERAL FINGER TAPPING.
Each subject was asked to maintain rhythmic tapping of the index finger of either the right or left hand at a freely chosen, comfortable rhythm. After practicing for several times, rhythm and EMG signals were monitored on the EMG machine until the rhythm was stable and EMG amplitude of each burst was similar. TMS, set at 0.5MT initially with an increment of 20% MT intensity 
1.5MT, was delivered randomly over the left motor cortex and then right motor cortex. The time interval between each EMG burst was monitored on the EMG machine and was measured in each experiment session to ensure that the variation of the time interval was not larger than one SD to keep the frequency constant. The time interval of TMS to both hemispheres was 1 h. The time interval for testing at each intensity was 10 min. Twenty EMG recordings of each hand were collected.
UNILATERAL TMS TO BIMANUAL IN-PHASE FINGER TAPPING. Subjects were instructed to tap the index fingers of both hands simultaneously and synchronously at the rhythms they could most easily maintain. Monitoring and TMS were done as the first experiment. TMS was delivered randomly first to the left motor cortex and then to the right motor cortex. Twenty trials were recorded at each magnetic intensity.
UNILATERAL TMS TO BIMANUAL ANTIPHASE FINGER TAPPING.
Subjects maintained rhythmic tapping of the index fingers alternatively. Antiphase finger tapping was defined as one index tapping and the other lifting from the table. The task was monitored by the EMG machine. The rhythm of both fingers was the same but the EMG burst of one hand was about the middle of 2 EMG bursts of the other hand (i.e., there was the same rhythm in both hands with an opposite phase). TMS would not be delivered if the rhythm did not reach a steady state. Test stimuli were delivered at 1.5MT. TMS was delivered randomly first to the left motor cortex and then to the right motor cortex; 20 trials were collected for each side.
Analysis
The RI was used to quantify the influence of TMS on unimanual and bimanual rhythmic movements (Lee and Stein 1981) and was also described in our previous study in palatal tremor (Chen et al. 2000). Data reduction was as follows: 1) The peaks of the last 5 EMG bursts before TMS in individual trials were identified manually; intervals between the burst peaks were measured as actual intervals. The mean of these 4 interpeak cycle intervals was the averaged interval (ave I). 2) The time between the last EMG burst before TMS and TMS was determined as a proportion of the averaged interval (%I). 3) The interval between TMS and the first EMG burst after TMS was defined as the silent period (SP) after TMS and was measured as the latency of the rhythmic movement reappearance and was also determined as a proportion of the averaged interval. 4) Intervals of the first 5 EMG bursts after TMS were also measured as a proportion of the averaged interval (I1' -I5'). The predicted time for the 5 bursts after TMS was calculated from the base of the averaged time interval of the last movement burst before TMS. 5) The difference between the actual and predicted time interval of the first 5 bursts after TMS [d = (I' – I)/ave I] was plotted against the time interval of the last EMG before TMS (%I) in each single trial (Fig. 1A). For each trial, one point was plotted in each of 5 graphs, one for each of the first 5 bursts after TMS. Because the time for delivering TMS varied randomly in each trial, the plotted points in each stimulus condition were combined to calculate 5 linear regressions, one for each of the 5 intervals after TMS. The time to deliver TMS varied randomly across trials, and the plotted points for all trials with a given stimulus condition were combined to calculate 5 individual linear regressions, one for each of the first 5 bursts after TMS. RI was defined as the average slope of the regression lines for these 5 bursts after TMS. The x-axis was the interval of the last EMG burst before TMS (%I); the y-axis was the interval of actual burst minus the predicted burst (d) (Fig. 1B). If TMS caused a prominent effect to make SP near constant, the slope would be near 1. If TMS caused no disruption, there would be no SP and the slope would be near 0. Therefore resetting was absent if RI equaled 0, and was complete if it equaled 1.
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For visual display, 20 rectified EMG trials were averaged. Because the stimuli were delivered randomly during the movement cycle interval, the movement bursts before TMS are flattened as a result of the effect of averaging out. EMG activity after TMS shows a burst pattern as a result of this superimposition if TMS resets the rhythmic movement.
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RESULTS |
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During the unimanual task, TMS affected both contralateral and ipsilateral hand tapping and correlated well with TMS intensity (Fig. 2A). This was also shown by SP duration. RI, even at subthreshold intensities, was relatively high, which might be attributable to activity of the motor cortices during finger tapping compared with the rest state. RI was not correlated with the tapping frequency at any intensity of either hemisphere during either the unimanual or bimanual task. In the unimanual finger tapping, the contralateral RI was significantly higher than the ipsilateral RI, regardless of which hemisphere TMS was applied (left TMS: P = 0.0001; F = 37.34, right TMS: P = 0.0003; F = 14.67). Post hoc testing showed that RI was significantly less in the ipsilateral than in the contralateral hand from 0.7 to 1.5MT (P = 0.0051 at 0.7MT; P = 0.0049 at 0.9MT; P = 0.0051 at 1.1MT; P = 0.0051 at 1.3MT; P = 0.0051 at1.5MT) to left TMS (Fig. 2B) and from 1.1 to 1.5MT (P = 0.0004 at 1.1MT; P = 0.0001 at 1.3MT; P = 0.0001 at 1.5MT) to right TMS (Fig. 2C). When we compared the side difference for contralateral TMS on the unimanual task, RI of the right hand to left TMS was higher than that of the left hand to right TMS (P = 0.035; F = 4.64). Post hoc tests showed significant differences at 0.7 and 1.3–1.5MT (P = 0.005 at 0.7MT; P = 0.0051 at 1.3MT; P = 0.0051 at 1.5MT). There was no difference in the ipsilateral RI of TMS to either hemisphere (P = 0.44; F = 0.44).
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There was no difference among the 5 RIs after TMS in unimanual or bimanual in-phase tasks and to TMS of either hemisphere. At higher magnetic intensities, the RI of each muscle burst after TMS gradually decreased in the contralateral hand during bimanual movements (Fig. 4A), although this trend was not significant. This was not seen in the ipsilateral hand (Fig. 4B).
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SP after TMS was correlated with RI for both uni- and bimanual in-phase tasks and for both hemispheres. Contralateral SP was significantly longer than the ipsilateral SP to left TMS (P = 0.0021; F = 10.17) and to right TMS (P = 0.001; F = 15.34) in the unimanual task. When we compared the SP at each intensity, the SP of the contralateral hand was significantly longer than the ipsilateral one at 0.7 to 1.5MT (P = 0.0001 at each MT) to left TMS in the unimanual task (Fig. 5A) and 0.9MT (P = 0.047), 1.1MT (P = 0.008), 1.3MT (P = 0.003), and 1.5MT (P = 0.006) to right TMS. There was no difference between the contralateral SP (P = 0.25; F = 1.33) or the ipsilateral SP (P = 0.38; F = 1.05) to left and right TMS. In the bimanual in-phase task, SP of the contralateral hand was longer than that of the ipsilateral hand when TMS was applied to either hemisphere (left TMS: P = 0.001; F = 13.83, right TMS: P = 0.031; F = 4.86) (Fig. 5B). Comparing TMS to left or right side, there was no significant difference in contralateral SP (P = 0.44; F = 0.60) or ipsilateral SP (P = 0.48; F = 0.50).
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In bimanual finger tapping, TMS produced less disruption on both hands in the antiphase task than in the in-phase task (Fig. 6A). RI of both hands with TMS to either hemisphere in the antiphase task was less than that in the in-phase task (P = 0.0001 in left and right TMS). There was no hemispheric difference (P = 0.70) in left or right TMS in bimanual antiphase movement. There was no difference in contralateral resetting (P = 0.65) or ipsilateral resetting (P = 0.47) when TMS was applied to either hemisphere. The contralateral RI was larger than the ipsilateral one (left TMS: P = 0.0155; right TMS: P = 0.0062). With TMS at 1.5MT to left motor cortex, the contralateral RI was 0.130 ± 0.047 in antiphase movement and 0.752 ± 0.049 in in-phase movement (P = 0.0001). With TMS at 1.5MT to right motor cortex, the contralateral RI was 0.116 ± 0.040 in antiphase movement and 0.699 ± 0.050 in in-phase movement (P = 0.0001). The ipsilateral RI in the antiphase movement at 1.5MT was also less (0.030 ± 0.016 in left TMS; 0.021 ± 0.017 in right TMS) than that in in-phase movement (0.629 ± 0.073 in left TMS; 0.576 ± 0.063 in right TMS) (P = 0.0001). RI for the first interval was the highest, and then declined in the following intervals in both hands during TMS to left and right hemispheres (Fig. 6B). In the in-phase movement, although there was transient suppression after TMS, both hands tapped concomitantly in the recovery phase. In the antiphase movement, although the TMS suppression phenomenon was not so marked, there was a phase transition from antiphase to in-phase immediately after TMS, especially at high intensity (Fig. 7). There was no significant change in the cycle interval before and after TMS.
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DISCUSSION |
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With unimanual movement, TMS more easily disrupted contralateral than ipsilateral movement. In unimanual movement, TMS disrupted contralateral rhythmic movements, as studies in normal subjects (Britton et al. 1993) and patients with Parkinson's tremor and essential tremor (Pascual-Leone et al. 1994) have shown. TMS had far less blocking effect on ipsilateral movement in our study. This blocking might be a direct effect of TMS on the motor cortex, although sensory feedback may also play a significant role. The resetting and the SP of both the contralateral and ipsilateral hands were correlated with magnetic intensities, as the results in patients with Parkinson's tremor and essential tremor (Pascual-Leone et al. 1994) and in palatal tremor (Chen et al. 2000) have demonstrated. Britton et al. (1993) argued that the action level was at the motor cortex because torque pulses were relatively ineffective in evoking resetting. Tremor resetting was correlated with SP, but not MEP amplitude (the muscle twitch) elicited by TMS (Pascual-Leone et al. 1994). In addition, resetting still exists when the perturbation effect is avoided and correlates with the first poststimulus EMG burst, which indicates a direct effect from TMS to the motor cortex (Wagner and Colebatch 1996). In our study, TMS at subthreshold intensity could still reset the rhythm without MEPs in the contralateral hand, and there was minimal resetting in the ipsilateral hand, even though no MEPs were measured.
Even though motor control is mainly contralateral, there are some possible reasons why TMS can influence the ipsilateral hand.
1) TMS may produce inhibitory effects on the opposite hemisphere (Ferbert et al. 1992) by the corpus callosum (Schnitzler et al. 1996) (Fig. 7A). TMS can produce an ipsilateral silent period and this appears to be mainly through transcallosal inhibition (Ferbert et al. 1992; Wassermann et al. 1991).
2) TMS may produce a transcallosal effect by influences on premotor cortices to affect the other hemisphere. Repetitive TMS over primary motor cortex can also increase supplementary motor area (SMA) activation (Siebner et al. 2001). In primates, hand representations of SMA are strongly interconnected by the corpus callosum (Rouiller et al. 1994), and lesions of the SMA can interrupt bimanual coordination (Chan and Ross 1988; Laplane et al. 1977).
3) TMS may have influence by an ipsilateral descending pathway. Positron emission tomography (PET) studies in humans demonstrate that finger or hand movements cause significant activation in the ipsilateral primary motor cortex (Blinkenberg et al. 1996; Shibasaki et al. 1993). At high stimulation intensities, TMS can elicit MEPs from ipsilateral limb muscles including the intrinsic hand muscles (Wassermann et al. 1991, 1994; Ziemann et al. 1999). This effect is likely by an uncrossed corticospinal and/or corticoreticulospinal pathway. Therefore TMS could affect a hypothetical ipsilateral oscillator system.
With bimanual in-phase movement, the 2 hemispheres influence each other mutually because, compared with unimanual movement, it becomes more difficult to disrupt contralateral movement and easier to disrupt ipsilateral movement. The RI of the contralateral hand to TMS in the bimanual task was lower than that in the unimanual task, whereas RI of the ipsilateral hand to TMS in the bimanual task was significantly higher than that in the unimanual task. The RI difference between the 2 hands decreased more in the bimanual task than in the unimanual task. It appeared that control of bimanual in-phase movement was synchronized.
Many actions are performed in cyclic or repetitive forms. To execute such cyclic movement, time is supposed to be determined by an internal clock containing a temporal oscillator (Treisman et al. 1992, 1994). Wing and Kristofferson (1973) proposed a hierarchical 2-level model for finger tapping with a central timer to trigger a response and a motor implementation mechanism. This model was applied to the study of motor disorders (O'Boyle et al. 1996; Pastor et al. 1992; Wing et al. 1984). Results from neuroimaging studies suggested that the premotor cortices, particularly the SMA, might participate in these internal timing mechanisms. In a functional magnetic resonance imaging (fMRI) study, the primary motor cortex, SMA, premotor area, and prefrontal area were more activated in memory-timed than visually cued finger movement. This indicated that these areas were involved in the generation of accurate timing, possibly functioning as a central clock (Kawashima et al. 2000).
In bimanual movement, there is decreased movement variation, suggesting interactions between separate left and right pacemaker systems (Helmuth and Ivry 1996). The authors of this study inferred that 2 independent timers were integrated and averaged to reduce the tapping variability. Another example is that the reaction and movement times of bimanual pointing were indistinguishable in both hands even when manual complexity was different (Kelso et al. 1979). This clearly requires bilateral interaction. When attempting to disrupt one clock, the opposite clock can maintain the rhythm relatively well, making the disruption of the clock more difficult. Such evidence appears to favor an independent clock in each hemisphere, with cross talk between the hemispheres to produce bimanual coordination (Fig. 8B).
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There is an almost equal right and left hemisphere stimulation effect, indicating that there is no hemispheric dominance for running bimanual movement. In the unimanual task, TMS could interrupt the rhythm of the right hand more easily, although the difference was small. However, hemispheric dominance was minimal in the bimanual movement. In the bimanual movement, contralateral RI and SP to TMS were similar for the 2 hands. This indicates that the influence of the clocks is similar. The dominance of handedness in bimanual movements is controversial. There is evidence that the clocking systems for rhythmic movements in each hemisphere are independent of each other. There were no hemispheric differences in cortical activation in bimanual tasks in both fMRI (Toyokura et al. 1999) and PET studies (Fox et al. 1985). However, some authors argue that there is hemispheric dominance for bimanual coordination (Lang et al. 1990; Stucchi and Viviani 1993; Swinnen et al. 1996; Viviani et al. 1998).
In bimanual movement, antiphase movement was more difficult to disrupt than in-phase movement. It was difficult for TMS to reset the rhythm of the bimanual antiphase movement for either hand. The reason that TMS has more difficulty affecting the rhythmic movement in this condition might be the clock in the nonstimulated hemisphere. In the bimanual antiphase movement, the clocks dissociate and work independently with mutual correlation (Fig. 8C). If these clocks lost their connection completely in the antiphase movement, TMS disruption should be only in the contralateral hand, and the ipsilateral rhythm would continue. Magnetic intensity was based on the threshold of the rest state for the respective hemisphere. The actual threshold may vary in different conditions, and the TMS effect may not be comparable in both the antiphase and in-phase movements. Complex sequential finger movements recruit different brain areas, including the primary sensorimotor area, premotor area, SMA, cerebellum, and putamen (Sadato et al. 1996), and the sensorimotor cortex and SMA are activated much more for antiphase than for in-phase tasks (Immisch et al. 2001; Stephan et al. 1999; Toyokura et al. 1999).
An alternative hypothesis to TMS having a direct effect on motor cortex is that sensory feedback blocks ongoing movement. The afferent information from the perturbed hand elicited by TMS may contribute to resetting the timing signals. The interaction of the central clock with peripheral input has been difficult to determine (Elble and Koller 1990). The internal clock that determines time perception has been studied as a surrogate for this oscillator. When time intervals to be estimated are accompanied by auditory clicks that recur at certain critical rates, perturbations in time estimation occur (Treisman et al. 1992). This indicates that the internal clock was influenced by peripheral afferents. The sensory input attributed to limb perturbation by TMS might cause a similar perturbation of timing estimation of the clock and produce a resetting of rhythm.
Other arguments are consistent with the sensory reafferent theory. 1) The phase resetting increases with TMS intensity. The degree of perturbation would be greater as TMS increases, increasing the sensory reafferent flow. The clock might be disrupted by this sensory reafferent, and when TMS is of sufficient intensity, the disruption might force the oscillation to restart. Resetting would likely be done to overcome the effects of the perturbation. Voluntary rhythm can be reset not only by TMS but also by peripheral nerve stimulation (Colebatch and Wagener 1999) and by torque pulses (Britton et al. 1992). Some reports have mentioned the influence of sensory reafference in the repetitive tapping of isochronous intervals (Aschersleben and Prinz 1995; Wing 1977). 2) The nonperturbed hand can provide an attractor for the perturbed hand and cause less phase resetting during bimanual in-phase movements. During bimanual tapping, additional tactile–kinesthetic reafferences from the other hand provide more information to decrease the variability (Drewing et al. 2002). The increased sensory reafferent might reinforce the stability of both hands and decrease the TMS blocking effect. Meanwhile, the perturbed hand might also cause a lag in the rhythm on the other hand. 3) Given the reduced spatial correspondence of the 2 hands during antiphase movements, the hand ipsilateral to the TMS is not affected by the perturbation, and thus can provide a strong reference for phase resetting or to overcome the perturbation elicited by TMS. 4) There was minimal resetting that was greater in the first interval than that in the following intervals during antiphase tapping for the hand contralateral to stimulation. Perhaps the perturbation will cause delay in the next movement, which looks like a phase reset, but instead the hand quickly returns to an antiphase mode.
However, sensory reafference cannot be the only mechanism influencing rhythmic movements. In the study of the disruption of patterns in 2-limb coordination, passive mobilization of a third limb by the experimenter affected antiphase movement more than in-phase movement (Swinnen et al. 1995). This points to the differential stability of these patterns and suggests that antiphase coordination depends more on the monitoring of kinesthetic afferences than on in-phase coordination (Swinnen et al. 1995). This result is contrasted with ours. Therefore further investigation is needed to clarify the interaction of reafferent and central effects to the central clock.
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FOOTNOTES |
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Address for reprint requests and other correspondence: K.-K. Liao, Department of Neurology, the Neurological Institute, Taipei Veterans General Hospital, 201, Section II, Shih-Pai Rd., Pei-tou District, Taipei 11217, Taiwan (E-mail: kkliao{at}vghtpe.gov.tw)
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ABSTRACT
INTRODUCTION
