Inherent differences in difficulty between on the beat (synchronization) and off the beat (syncopation) coordination modes are well known. Synchronization is typically quite easy and, once begun, may be carried out with little apparent attention demand. Syncopation tends to be difficult, even though it has been described as a simple, phase-shifted version of a synchronized pattern. We hypothesize that syncopation, unlike synchronization, is organized on a cycle-by-cycle basis, thereby imposing much greater preparatory and attentional demands on the central nervous system. To test this hypothesis we used fMRI to measure the BOLD response during syncopation and synchronization to an auditory stimulus. We found that the distribution of cortical and subcortical areas involved in intentionally coordinating movement with an external metronome depends on the timing pattern employed. Both synchronized and syncopated patterns require activation of contralateral sensorimotor and caudal supplementary motor cortices as well as the (primarily ipsilateral) cerebellum. Moving off the beat, however, requires not only additional activation of the cerebellum but also the recruitment of another network comprised of the basal ganglia, dorsolateral premotor, rostral supplementary motor, prefrontal, and temporal association cortices. No areas were found to be more active during synchronization than syncopation. The functional role of the cortical and subcortical regions areas involved in syncopation supports the hypothesis that whereas synchronization requires little preparation and monitoring, syncopated movements are planned and executed individually on each perception-action cycle.
We used a 61-channel electrode array to investigate the spatiotemporal dynamics of electroencephalographic (EEG) activity related to behavioral transitions in rhythmic sensorimotor coordination. Subjects were instructed to maintain a 1:1 relationship between repeated right index finger flexion and a series of periodically delivered tones (metronome) in a syncopated (anti-phase) fashion. Systematic increases in stimulus presentation rate are known to induce a spontaneous switch in behavior from syncopation to synchronization (in-phase coordination). We show that this transition is accompanied by a large-scale reorganization of cortical activity manifested in the spatial distributions of EEG power at the coordination frequency. Significant decreases in power were observed at electrode locations over left central and anterior parietal areas, most likely reflecting reduced activation of left primary sensorimotor cortex. A second condition in which subjects were instructed to synchronize with the metronome controlled for the effects of movement frequency, since synchronization is known to remain stable across a wide range of frequencies. Different, smaller spatial differences were observed between topographic patterns associated with synchronization at low versus high stimulus rates. Our results demonstrate qualitative changes in the spatial dynamics of human brain electrical activity associated with a transition in the timing of sensorimotor coordination and suggest that maintenance of a more difficult anti-phase timing relation is associated with greater activation of primary sensorimotor areas.
For low rhythmic rates (1.0 to approximately 2.0 Hz), subjects are able to successfully coordinate finger flexion with an external metronome in either a syncopated (between the beats) or synchronized (on each beat) fashion. Beyond this rate, however, syncopation becomes unstable and subjects spontaneously switch to synchronization to maintain a 1:1 stimulus/response relationship. We used a whole-head magnetometer to investigate the spatiotemporal dynamics of neuromagnetic activity (MEG) associated with both coordinative patterns at eight different rates spanning the range 1.0-2.75 Hz. Timing changes in the event-related fields accompanied transitions from syncopation to synchronization and followed the placement of the motor response within each stimulus/response cycle. Decomposition of event-related fields into component auditory and motor brain responses revealed that the amplitude of the former decreased with increasing coordination rate whereas the motor contribution remained approximately constant across all rates. Such an interaction may contribute to changes in auditory-motor integration that cause syncopation to become unstable. Examination of event-related changes in high frequency bands revealed that MEG signal power in the beta band (15-30 Hz) was significantly lower during syncopated coordination in sensors covering the contralateral sensorimotor area suggesting a dependence of beta rhythm amplitude on task difficulty. Suppression of beta rhythms was also stronger during synchronization preceded by syncopation, e.g., after subjects had switched, when compared with a control condition in which subjects synchronized throughout the entire range of rates.
We have studied the effect of movement rate on MEG activity associated with self-paced finger movement in four subjects to determine whether the amplitude or latency of motor-evoked activity changes across a range of rates. Subjects performed a continuation paradigm at 21 distinct rates (range: 0.5-2.5 Hz) chosen because of their relevance for many types of sensorimotor coordination (e.g. musical performance). Results revealed a pair of field patterns whose topography and temporal dynamics were similar across all subjects. The strongest pattern was a movement-evoked field (MEF) that emerged during the response and exhibited one or two polarity reversals in time depending on the subject. The MEF complex was tightly coupled to the biphasic response profile but neither latency nor peak amplitude of each MEF component had significant dependence on the temporal duration between successive responses, i.e. movement rate. In contrast, the maximal amplitude of a second, weaker pattern decreased by over 50% when movement rates exceeded 1.1 Hz (inter-response interval <1 s). This pattern was characterized by a change in field line direction over the midline of the scalp and a gradual accumulation of amplitude prior to movement onset. Both characteristics are suggestive of a readiness field. The observed rate-dependent changes in this field may contribute to known transitions in sensorimotor coordination that emerge when the frequency of coordination is increased.
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