Cortical and subcortical networks underlying syncopated and synchronized coordination revealed using fMRI

Abstract

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.

Emergence of rhythm during motor learning

“…This can be viewed as a shift from controlled to automatic timing processes. A similar shift in brain activation from cognitive to motor-related areas is also observed when subjects switch from a syncopation mode to a synchronization mode when responding to an isochronous series of external stimuli [20,[27][28][29]. Syncopated movements are thought to be performed as a series of independent movements that are planned and executed on each perception-action cycle.…”

A parametric fMRI investigation of context effects in sensorimotor timing and coordination

“…BOLD patterns observed during continuation depend directly on whether subjects synchronize (move coincident with stimuli) or syncopate (move between stimuli) with the pacing metronome (Jantzen et al, 2004) during the pacing phase. Task related differences in BOLD activity distinguishing these coordination patterns Mayville, Jantzen, Fuchs, Steinberg, & Kelso, 2002) persist during continuation despite similar sensorimotor and timing constraints. Such findings suggest that the neural representation of a temporal interval may be flexibly determined by the sensory and motor systems engaged during timing acquisition (pacing) and that subsequent temporal processing based on this interval (continuation) continues to rely on the same neural representation.…”

Stabilization of bimanual coordination due to active interhemispheric inhibition: a dynamical account

“…Baraldi et al (1999) found support for the participation of two separate neural populations in each hemisphere, one in M1 and one in PM1: the first being activated during contralateral finger movements only, whereas the second exhibited signal changes during movements of either hand, indicating that unimanual movements are accompanied by cortical activity in both hemispheres. Compared to paced movements, self-paced rhythmic finger movements generally recruit more and larger neuronal populations that typically include (bilateral) SMA (Halsband et al 1993;Freund 1996;Kaiser et al 2000; and (ipsilateral) PM1 (Stippich et al 2000), especially during difficult tasks (Mayville et al 2002). In addition, several research groups found unilateral cortical activation during discrete and (symmetrical) bihemispheric activation during sequential unimanual motor behaviors (Cheyne and Weinberg 1989;Pulvermüller et al 1995;Manganotti et al 1998;Andrew and Pfurtscheller 1999;Babiloni et al 1999;Pfurtscheller et al 2000), indicating the presence of an active (time-varying) cross-talk between bilateral and mesial central and prefrontal regions.…”