Distributed Neural Systems Underlying the Timing of Movements

TLDR

Timing is essential for skilled movements, but the neural systems that support timekeeping are poorly understood. Whole‑brain fMRI was used to image subjects tapping in synchrony with tones (Synchronization) and then tapping without an auditory cue (Continuation), with two control conditions involving tone listening and pitch discrimination. The study found that synchronized and continuation tapping activated left sensorimotor cortex, right cerebellum, and right STG, while only continuation tapping engaged a medial premotor network (caudal SMA, left putamen, left ventrolateral thalamus) and right IFG, indicating that precise internal timing relies on interrelated explicit timing, auditory memory, and sensorimotor systems.

Abstract

Timing is essential to the execution of skilled movements, yet our knowledge of the neural systems underlying timekeeping operations is limited. Using whole-brain functional magnetic resonance imaging, subjects were imaged while tapping with their right index finger in synchrony with tones that were separated by constant intervals [Synchronization (S)], followed by tapping without the benefit of an auditory cue [Continuation (C)]. Two control conditions followed in which subjects listened to tones and then made pitch discriminations (D). Both the S and the C conditions produced equivalent activation within the left sensorimotor cortex, the right cerebellum (dorsal dentate nucleus), and the right superior temporal gyrus (STG). Only the C condition produced activation of a medial premotor system, including the caudal supplementary motor area (SMA), the left putamen, and the left ventrolateral thalamus. The C condition also activated a region within the right inferior frontal gyrus (IFG), which is functionally interconnected with auditory cortex. Both control conditions produced bilateral activation of the STG, and the D condition also activated the rostral SMA. These results suggest that the internal generation of precisely timed movements is dependent on three interrelated neural systems, one that is involved in explicit timing (putamen, ventrolateral thalamus, SMA), one that mediates auditory sensory memory (IFG, STG), and another that is involved in sensorimotor processing (dorsal dentate nucleus, sensorimotor cortex).