Brain networks underlying human timing behavior are influenced by prior context

Abstract

The continuation paradigm is often used to investigate the behavioral and neural mechanisms of timing. Typically, a movement rate is established by pacing with a metronome. Then, the metronome is turned off and the subject continues at the established rate. Performance during continuation is assumed to be based on internal timing mechanisms. Here, we investigated the degree to which the neural activity underlying time representation depends on the initial pacing context, that is, whether pacing was established by moving in-phase (the usual procedure) or anti-phase (syncopation) with an auditory metronome. Functional MRI was measured from 14 subjects during four conditions: synchronized pacing, synchronized continuation, syncopated pacing, and syncopated continuation. In general, movements were timed consistently for all four conditions. However, a much broader network of activation was engaged during syncopation compared with synchronization, including increased activation in supplementary motor area, left premotor area, right thalamus, bilateral inferior frontal gyrus, and cerebellum. No differences were found when comparing continuation with the preceding pacing phase except for decreased activity in auditory-related regions due to the absence of the metronome. These results demonstrate that the cortical and subcortical areas recruited to support a simple motor timing task depend crucially on the method used to establish the temporal reference. Thus, the neural mechanisms underlying time and timing are highly flexible, reflecting the context in which the timing is established.T he ability of humans to accurately maintain temporal information after the removal of external environmental cues is often exploited to investigate the neural basis of internal timing mechanisms (1). An illustrative approach first used by Stevens (2) and popularized by Wing and Kristofferson (3) is the continuation paradigm. The task consists of two stages. In the first stage (termed pacing), movements are made to coincide with an external periodic stimulus or metronome. In the second so-called continuation stage, the metronome is removed and the subject is required to maintain movement at the rate previously established during pacing. During continuation it is assumed that timing is based on internal mechanisms that use a representation of the required interval developed during pacing. When applied to patient populations, this approach has been central in identifying cerebellum and basal ganglia as putative structures mediating these temporal processes during continuation (4-6). More recent functional imaging studies employing this paradigm have identified broader networks of cortical and subcortical structures underlying timing (7,8). Although these latter studies demonstrate that pacing and continuation, in addition to imposing similar task demands, activate substantially overlapping networks, the degree to which the neural areas supporting continuation are influenced by the network of neural activity generated during pacing has not ...

Emergence of rhythm during motor learning

“…This is in line with the idea of dissociation between automatic timing processes subserved by motorrelated areas and cognitively controlled timing processes subserved by prefrontal cortex [7]. Automatic timing processes include performance of a well-learned rhythm [17], control of the acceleration and deceleration of a learned sequential hand movement [18], or synchronous tapping to the beat of a rhythm [19,20] especially as performed by professional musicians [8]. Controlled timing processes include encoding of time duration [21,22], explicit discrimination of time intervals [23], on-line adjustment of the timing of motor or cognitive action [19,24,25], or those in early phases of rhythm learning [26].…”

“…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.…”

Social coordination dynamics: Measuring human bonding

“…This notion is bolstered by evidence showing that observation of another person performing rhythmic movements generates a kinematically specific memory trace of the observed motions in primary motor cortex (Stefan, Cohen, Duque, Mazzocchio, Celnik, Sawaki, Ungerleider, & Classen, 2005). Moreover, representations at the neural level have been shown to be highly flexible and context-dependent (Jantzen, Steinberg, & Kelso, 2004;, influenced both by environmental (Wheeler, Peterson & Buckner, 2000) and task demands (Oullier, Jantzen, Steinberg, & Kelso, 2005).…”

Do We Have a Common Mechanism for Measuring Time in the Hundreds of Millisecond Range? Evidence From Multiple-Interval Timing Tasks

“…Thus the present results support the notion of a distributed system for time processing. Neurophysiological evidence for the existence of task-dependent timing processes has come from recent fMRI research, demonstrating that the specific neural structures recruited for temporal processing may be at least partially determined by the way in which timing information is presented (Jantzen et al 2004). Thus different nodes of the distributed system may change their level of participation in the network depending on nontemporal parameters such as S, N, and M. In addition, structures such as SMA and the basal ganglia could be the core of this network, participating in most of the timing contexts.…”