Spatiotemporal reorganization of electrical activity in the human brain associated with a timing transition

Abstract

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.

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.…”

Striatal Activity during Intentional Switching Depends on Pattern Stability

“…A central tenet of coordination dynamics is that switching between patterns depends upon their stability (Kelso, 1995;Swinnen, 2002;Park and Turvey, 2008), as assessed in behavioral and neuroimaging studies using quantitative measures of stability such as relaxation time, switching time, and variability (Kelso et al, 1992;Mayville et al, 1999;Daffertshofer et al, 2000;Fuchs et al, 2000a,b;Meyer-Lindenberg et al, 2002;Aramaki et al, 2006;Jantzen et al, 2009). In coordination dynamics, manipulation of key control parameters results in a loss of stability and spontaneous switching to patterns that better meet current demands.…”

The phi complex as a neuromarker of human social coordination

“…Such selforganized pattern formation in the brain is a subject of much active investigation in the neurosciences and expresses itself in various forms, including brain oscillations (e.g., refs. [40][41][42], transient phase synchrony among neural populations (30,38,(43)(44)(45)(46)(47), multistability, abrupt phase transitions (''switches'') in behaviorally induced cortical activity patterns (48)(49)(50)(51)(52)(53), and so forth. A positive contribution of coordination dynamics to understanding the brain-behavior relation is that it has been able (i) to identify key coordination or collective variables for complex patterns of behavior; and (ii) to derive patterns of collective behavior from the coupling among interacting components at both behavioral and brain levels (see refs.…”