Midfrontal theta tracks action monitoring over multiple interactive time scales

Quickly detecting and correcting mistakes is a crucial brain function. EEG studies have identified an idiosyncratic electrophysiological signature of online error correction, termed midfrontal theta. Midfrontal theta has so far been investigated over the fast time-scale of a few hundred milliseconds. But several aspects of behavior and brain activity unfold over multiple time scales, displaying “scale-free” dynamics that have been linked to criticality and optimal flexibility when responding to changing environmental demands. Here we used a novel line-tracking task to demonstrate that midfrontal theta is a transient yet non-phase-locked response that is modulated by task performance over at least three time scales: a few hundred milliseconds at the onset of a mistake, task performance over a fixed window of the previous 5 s, and scale-free-like fluctuations over many tens of seconds. These findings provide novel evidence for a role of midfrontal theta in online behavioral adaptation, and suggest new approaches for linking EEG signatures of human executive functioning to its neurobiological underpinnings.