Theta phase mediates deliberate action switching in human Supplementary Motor Areas

The ability to deliberately overwrite ongoing automatic actions is a necessary feature of adaptive behavior. It has been proposed that the supplementary motor areas (SMAs) operate as a controller that orchestrates the switching between automatic and deliberate processes by inhibiting ongoing behaviors and so facilitating the execution of alternative ones. In addition, previous studies support the involvement of SMAs theta waves (4-9 Hz) in cognitive control. However, the exact role of such oscillatory dynamics and their contribution to the control of action are not fully understood. To investigate the mechanisms by which the SMAs support direct control of deliberate behavior, we recorded intracranial electroencephalography (iEEG) activity in humans performing a motor sequence task. Subjects had to perform a "change of plans" motor task requiring habitual movements to be overwritten at unpredictable moments. We found that SMAs were exclusively active during trials that demand action reprogramming in response to the unexpected cue but were silent during automatic action execution. Importantly, SMAs activity was characterized by a distinct temporal pattern, expressed in a stereotypical phase alignment of theta oscillations. More specifically, single trial motor performance was correlated with the trial contribution to the global inter-trial phase coherence, with higher coherence associated with faster trials. In addition, theta phase modulated the amplitude of gamma oscillations, with higher cross-frequency coupling in faster trials. Our results suggest that within frontal cortical networks, theta oscillations could encode a control signal that promotes the execution of deliberate actions.