Frontal connectivity dynamics encode contextual information during action preparation

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Abstract

The context in which we perform motor acts shapes our behavior, with movement speed and accuracy modulated by contingent factors, such as the occurrence of cues that trigger or inhibit our actions. This flexibility relies on network interactions encompassing premotor and prefrontal regions, including the supplementary motor area (SMA) and the right inferior frontal gyrus (rIFG). However, the dynamic interplay between these regions during action preparation and execution based on contextual demands remains unclear. Here, we demonstrate that contextual information is encoded in SMA and rIFG interareal connectivity before action. Using Transcranial Magnetic Stimulation (TMS) and electroencephalography (EEG) during Go/No- Go tasks with varying target probabilities, we found that, during the preparatory stages of action, α-band rIFG connectivity increased in contexts where motor responses were more frequently withheld. In contrast, SMA exhibited a reversed pattern only near the target onset. Finally, β-band connectivity encoded proactive inhibition processes, increasing when action likelihood was low. Accordingly, during response implementation, both areas exhibited greater β-band connectivity when action was withheld compared to when a motor response was required, further supporting its role in inhibitory control. Our results demonstrate that α- and β-band oscillatory network dynamics support context-sensitive adaptations, illustrating how premotor and prefrontal regions synergistically modulate their interactions as they transition from preparation to response. These findings advance understanding of how the brain integrates predictive information to dynamically organize motor and cognitive resources before an action unfolds, revealing that connectivity encodes critical information driving behavior.

Significance statement

Adaptive behavior relies on the brain’s ability to anticipate and adjust actions based on contextual cues. Using Transcranial Magnetic Stimulation and electroencephalography (TMS-EEG), we show that the supplementary motor area (SMA) and the right inferior frontal gyrus (IFG) dynamically modulate their functional connectivity based on target predictability during action preparation and initiation. We reveal distinct oscillatory mechanisms by which SMA enhances motor readiness and IFG supports inhibitory control before action execution. These findings provide new insights into how frontal networks integrate probabilistic information to optimize action outputs in predictable contexts, with implications for disorders involving deficits in motor planning and control.

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