Behavioral Relevance Coding in Human Area 46 Precedes Selective Motor Activation to Action Targets

Abstract

The lateral prefrontal cortex (LPFC) actively contributes to the adaptive control of goal-directed behavior. Evidence suggests that the LPFC encodes the behavioral relevance of stimuli, distinguishing action targets from irrelevant objects; however, how this selectivity emerges over time and integrates within large-scale cortical dynamics underlying action preparation remains unclear. We recorded stereo-electroencephalography (sEEG) activity from 43 patients affected by drug-resistant epilepsy while they prepared to grasp an object and compared it with passive observation of the same object. Gamma-band responses were used to characterize cortical responsiveness and to track the spatiotemporal propagation of activity during action preparation. Neural activity first emerged in the occipitotemporal cortex in both experimental conditions and then progressed along two parallel pathways: an intraparietal and a prefrontal one. The intraparietal pathway showed highly similar dynamics during both action preparation and passive observation, suggesting largely intention-independent visuospatial processing. In contrast, the prefrontal pathway exhibited progressively stronger selectivity for behaviorally relevant objects as activity advanced rostrally. Within this pathway, area 46 exhibited sustained responses selectively associated with action-relevant objects, preceding the similarly selective engagement of premotor and motor regions. Overall, our findings identify area 46 as a key node in whole-brain dynamics that orchestrates action preparation by integrating object relevance into executive control signals guiding premotor and motor engagement. NEW & NOTEWORTHYFilling a critical gap in system-level accounts of LPFC function, whole-brain recordings reveal that area 46 selectively codes object-related information relevant for action and gates motor region activity only when the object represents a true action target.