Integrated Representations of Threat and Controllability in the Lateral Frontal Pole

Abstract

Emotional processing is ubiquitous in everyday life, informing goal pursuit not only in response to current demands, but also in anticipation of future outcomes. Lateral prefrontal (LPFC) function supports cognitive control, and emerging evidence suggests a unique role for its anterior-most region--the lateral frontal pole (FPl)--in integrating putatively amygdala-originated emotion signals with goal information. However, whether these organizational properties of LPFC are expressed during the anticipation of future threat remains unknown. Here, we used FIR modeling and pattern similarity analysis to examine dynamic engagement and representational properties of distinct LPFC regions during threat anticipation requiring goal-directed action. Healthy participants (n=67) were scanned during a threat-of-shock paradigm consisting of a prolonged (18s) countdown to possible shock administration. Threat unpleasantness and controllability were manipulated orthogonally: in controllable trials, participants could avoid an unpleasant or mild shock by making a successful time-sensitive response; in uncontrollable trials, shocks were administered regardless of performance. LPFC robustly coded for anticipated threat unpleasantness, with FPl showing the strongest modulation by threat unpleasantness and controllability relative to caudal and mid-LPFC regions. Caudal and mid-LPFC maintained independent representations of threat unpleasantness and controllability. In contrast, FPl held conjunctive threat-and-controllability representations, which were associated with successful motor performance following anticipation of unpleasant shocks. Stronger conjunctive FPl representations were also associated with greater inverse amygdala-FPl coupling. Together, these findings provide insight into LPFC organization under naturalistic emotional challenges and highlight a key role for FPl in integrating affective and control-related information during threat anticipation to support goal-directed action. Significance StatementAnticipating emotionally-charged events--such as a painful outcome we may or may not be able to avoid--requires integrating emotion and control to guide behavior. However, the neural mechanisms through which emotional states influence goal-directed behavior in naturalistic, anticipatory emotional contexts remain unclear. Using a threat-of-shock paradigm and multivariate analyses we show that the anterior-most region of the lateral prefrontal cortex (LPFC)--the lateral frontal pole (FPl)--uniquely integrates information about the emotional unpleasantness and controllability of a future event, and that the strength of this integrated signal predicts better behavioral performance. These findings extend models of LPFC function to naturalistic, emotional contexts, and highlight the FPl as a key node for translating emotional and behavioral-control information into adaptive action.