Emotional Context Sculpts Action Goal Representations in the Lateral Frontal Pole

Abstract

Emotional states provide an ever-present source of contextual information that should inform behavioral goals. Despite the ubiquity of emotional signals in our environment, the neural mechanisms underlying their influence on goal-directed action remains unclear. Prior work suggests that the lateral frontal pole (FPl) is uniquely positioned to integrate affective information into cognitive control representations. We used pattern similarity analysis to examine the content of representations in FPl and interconnected mid-lateral prefrontal and amygdala circuitry. Healthy participants (n = 37; n = 21 females) were scanned while undergoing an event-related Affective Go/No-Go task, which requires goal-oriented action selection during emotional processing. We found that FPl contained conjunctive emotion–action goal representations that were related to successful cognitive control during emotional processing. These representations differed from conjunctive emotion–action goal representations found in the basolateral amygdala. While robust action goal representations were present in mid-lateral prefrontal cortex, they were not modulated by emotional valence. Finally, converging results from functional connectivity and multivoxel pattern analyses indicated that FPl emotional valence signals likely originated from interconnected subgenual anterior cingulate cortex (ACC) (BA25), which was in turn functionally coupled with the amygdala. Thus, our results identify a key pathway by which internal emotional states influence goal-directed behavior.

SIGNIFICANCE STATEMENT Optimal functioning in everyday life requires behavioral regulation that flexibly adapts to dynamically changing emotional states. However, precisely how emotional states influence goal-directed action remains unclear. Unveiling the neural architecture that supports emotion–goal integration is critical for our understanding of disorders such as psychopathy, which is characterized by deficits in incorporating emotional cues into goals, as well as mood and anxiety disorders, which are characterized by impaired goal-based emotion regulation. Our study identifies a key circuit through which emotional states influence goal-directed behavior. This circuitry comprised the lateral frontal pole (FPl), which represented integrated emotion–goal information, as well as interconnected amygdala and subgenual ACC, which conveyed emotional signals to FPl.