Frontopolar Cortex Interacts With Dorsolateral Prefrontal Cortex to Causally Guide Metacognition

Accurate metacognitive judgments about an individual's performance in a mental task require the brain to have access to representations of the quality and difficulty of first-order cognitive processes. However, little is known about how accurate metacognitive judgments are implemented in the brain. Here, we combine brain stimulation with functional neuroimaging to determine the neural and psychological mechanisms underlying the frontopolar cortex's (FPC) role in metacognition. Specifically, we evaluate two-layer neural architectures positing that FPC enables metacognitive judgments by communicating with brain regions encoding first-order decision difficulty. In support of two-layer architectures of metacognition, we found that high-intensity transcranial alternating current stimulation (tACS; 4 mA peak-to-peak) over FPC impaired metacognitive accuracy; at the neural level, this impairment was reflected by reduced coupling between FPC and dorsolateral prefrontal cortex (DLPFC), particularly during difficult metacognitive judgments. We also evaluated conceptual accounts assuming that metacognition relies on self-directed mentalizing. However, we observed no influence of FPC tACS on mentalizing performance and only a weak overlap of the networks underlying metacognition and mentalizing. Together, our findings put the FPC at the center of a two-layer architecture that enables accurate evaluations of cognitive processes, mainly via the FPC's connectivity with regions encoding first-level task difficulty, with little contributions from mentalizing-related processes.