Neural networks underlying the metacognitive uncertainty response

Humans monitor states of uncertainty that can guide decision-making. These uncertain states are evident behaviorally when humans decline to make a categorization response. Such behavioral uncertainty responses (URs) have also defined the search for metacognition in animals. While a plethora of neuroimaging studies have focused on uncertainty, the brain systems supporting a volitional strategy shift under uncertainty have not been distinguished from those observed in making introspective post-hoc reports of categorization uncertainty. Using rapid event-related fMRI, we demonstrate that the neural activity patterns elicited by humans' URs are qualitatively different from those recruited by associative processes during categorization. Participants performed a one-dimensional perceptual-categorization task in which an uncertainty-response option let them decline to make a categorization response. Uncertainty responding activated a distributed network including prefrontal cortex (PFC), anterior and posterior cingulate cortex (ACC, PCC), anterior insula, and posterior parietal areas; importantly, these regions were distinct from those whose activity was modulated by task difficulty. Generally, our results can be characterized as a large-scale cognitive control network including recently evolved brain regions such as the anterior dorsolateral and medial PFC. A metacognitive theory would view the UR as a deliberate behavioral adjustment rather than just a learned middle category response, and predicts this pattern of results. These neuroimaging results bolster previous behavioral findings, which suggested that different cognitive processes underlie responses due to associative learning versus the declaration of uncertainty. We conclude that the UR represents an elemental behavioral index of metacognition.