Neuronal correlates of metacognition in primate frontal cortex

We spend a large portion of life as the object of our own thoughts. Daily we reflect on all sorts of recent and not so recent decisions, and the products of those reflective thoughts serve to guide future goals, actions, and thoughts. The process of "thinking about thinking", or metacognition, has garnered scrutiny in psychology studies for decades and recently in some imaging and neurological studies, but its neuronal basis remains unknown. Moreover, metacognition is largely thought a uniquely human ability, and only very recently has some evidence suggested other species may harbor metacognitive skills. To begin investigating neuronal mechanisms underlying metacognition, we performed two experiments.First, we tested whether rhesus macaques exhibited evidence for metacognition. We trained monkeys to perform a visual oculomotor metacognition task. In each trial, monkeys made a decision then made a bet. To earn maximum reward, monkeys had to monitor their decision and then make a bet to indicate whether the decision was correct or incorrect. We found the monkeys' behavior was best explained by a metacognitive strategy, and we ruled out possible alternative strategies to perform the task such as reliance on visual stimuli or saccadic reaction times.Second, we tested whether neurons exhibited activity correlated with metacognition. While monkeys performed the task we recorded from single neurons in three frontal cortical areas known to play roles in higher cognitive functions: the frontal eye field, lateral prefrontal cortex, and the supplementary eye field. Our predictions were that frontal eye field neuronal activity would correlate with making the decisions but not the bets, and that lateral prefrontal cortex and supplementary eye field neuronal activity would correlate with linking the decisions to the bets - the putative metacognitive signals. We found signals in all three brain areas correlated with making decisions and correlated with making bets. The supplementary eye field was the only area of the three that exhibited strong signals correlated with metacognitive monitoring, and these signals appeared early and were sustained throughout the task. Our results identify the supplementary eye field as a likely contributor to metacognitive monitoring