Planning requires anticipating the environmental contingencies that we will encounter and also our own future behaviour in those scenarios. The evolutionary origins of such prospective decision simulations have, however, been difficult to investigate. Moreover, in humans, these metacognitive processes are associated with a distinctively human brain region in the anterior lateral prefrontal cortex. Here we demonstrate these capacities in macaques and their neural bases in two complementary patterns of brain activity in different ventrolateral prefrontal areas: areas 45a and 47/12o. We also examine the impact of ultrasonic disruption of each area. We compare behavioural, brain activity and disruption patterns in humans and macaques. Finally, comparative connectional analysis revealed similarities between the conjunction of the two circuits associated with areas 45a and 47/12o in macaques and the human anterior lateral prefrontal area. In combination, the results suggest behavioural and anatomical origins of metacognitive processes that have become especially sophisticated in humans.