Activity across prefrontal cortical populations represents stimuli in a low-dimensional manifold that often undergoes transformations during the execution of cognitive tasks. These dynamics are commonly thought to be determined by whatever cognitive operation is being performed at the time, for example, rotation of stimulus representation in population activity during working memory is thought to reduce interference by subsequent distractors. The assumption that cognitive operations dictate stimulus transformations has not yet been tested experimentally. Here we show that the activity space of prefrontal neurons in naïve monkeys exhibits significant rotations, some aspects of which remain remarkably unchanged after training to perform working memory tasks. Training does induce changes in population dynamics, which further distinguish correct and error trials during task execution. Our results reveal automatic functions of prefrontal neural circuits that form the substrate of cognitive flexibility.