“What should I do next?” The answer is simple if there is one obvious choice but complicated if there are multiple options and no standout winner. The brain can deal with both scenarios, engaging circuits that drive more automatic responses in some cases and circuits that support deliberation in others. Understanding how this cognitive flexibility is implemented in the brain has the potential to reveal organizational principles for neural information processing. We have therefore carried out large-scale recordings studies in freely behaving rats performing cognitive tasks to identify signatures of dynamic circuit engagement. Here I will present results from two of these studies, including 1) observations of dynamic engagement of non-local hippocampal representations related to ongoing decision-making and 2) a demonstration of the necessity of the sequential neural activity patterns underlying non-local hippocampal representations for learning a specific task rule. These results highlight the differential engagement of hippocampal information processing at different times in support of flexible behavior.