Human neuroimaging has revealed the anatomical correlates of remembering past experiences and weighing decisions. Notably, these same regions, including the hippocampus, parietal midline, and medial prefrontal cortex, have shown robust patterns of activity independent of any external stimuli, a network known as the default mode network (DMN). Consequently, it is thought that DMN fluctuations during passive epochs might relate to visualizing past experience and mental simulation. I’ll present two studies that provide converging evidence supporting this idea. In the first study, we examine fMRI datasets from anesthetized monkeys with simultaneous hippocampal electrophysiology recordings, to determine whether spontaneous neural events, such as ripples, influence specific resting-state networks. Second, I’ll present fMRI results that capture the neural computations enabling humans to rapidly simulate the outcome of sequential choices, with little or no learning. I’ll then conclude by discussing future directions for mechanistically examining the neurophysiology behind internally guided behaviours like mental simulation.