The head-direction (HD) circuit, an upstream provider of orientation signals for navigation, maintains coherent internal orientation memory that stays stable within each environment for weeks. During non-REM sleep, when hippocampal trajectories are replayed for memory formation, HD cells remain coordinated and directly influence this hippocampal replay. This suggests the HD system conveys a “virtual” orientation signal to support memory replay, with the thalamus appearing to play a crucial role in generating it. Overall, the HD system supplies the hippocampus and associated structures with a coherent, possibly lifelong-stable signal maintained across brain states to support spatial navigation and memory formation.