Spatial orientation enables animals to navigate their environment by rapidly mapping the external world and remembering key locations1. In mammals, the head-direction (HD) system is an essential component of the navigation system of the brain2. Although the tuning of neurons in other areas of this system is unstable—evidenced, for example, by the change in the spatial tuning of hippocampal place cells3 across days4–11—the stability of the neuronal code that underlies the sense of direction remains unclear. Here, by longitudinally tracking the activity of the same HD cells in the post-subiculum of freely moving mice, we show stability and plasticity at two levels. Although the population structure remained highly conserved across environments and over time, subtle shifts in population coherence encoded environment identity. In addition, the HD system established a distinct, environment-specific alignment between its internal representation and external landmarks, which persisted for weeks, even after a single exposure. These findings suggest that the HD system forms long-lasting orientation memories that are anchored to specific environments.
