Environment-dependent firing in rigidly organized head-direction cells is stable across weeks

Primary sensory cortical areas are characterized by low-level representations of sensory inputs, but whether these representations are stable over a long period of time or whether they are continuously renewed is still unclear. The head-direction (HD) signal is essential for the spatial navigation system. In the cortex, it is processed by the postsubiculum (PoSub). HD cells each fire for a specific direction of the head of the animal in the horizontal plane and constitute a vast majority of PoSub principal neurons. To address the question of representational stability, we used one-photon calcium imaging with portable microscopes (‘miniscopes’) to longitudinally monitor ensembles of HD cells in the PoSub over periods of weeks in freely moving animals visiting several different environments. In the PoSub, the representation of the HD signal was stable at two levels. First, the pairwise offset between HD neurons was preserved for several months, indicating that the subcortical representation of the HD signal is certainly itself stable and that thalamocortical integration is rigid. Second, the orientation of the HD signal at the population level was maintained in a given environment over the same period of time, suggesting that the HD system preserves long-term memories of spatial orientation in different environments. Furthermore, HD neurons in the PoSub participated differently in the HD signal across environments, resulting in environment-specific coding of head direction. Together, these findings shed light on how spatial information is represented over time in the brain’s navigation system.