Sofia Skromne Carrasco

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 days^{4,5,6,7,8,9,10,11}—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.

The generation of the head-direction (HD) signal, a cornerstone of the brain’s navigation system, is classically attributed to the lateral mammillary nucleus (LMN) and associated brainstem structures, where attractor-like dynamics are thought to maintain population coherence. Here, using multi-site recordings and optogenetic perturbations along the mammillary–thalamic–cortical pathway, we demonstrate that HD neurons in the anterodorsal nucleus of the thalamus (ADN) maintain coherent population dynamics even when their LMN inputs become decorrelated during non-REM sleep. These findings reveal that thalamic coherence does not strictly depend on structured input from the LMN; instead, it can emerge from local thalamic processes involving shared inhibition and non-linear responses. Together, our findings reveal a previously unrecognized, state-dependent shift in the circuit organizing the HD signal, establishing the thalamus as an active substrate capable of independently sustaining internal representations across brain states.

Animals use visual objects to guide navigation-related behaviors. However, visual object–preferring areas have yet to be described in the mouse brain, limiting our understanding of how visual objects affect spatial navigation system processing. Using functional ultrasound imaging, we identified brain areas that were preferentially activated by images of objects compared with their scrambled versions. Whereas visual cortex did not show a preference, areas associated with spatial navigation were preferentially activated by visual objects. Electrophysiological recordings in postsubiculum, the cortical head direction (HD) system hub, confirmed a preference for visual objects in both HD cells and fast-spiking interneurons. In freely moving animals, visual objects increased firing rates of HD cells aligned with a visual object but decreased activity in HD cells coding for other directions.

Animals use visual objects to guide navigation-related behaviors, from hunting prey, to escaping predators, to exploring the world. However, little is known about where visual objects are encoded in the mouse brain or how they impact processing in the spatial navigation system. Using functional ultrasound imaging in mice, we conducted a brain-wide screen and identified brain areas that were preferentially activated by images of objects compared to scrambled versions of the same images. While visual cortical areas did not show a significant preference, regions associated with spatial navigation were preferentially activated by visual objects. Electrophysiological recordings in postsubiculum, the primary cortical area of the head direction (HD) system, further confirmed a preference for visual objects, which was present in both HD cells and fast-spiking interneurons. Finally, we found that visual objects dynamically modulated HD cells, selectively increasing firing rates of HD cells aligned with a visual landmark’s direction, while decreasing activity in HD cells coding for other directions. These results reveal that visual objects refine population-level coding of head direction.

Spatial orientation is a universal ability that allows animals to navigate their environment. In mammals, the head-direction (HD) system is an essential component of the brain’s navigation system, yet the stability of its underlying neuronal code remains unclear. Here, by longitudinally tracking the activity of the same HD cells in freely moving mice, we show that the internal organization of population activity in the HD system was preserved for several months. Furthermore, the HD system developed a unique mapping between its internal organization and spatial orientation in each environment. This was not affected by visits to other environments and was stabilized with experience. These findings demonstrate that stable neuronal code supports the sense of direction and forms long-lasting orientation memories.