Diversity and sensorimotor specialization of head direction cells in the mouse thalamus

There is increasing recognition of diversity within functionally defined classes of spatially modulated brain cells. One such functional class, the head direction (HD) cells, provides our sense of direction and is essential for spatial navigation. HD signals are routed to the cortex via the thalamus, with the highest density of HD cells found within the anterodorsal thalamic nucleus (ADn). Variability in axonal projections and in vivo firing patterns suggest the existence of distinct neuronal subpopulations in the ADn. We investigated this diversity by extracellularly recording and juxtacellularly labeling single HD cells in subregions of the ADn in awake mice. We find that in vivo firing patterns of individual HD cells are differentially modulated by light pulses, sound, and movement, indicating sensorimotor specialization. We also reveal a mediolateral gradient of calretinin (CR)-expressing (CR+) cells, with CR+ HD cells having narrower tuning widths, lower peak firing rates, and different intrinsic properties compared with CR- HD cells. We identify distinct axonal projection patterns, including HD cells innervating the thalamic reticular nucleus (TRN) and different layers of the granular retrosplenial cortex, as well as HD cells with additional collaterals in the dorsomedial striatum. We also define an unusual CR+ subpopulation, the tortuosa HD cells, which possess twisted dendrites and a descending axon that does not innervate the TRN. Together, these findings suggest that ADn HD cells comprise specific cell types that integrate multimodal streams of sensorimotor input within their receptive fields that relate to attention and arousal, thereby providing downstream targets with dynamically updated and behaviorally relevant directional information.