No abstract

SUMMARYHead direction (HD) cells, key neuronal elements in the mammalian’s navigation system, are hypothesized to act as a continuous attractor network, in which temporal coordination between cell members is maintained under different brain states or external sensory conditions, resembling a unitary neural representation of direction. Whether and how multiple identified HD signals in anatomically separate HD cell structures are part of a single and unique attractor network is currently unknown. By manipulating the cerebellum, we identified pairs of thalamic and retrosplenial HD cells that lose their temporal coordination in the absence of external sensory drive, while the neuronal coordination within each of these brain regions remained intact. Further, we show that distinct cerebellar mechanisms are involved in the stability of direction representation depending on external sensory conditions. These results put forward a new role for the cerebellum in mediating stable and coordinated HD neuronal activity toward a unitary thalamocortical representation of direction.

The head-direction (HD) system, a key neural circuit for navigation, consists of several anatomical structures containing neurons selective to the animal’s head direction. HD cells exhibit ubiquitous temporal coordination across brain regions, independently of the animal’s behavioral state or sensory inputs. Such temporal coordination mediates a single, stable, and persistent HD signal, which is essential for intact orientation. However, the mechanistic processes behind the temporal organization of HD cells are unknown. By manipulating the cerebellum, we identify pairs of HD cells recorded from two brain structures (anterodorsal thalamus and retrosplenial cortex) that lose their temporal coordination, specifically during the removal of the external sensory inputs. Further, we identify distinct cerebellar mechanisms that participate in the spatial stability of the HD signal depending on sensory signals. We show that while cerebellar protein phosphatase 2B-dependent mechanisms facilitate the anchoring of the HD signal on the external cues, the cerebellar protein kinase C-dependent mechanisms are required for the stability of the HD signal by self-motion cues. These results indicate that the cerebellum contributes to the preservation of a single and stable sense of direction.