Cerebellum promotes sequential foraging strategies and contributes to the directional modulation of hippocampal place cells

Cerebellum contributes to spatial coding in the hippocampus. When PKC-dependent mechanisms are impaired in cerebellar Purkinje cells, hippocampal place cells indeed lose their spatial selectivity in the dark, when the animal relies mostly on self-motion cues to navigate. This impairment in PKC-dependent cerebellar functions additionally leads to behavioral deficits in using both external and self-motion cues when learning a goal-oriented navigation task. However, it is unclear how cerebellum influences the exploration strategy used by an animal during free foraging in an open environment. Moreover, place cells are influenced by other navigational variables than positions, such as movement direction and speed. Does the cerebellum also play a role in the modulation of place cells by these other covariates? We recorded hippocampal place cells in mice with impaired PKC-dependent mechanisms (L7-PKCI) and in their littermate controls while they performed a foraging task where they could obtain a reward after visiting a subset of hidden locations. We found that L7-PKCI and control mice developed different foraging strategies: while control mice repeated reliable spatial sequences to maximize their rewards, L7-PKCI mice persisted to use a random foraging strategy. The sequence-based strategy was associated with more place cells exhibiting theta-phase precession and theta modulation. It was also correlated with a larger fraction of place cells that were modulated concomitantly by movement direction and speed. Finally, in the dark, the modulation of place cells by movement direction was markedly reduced in L7-PKCI mice, demonstrating that PKC-dependent cerebellar functions control how self-motion cues influence not only position but also direction coding in the hippocampus. Cerebellum thus contributes to developing optimal sequential paths during foraging behavior, which may reflect its impact on self-motion and theta signals contributing to place cells coding.