Hippocampal representations of distance, space, and direction and their plasticity predict navigational performance

The hippocampus is implicated in episodic memory and allocentric spatial navigation. However, spatial selectivity is insufficient to navigate; one needs information about the distance and direction to the reward on a specific journey. The nature of these representations, whether they are expressed in an episodic-like sequence, and their relationship with navigational performance are unknown. We recorded single units from dorsal CA1 of the hippocampus while rats navigated to an unmarked reward zone defined solely by distal visual cues, similar to the classic water maze. The allocentric spatial selectivity was substantially weaker than in typical real world tasks, despite excellent navigational performance. Instead, the majority of cells encoded path distance from the start of trials. Cells also encoded the rats allocentric position and head angle. Often the same cells multiplexed and encoded path distance, head direction and allocentric position in a sequence, thus encoding a journey-specific episode. The strength of neural activity and tuning strongly correlated with performance, with a temporal relationship indicating neural responses influencing behavior and vice versa. Consistent with computational models of associative Hebbian learning, neural responses showed increasing clustering and became better predictors of behaviorally relevant variables, with neurometric curves exceeding and converging to psychometric curves. These findings demonstrate that hippocampal neurons multiplex and exhibit highly plastic, task- and experience-dependent tuning to path-centric and allocentric variables to form an episode, which could mediate navigation.