Construction of a hippocampal cognitive map depends upon spatial context

Abstract

The hippocampus encodes both spatial and non-spatial features of an environment thought to be critical to guide navigational trajectories and associative learning, respectively. These seemingly dichotomous roles have been reconciled in a proposed cognitive map - a representation of environment structure abstracted away from specific behavioral demands. However, the extent to which a cognitive map is independent of behavioral demands remains unclear because direct comparisons across environments with common structure but different spatial/behavioral context is lacking. Here we compare behaviors in mice trained to navigate to a hidden target in a physical arena and manipulate a joystick to a virtual target to collect a delayed reward. Comparison of behaviors with an artificial agent revealed a common algorithmic basis for learned foraging trajectories in both contexts. Imaging CA1 neural activity revealed a similar map-like encoding of active foraging; however, detailed analysis of ensemble activity, optogenetic inactivation, and modeling revealed a context-specific functional dissociation. In a navigational context, CA1 was critical for retrospective evaluation of spatial trajectories, but dispensable for initiation. In a non-navigational context, CA1 activity was critical for initiation and planning foraging trajectories. This work highlights how construction of a cognitive map to facilitate idiosyncratic behavioral demands7 is critical for foraging in diverse spatial contexts.

A neural circuit architecture for rapid behavioral flexibility in goal-directed navigation

“…When combined with optimal RL algorithms [16], this enabled us to specify how these control parameters should change based on experience. This approach bears similarities to recent studies proposing that learning operates on generative parameters that control distributions of movements, rather than on the higher-dimensional space of all possible movements [90–92]. We then used this approach to specify how these control parameters should be structured as a function of the fly’s current heading to maintain a goal heading over time.…”