Mice identify subgoal locations through an action-driven mapping process

Mammals instinctively explore and form mental maps of their spatial environments. Models of cognitive mapping in neuroscience mostly depict map-learning as a process of random or biased diffusion. In practice, however, animals explore spaces using structured, purposeful, sensory-guided actions. Here we test the hypothesis that executing specific exploratory actions is a key strategy for building a cognitive map. Previous work has shown that in arenas with obstacles and a shelter, mice spontaneously learn efficient multi-step escape routes by memorizing allocentric subgoal locations. We thus used threat-evoked escape to probe the relationship between ethological exploratory behavior and allocentric spatial memory. Using closed-loop neural manipulations to interrupt running movements during exploration, we found that blocking runs targeting an obstacle edge abolished subgoal learning. In contrast, blocking other movements while sparing edge-directed runs had no effect on memorizing subgoals. Finally, spatial analyses suggest that the decision to use a subgoal during escape takes into account the mouse’s starting position relative to the layout of the environment. We conclude that mice use an action-driven learning process to identify subgoals and that these subgoals are then integrated into a map-based planning process. We suggest a conceptual framework for spatial learning that is compatible with the successor representation from reinforcement learning and sensorimotor enactivism from cognitive science.