Habit and the hippocampus: Model-based spatial representations without outcome-sensitive control

Abstract The hippocampus encodes cognitive maps that support goal-directed navigation. Hippocampal neurons can encode future states and trajectories, and disruption of the hippocampus can impair sensitivity to outcome revaluation when decisions depend on spatial or contextual memory, suggesting a link between hippocampal model-based representations and value-sensitive control. However, few studies have investigated whether hippocampal representations can support habitual, outcome-insensitive action selection. Here, we developed a two-outcome spatial navigation task in which identical turning actions (left or right) led to opposite rewards (milk or water) depending on spatial location. Separate groups of rats (16 males, 22 females) were trained under conditions that either required hippocampal-dependent discrimination between choice points or allowed hippocampal-independent performance based on visual beacons. Intrahippocampal muscimol confirmed the differential dependence of these task variants on the hippocampus. After extensive training, outcome sensitivity was assessed by water restriction, which reliably shifted preference from milk to water. When tested in extinction under water restriction, rats continued to select milk-associated responses despite the change in outcome value, indicating habitual, outcome-insensitive control. Critically, this insensitivity was observed regardless of whether task performance depended on the hippocampus. Outcome sensitivity emerged only after a fully reinforced revaluation training session, and did so independently of the original training condition. These findings demonstrate that hippocampal-dependent navigation can be governed by value-insensitive action policies, and thus show that reliance upon hippocampal representations for pathfinding is not sufficient to confer outcome-sensitive control, thereby dissociating the use of cognitive maps from value updating in navigational decision making. Significance Statement The hippocampus is widely thought to support goal-directed navigation by constructing internal models (“cognitive maps”) that enable flexible decision making. In laboratory experiments, goal-directed behavior is typically defined by sensitivity to outcome revaluation. However, we show here that the hippocampus can support outcome-insensitive (habitual) action selection during a spatial task in which identical actions lead to different rewards depending on location. Even when accurate performance required the hippocampus, rats trained on this task failed to adjust their choices after outcome revaluation. Outcome sensitivity emerged only after a fully reinforced revaluation training session. These findings dissociate reliance on hippocampal representations from value-sensitive control, demonstrating that use of a cognitive map is not sufficient to confer goal-directed behavior.