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

Abstract

Goal-directed decisions depend on predictions of future outcomes and are thus sensitive to revaluation of expected outcomes, whereas habitual decisions depend on cached action values or stimulus-response associations and are insensitive to outcome revaluation. Hippocampal neurons encode future states (potentially supporting prediction of future outcomes during goal-directed choice) as well as present states (potentially supporting retrieval of state-dependent action values during habitual choice). Prior studies suggest a role for the hippocampus in goal-directed, outcome-sensitive decision making, but few studies have examined its role in habitual, outcome-insensitive action selection. Here, we tested this using a two-outcome spatial navigation task in which identical turning actions (left or right) led either to preferred milk or non-preferred water outcomes, depending on the spatial location at which the choice was made. Rats (20 males, 22 females) were trained under conditions that either required hippocampal-dependent discrimination between choice points or allowed hippocampal-independent navigation using visual beacons. Rats then underwent 24 h water restriction during which separate cohorts underwent Contingency Updating (CU), in which rats re-experienced the maze action-outcome contingencies while thirsty, or Incentive Learning (IL), in which rats received only a two-bottle preference test while thirsty without re-experiencing maze contingencies. Both cohorts were later tested under thirst on an unbaited maze. CU rats shifted their choices toward water-associated responses, whereas IL rats perseverated on milk-associated responses, even when navigation depended on the hippocampus. These results provide novel evidence that hippocampal-dependent navigational decisions can show insensitivity to outcome revaluation, a widely-used behavioral criterion for habitual control. Significance StatementWe show here that the dorsal hippocampus can support navigational decisions that are insensitive to outcome revaluation during a spatial task in which identical actions lead to different outcomes depending on location. Even when the hippocampus was required for accurate navigation to reach a preferred outcome, rats overtrained on this task failed to adjust their choices after revaluation altered their outcome preferences. To our knowledge, these findings provide the first direct evidence that hippocampal-dependent navigation can satisfy a widely used behavioral criterion for habitual control.