A hippocampo-cortical pathway detects changes in the validity of an action as a predictor of reward

Much research has been dedicated to understanding the psychological and neural bases of goal-directed action, yet the relationship between context and goal-directed action is not well understood. Here, we used excitotoxic lesions, chemogenetics, and circuit-specific manipulations to demonstrate the role of the ventral hippocampus (vHPC) in contextual learning that supports sensitivity to action-outcome contingencies, a hallmark of goal-directed action. We found that chemogenetic inhibition of the ventral, but not dorsal, hippocampus attenuated sensitivity to instrumental contingency degradation. We then tested the hypothesis that this deficit was due to an inability to discern the relative validity of the action compared with the context as a predictor of reward. Using latent inhibition and Pavlovian context conditioning, we confirm that degradation of action-outcome contingencies relies on intact context-outcome learning and show that this learning is dependent on vHPC. Finally, we show that chemogenetic inhibition of vHPC terminals in the medial prefrontal cortex also impairs both instrumental contingency degradation and context-outcome learning. These results implicate a hippocampo-cortical pathway in adapting to changes in instrumental contingencies and indicate that the psychological basis of this deficit is an inability to learn the predictive value of the context. Our findings contribute to a broader understanding of the neural bases of goal-directed action and its contextual regulation.