Spatial Rule Learning and Corresponding CA1 Place Cell Reorientation Depend on Local Dopamine Release

Incentives drive goal-directed behavior; however, how they impact the formation and stabilization of goal-relevant hippocampal maps remains unknown. Since dopamine is involved in reward processing, affects hippocampal-dependent behavior, and modulates hippocampal plasticity, we hypothesized that local dopaminergic transmission in the hippocampus serves to mold the formation and updating of hippocampal cognitive maps to adaptively represent reward-predicting space of sensory inputs. We recorded CA1 place cells of rats throughout training on a spatial extra-dimensional set-shift task. After learning to rely on one of two orthogonal sets of cues, we introduced a rule shift and infused locally the D_1/5 receptor (D_1/5R) antagonist SCH23390. Successful learning was accompanied by place cell reorientation to represent rule-relevant spatial dimension. SCH23390 infusion prevented this remapping and, consequently, impaired learning, causing perseveration. These findings suggest that dopaminergic innervation provides reward information to the hippocampus and is critical for the stabilization of goal-related hippocampal representation, contributing to successful goal-directed behavior. Efficient goal-directed behavior requires processing certain aspects of the environment, ignoring others. Retailleau and Morris show that the learning of new spatial rules is mediated by local dopamine release and that intact D1 receptor function is necessary for the formation of a goal-relevant representation of space of CA1 place cells.