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 D1/5 receptor (D1/5R) antagonist SCH23390. Successful learning was accompanied by place cell reorientation to represent rule-relevant spatial dimension. SCH23390 infusion prevented this re-mapping 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.