Expectancy-related changes in firing of dopamine neurons depend on hippocampus

Zhewei Zhang, Yuji K. Takahashi, Marlian Montesinos-Cartegena, Thorsten Kahnt, Angela J. Langdon, Geoffrey Schoenbaum

Abstract: The orbitofrontal cortex (OFC) and hippocampus (HC) both contribute to the cognitive maps that support flexible behavior. Previously, we used the dopamine neurons to measure the functional role of OFC. We recorded midbrain dopamine neurons as rats performed an odor-based choice task, in which expected rewards were manipulated across blocks. We found that ipsilateral OFC lesions degraded dopaminergic prediction errors, consistent with reduced resolution of the task states. Here we have repeated this experiment in male rats with ipsilateral HC lesions. The results show HC also shapes the task states, however unlike OFC, which provides information local to the trial, the HC is necessary for estimating upper-level hidden states that distinguish blocks. The results contrast the roles of the OFC and HC in cognitive mapping and suggest that the dopamine neurons access rich information from distributed regions regarding the environment’s structure, potentially enabling this teaching signal to support complex behaviors. The role of the hippocampus in shaping dopaminergic prediction errors is unclear. Here, the authors show that without a functional hippocampus, dopaminergic neurons fail to properly encode prediction errors, particularly during changes in upper-level states.

External IDs:doi:10.1038/s41467-024-53308-z