Differential encoding of action selection by orbitofrontal and striatal population dynamics

Survival relies on the ability to flexibly choose between different actions according to varying environmental circumstances. Many lines of evidence indicate that action selection involves signaling in corticostriatal circuits, including the orbitofrontal cortex (OFC) and dorsomedial striatum (DMS). While choice-specific responses have been found in individual neurons from both areas, it is unclear whether populations of OFC or DMS neurons are better at encoding an animal's choice. To address this, we trained head-fixed mice to perform an auditory guided two-alternative choice task, which required moving a joystick forward or backward. We then used silicon microprobes to simultaneously measure the spiking activity of OFC and DMS ensembles, allowing us to directly compare population dynamics between these areas within the same animals. Consistent with previous literature, both areas contained neurons that were selective for specific stimulus-action associations. However, analysis of concurrently recorded ensemble activity revealed that the animal's trial-by-trial behavior could be decoded more accurately from DMS dynamics. These results reveal substantial regional differences in encoding action selection, suggesting that DMS neural dynamics are more specialized than OFC at representing an animal's choice of action. NEW & NOTEWORTHY While previous literature shows that both orbitofrontal cortex (OFC) and dorsomedial striatum (DMS) represent information relevant to selecting specific actions, few studies have directly compared neural signals between these areas. Here we compared OFC and DMS dynamics in mice performing a two-alternative choice task. We found that the animal's choice could be decoded more accurately from DMS population activity. This work provides among the first evidence that OFC and DMS differentially represent information about an animal's selected action.