Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions

TLDR

Shifting between goal‑directed and habitual actions allows for efficient and flexible decision making, and prior work shows that the orbital frontal cortex and dorsal medial striatum are necessary for goal‑directed actions while the dorsal lateral striatum is necessary for habitual actions. The study demonstrates a novel within‑subject instrumental lever‑pressing paradigm in which mice shift between goal‑directed and habitual actions. The paradigm uses a within‑subject instrumental lever‑pressing task that allows mice to transition between goal‑directed and habitual actions within the same session. Neuronal recordings and causal manipulations reveal that the orbitofrontal cortex drives goal‑directed behavior, with its activity increasing during outcome revaluation and correlating with goal‑directed pressing, while the dorsal medial and lateral striatum support goal‑directed and habitual actions respectively, and optogenetic activation of OFC enhances goal‑directed pressing whereas its inhibition impairs it, highlighting corticostriatal interactions underlying the shift between habit and goal‑directed actions.

Abstract

Shifting between goal-directed and habitual actions allows for efficient and flexible decision making. Here we demonstrate a novel, within-subject instrumental lever-pressing paradigm, in which mice shift between goal-directed and habitual actions. We identify a role for orbitofrontal cortex (OFC) in actions following outcome revaluation, and confirm that dorsal medial (DMS) and lateral striatum (DLS) mediate different action strategies. Simultaneous in vivo recordings of OFC, DMS and DLS neuronal ensembles during shifting reveal that the same neurons display different activities depending on whether presses are goal-directed or habitual, with DMS and OFC becoming more and DLS less engaged during goal-directed actions. Importantly, the magnitude of neural activity changes in OFC following changes in outcome value positively correlates with the level of goal-directed behavior. Chemogenetic inhibition of OFC disrupts goal-directed actions, whereas optogenetic activation of OFC specifically increases goal-directed pressing. These results also reveal a role for OFC in action revaluation, which has implications for understanding compulsive behavior. Interactions between corticostriatal circuits are implicated in the shifts between habit- and goal-directed actions. Gremel and Costa show that the orbital frontal cortex and the dorsal medial striatum are necessary for goal-directed actions, whereas the dorsal lateral striatum is necessary for habitual actions.