Distinct corticostriatal compartments drive competition between adaptive and automatized behavior

Abstract

AbstractCortical and basal ganglia circuits play a crucial role in the formation of goal-directed and habitual behaviors. In this study, we investigate the cortico-striatal circuitry involved in learning and how cortical interactions with specific striatal subregions are involved in the emergence of inflexible behaviors such those observed in addiction. Specifically, we develop a computational model of cortico-striatal interactions that performs concurrent goal-directed and stimulus-response learning. The model accomplishes this by distinguishing learning processes in the dorsomedial striatum (DMS) that rely on reward prediction error signals as distinct from the dorsolateral striatum (DLS) where learning is supported by salience signals. These striatal subregions each operate on unique cortical input: the DMS receives input from the prefrontal cortex (PFC), which represented outcomes and the DLS receives input from the premotor cortex which determined action selection. Following an initial learning of a two-alternative forced choice task, we subjected the model to reversal learning, reward devaluation, and punishment learning. Behavior driven by stimulus-response associations in the DLS resisted goal-directed learning of new reward feedback rules despite devaluation or punishment, indicating the expression of habit. We repeated these simulations after the loss of executive control, which was implemented as poor outcome representation in the PFC. Following this manipulation, no detectable effect of reward devaluation was observed, however, the efficacy of goal-directed learning was reduced, and stimulus response associations in the DLS were even more resistant to the learning of new reward feedback rules. In summary, this model describes how impaired coding in PFC reflects the loss of executive control thus leading to the emergence of inflexible behavior.Graphical Abstract