Distinct cortico-striatal compartments drive competition between adaptive and automatized behavior

Abstract

Pathology in neural circuits that control the expression of goal-directed and habitual behaviors is hypothesized to be a major contributing factor to addiction. In this study, we investigate cortico-striatal circuitry involved in learning and how cortical interactions with specific striatal subregions are involved in the emergence of inflexible behaviors such as compulsive drinking. Specifically, we develop a computational model of cortico-striatal interactions that performs concurrent goal directed and stimulus-response learning. The model accomplishes learning by distinguishing between the dorsomedial striatum (DMS)-where dopamine release encodes reward prediction error-and the dorsolateral striatum (DLS)-where dopamine release encodes motivation or salience. 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 determines 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 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 provides a mechanism that describes how the loss of executive control could contribute to the emergence of inflexible behavior.