Posterior dorsomedial striatum is critical for both selective instrumental and Pavlovian reward learning

The dorsal striatum (DS) has been implicated in instrumental learning but its role in the acquisition of stimulus-driven behaviour is not clear. To explore the contribution of the DS to both response-outcome (R-O) and stimulus-outcome (S-O) associative learning, we pharmacologically inactivated subregions (dorsolateral, anterior dorsomedial and posterior dorsomedial) of the DS during acquisition sessions in which subjects acquired two unique, novel R-O pairs or two unique, novel S-O pairs. To test whether specific R-O or S-O associations were learned under inactivation, rats were tested following selective-satiety devaluation of one outcome under drug-free conditions. In the instrumental task, control rats and rats with dorsolateral striatum (DLS) inactivation during learning responded less on the lever that had earned the devalued outcome than on the alternative lever at test, indicating that the DLS is not critical for the formation of R-O associations. In contrast, rats with inactivation of the medial DS (DMS) (either anterior or posterior) during learning responded indiscriminately, suggesting failure to acquire the novel R-O associations. In the Pavlovian task, both controls and rats with anterior DMS inactivation during learning responded less in the presence of the stimulus predicting the devalued outcome, whereas rats with DLS or posterior DMS inactivation during learning responded equally to the stimuli, indicating that they had not acquired the novel S-O associations. These data confirm that the DLS and anterior region DMS mediate different aspects of reward-related learning, and suggest that the posterior DMS may mediate a function common to both forms of learning (R-O and S-O). Finally, we demonstrate that both S-O and R-O associations are required for selective Pavlovian-instrumental transfer.