Hypotheses of striatal orchestration of behavior ascribe distinct functions to striatal subregions, with the dorsolateral striatum (DLS) especially implicated in habitual and skilled performance. Thus neural activity patterns recorded from the DLS, but not the dorsomedial striatum (DMS), should be correlated with habitual and automatized performance. Here, we recorded DMS and DLS neural activity in rats during training in a task promoting habitual lever pressing. Despite improving performance across sessions, clear changes in corresponding neural activity patterns were not evident in DMS or DLS during early training. Although DMS and DLS activity patterns were distinct during early training, their activity was similar following extended training. Finally, performance after extended training was not associated with DMS disengagement, as would be predicted from prior work. These results suggest that behavioral sequences may continue to engage both striatal regions long after initial acquisition, when skilled performance is consolidated.

Flexible and efficient decision-making in complex environments can be achieved through constant interactions between the goal-directed and habitual systems. While goal-directed behavior is considered dependent upon Response-Outcome (R-O) associations, habits instead rely on Stimulus-Response (S-R) associations. However, the stimuli that support the S-R association underlying habitual responding in typical instrumental procedures are poorly defined. To resolve this issue, we designed a discrete-trials procedure, in which rats must wait for lever insertion and complete a sequence of five lever presses to obtain a reward (20% sucrose or grain-based pellets). Lever insertion thus constituted an audio-visual stimulus signaling the opportunity for reward. Using sensory-specific satiety-induced devaluation, we found that rats trained with grain-based pellets remained sensitive to outcome devaluation over the course of training with this procedure whereas rats trained with a solution of 20% sucrose rapidly developed habit, and that insensitivity to outcome devaluation in rats trained with sucrose did not result from a bias in general satiety. Importantly, although rats trained with pellets were sensitive to satiety-induced devaluation, their performance was not affected by degradation of instrumental contingency and devaluation by conditioned taste aversion (CTA), suggesting that these rats may also have developed habitual responding. To test whether the discrete-trials procedure biases subjects towards habitual responding, we compared discrete-trials to free-running instrumental responding, and found that rats trained with sucrose in a fixed-ratio 5 (FR5) procedure with continuous presentation of the lever were goal-directed. Together, these results demonstrate that discrete presentations of a stimulus predictive of reward availability promoted the formation of S-R habit in rats trained with liquid sucrose. Further research is necessary to explain inconsistencies in sensitivity to outcome devaluation when rats are trained with grain-based pellets.

Ample evidence shows that the setting can control drug choices in both humans and animals. Here we reveal in rats that a major mechanism of this control involves a regulation of the drug influence on other competing options at the time of choice. Briefly, rats were offered a choice between a drug dose (cocaine or heroin) and a brief access to water sweetened with saccharin in two different settings. In one setting, choosing under the influence was not possible and rats largely preferred saccharin over either cocaine or heroin. In contrast, when the same rats were shifted to a setting where choosing under the influence was possible, they chose the drug either nonexclusively or exclusively depending on whether the drug enhanced or suppressed sweet reward, respectively. Thus, when rats were under the orexigenic influence of heroin at the time of choice, they more frequently chose saccharin in alternation with heroin. In contrast, when rats were under the anorexic influence of cocaine, they stopped choosing saccharin and continued taking cocaine exclusively. These settingand drug-specific changes in preference were rapid and reversible, and could be induced by passively administering cocaine or heroin before choice. Finally, rats behaved as if they were oblivious to the drug influence on their choices. This behavior could explain why rats are vulnerable to harm themselves, sometimes to the point of death, in settings where choices are made under the drug influence, notably if this influence excludes other important options or, conversely, enhances harmful ones.