Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning

Abstract

Habits are controlled by antecedent stimuli rather than by goal expectancy. Interval schedules of feedback have been shown to generate habits, as revealed by the insensitivity of behaviour acquired under this schedule to outcome devaluation treatments. Two experiments were conducted to assess the role of the dorsolateral striatum in habit learning. In Experiment 1, sham operated controls and rats with dorsolateral striatum lesions were trained to press a lever for sucrose under interval schedules. After training, the sucrose was devalued by inducing taste aversion to it using lithium chloride, whereas saline injections were given to the controls. Only rats given the devaluation treatment reduced their consumption of sucrose and this reduction was similar in both the sham and the lesioned groups. All rats were then returned to the instrumental chamber for an extinction test, in which the lever was extended but no sucrose was delivered. In contrast to sham operated controls, rats with dorsolateral striatum lesions refrained from pressing the lever if the outcome was devalued. To assess the specificity of the role of dorsolateral striatum in this effect a second experiment was conducted in which a group with lesions of dorsomedial striatum was added. In relation now to both the sham and the dorsomedial lesioned groups, only rats with lesions of dorsolateral striatum significantly reduced responding after outcome devaluation. In conclusion, this study provides direct evidence that the dorsolateral striatum is necessary for habit formation. Furthermore, it suggests that, when the habit system is disrupted, control over instrumental performance reverts to the system controlling the performance of goal-directed instrumental actions.

The role of learning-related dopamine signals in addiction vulnerability

“…By arguing that goal-trackers are indeed more goal-directed, this suggests the involvement of goaldirected neural structures (Yin et al, 2004(Yin et al, , 2005O'Doherty et al, 2004;Killcross and Coutureau, 2003). In agreement, goal-trackers do seem to recruit cortical "top-down" regulation of their response to reward-cues (Flagel et al, 2011a).…”

Moment-to-moment dynamics of ADHD behaviour

“…Habit learning is characterized by a transition from response-consequence associations that are flexible and sensitive to reinforcement devaluation, to stimulus-response associations that are less flexible and sensitive (e.g. [20]). Thus, the initial part of habit learning may mainly involve activity in the mesolimbic dopaminergic branch, while the established habit and the skilled execution of the motor sequence may mainly involve the nigrostriatal dopaminergic branch.…”

“…It may be argued that the present study is mainly concerned with acquisition, since the task was new and relatively short. On the other hand, animal model studies have indicated that operant learning rapidly become habitual when the contingency between the response and reinforcer is weakened by using interval schedules [20], as used in the present study. Hence, it might be speculated that the control group rapidly developed a habit, while this process was hampered in the ADHD group.…”

Adenosine Signaling in Striatal Circuits and Alcohol Use Disorders

“…Recent studies have investigated the contribution of adenosine signaling in sub-regions of the dorsal striatum, the dorsomedial striatum (DMS; equivalent to caudate nucleus) and the dorsolateral striatum (DLS; equivalent to putamen) to habitual-seeking behaviors. Notably, the DMS primarily regulates goal-directed (action-outcome) behavior, which is sensitive to outcome devaluation and instrumental learning, whereas the DLS is more involved in habit (stimulus-response) formation (Yin and Knowlton, 2006;Yin et al, 2004;Yu et al, 2009). Since ethanol appears to impair several striatal functions including reward evaluation, motor function and habit formation (Corbit et al, 2012), the behavioral associations of adenosine signaling in habit formation have been examined.…”

“…Recent studies demonstrate that two different dorsal striatum regions, the dorsomedial striatum (DMS) and dorsolateral striatum (DLS), play distinctive roles in behavior development (Yin and Knowlton, 2006;Yin et al, 2007;. Notably, the DMS primarily regulates goal directed (action-outcome) behavior, which is sensitive to outcome devaluation and instrumental learning, whereas the DLS is involved in habit formation (stimulus-response) Graybiel, 2008;Yin et al, 2004). The DMS (analogous to the caudate) is a part of the associative network, which is involved in 'working memory' and the anticipation of reward.…”