Abstract
It has been proposed that compulsive drug seeking reflects an underlying dysregulation in adaptive behavior that favors habitual (automatic and inflexible) over goal-directed (deliberative and highly flexible) action selection. Rodent studies have established that repeated exposure to cocaine or amphetamine facilitates the development of habits, producing behavior that becomes unusually insensitive to a reduction in the value of its outcome. The current study more directly investigated the effects of cocaine pre-exposure on goal-directed learning and action selection using an approach that discourages habitual performance. After undergoing a 15-day series of cocaine (15 or 30 mg/kg, i.p.) or saline injections and a drug withdrawal period, rats were trained to perform two different lever-press actions for distinct reward options. During a subsequent outcome devaluation test, both cocaine- and saline-treated rats showed a robust bias in their choice between the two actions, preferring whichever action had been trained with the reward that retained its value. Thus, it appears that the tendency for repeated cocaine exposure to promote habit formation does not extend to a more complex behavioral scenario that encourages goal-directed control. To further explore this issue, we assessed how prior cocaine treatment would affect the rats’ ability to learn about a selective reduction in the predictive relationship between one of the two actions and its outcome, which is another fundamental feature of goal-directed behavior. Interestingly, we found that cocaine-treated rats showed enhanced, rather than diminished, sensitivity to this action–outcome contingency degradation manipulation. Given their mutual dependence on striatal dopamine signaling, we suggest that cocaine’s effects on habit formation and contingency learning may stem from a common adaptation in this neurochemical system.
Highlights
Recreational drug use can develop into a pathological behavior that is difficult to control or abstain from despite its many harmful consequences
While it was suggested that this phenomenon could reflect a state of DMS dysfunction, leading to impaired goal-directed control, we suggest that it may contribute to the augmented contingency degradation effect reported here
Rats pre-treated with cocaine exhibited normal sensitivity to outcome devaluation, demonstrating that they had encoded the two action–outcome relationships and Treatment
Summary
Recreational drug use can develop into a pathological behavior that is difficult to control or abstain from despite its many harmful consequences. When rodents are given extensive opportunity to self-administer cocaine, they can develop a compulsive tendency to seek out the drug even when doing so leads to physical punishment [1, 2] Some have proposed that compulsive tendencies are caused by drug-induced dysregulation of neural systems that normally mediate adaptive reward-related learning and decision-making [3,4,5,6,7,8] This hypothesis draws heavily on literature regarding animal learning, current evidence shows that humans and rodents use analogous action selection strategies when pursuing rewards [9,10,11,12,13]. Outcome devaluation tests are conducted in extinction to ensure that changes in performance are based on previously encoded action–outcome learning
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