18668682 - 2005 Nature Publishing Group...

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NATURE NEUROSCIENCE VOLUME 8 | NUMBER 11 | NOVEMBER 2005 1481 REVIEW N E U RO B I O LO G Y O F A D D I C T I O N Neural systems of reinforcement for drug addiction: from actions to habits to compulsion Barry J Everitt & Trevor W Robbins Drug addiction is increasingly viewed as the endpoint of a series of transitions from initial drug use—when a drug is voluntarily taken because it has reinforcing, often hedonic, effects—through loss of control over this behavior, such that it becomes habitual and ultimately compulsive. Here we discuss evidence that these transitions depend on interactions between pavlovian and instrumental learning processes. We hypothesize that the change from voluntary drug use to more habitual and compulsive drug use represents a transition at the neural level from prefrontal cortical to striatal control over drug seeking and drug taking behavior as well as a progression from ventral to more dorsal domains of the striatum, involving its dopaminergic innervation. These neural transitions may themselves depend on the neuroplasticity in both cortical and striatal structures that is induced by chronic self-administration of drugs. The nucleus accumbens is well known to mediate the reinforcing effects of drugs, but more recent research emphasizes the role of the striatum as a whole, including the shell and core components of the nucleus accumbens, in the processes leading first to drug abuse and then to addiction. This view has been stimulated by progress in understanding the dopamine-dependent, serial communication between the various domains of the striatum via a cascading loop interconnectivity 1 , and by an improved understanding of associative learning mechanisms that conceive of behavioral output as an interaction between pavlovian and instrumental learning processes 2,3 . In particular, the description of two processes that seem to function partly in parallel, but with the second eventually dominating behavioral output, has led to the concepts of action-outcome and stimulus-response (‘habit’) learning. Here we elaborate the hypothesis that these behavioral processes can be mapped onto the parallel and serial, dynamic functioning of corticostriatal cir- cuitry ( Fig. 1 ) to mediate the ‘switches’ 4,5 between drug reinforcement, drug abuse and drug addiction. Reinforcement, conditioning and the nucleus accumbens The reinforcing effects of addictive drugs are multidimensional ( Box 1 ). Drugs act as ‘instrumental reinforcers’—that is, they increase the likelihood of responses that produce them, resulting in drug self- administration or ‘drug taking’ (defined in Box 2 ). Environmental stimuli that are closely associated in time and space with the effects of self-administered drugs gain incentive salience through the process of pavlovian conditioning ( Box 2 ). Drugs produce subjective or ‘discriminative’ effects, which include the sensing of autonomic activity (‘feelings’) or distortions in sensory processing. Stimulant drugs such
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