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The Journal of Neuroscience, December 3, 2003, 23(35):11214-11223

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Behavioral/Systems/Cognitive
Selective Encoding of Cocaine versus Natural Rewards by Nucleus Accumbens Neurons Is Not Related to Chronic Drug Exposure

Regina M. Carelli and Joyce Wondolowski

Department of Psychology, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-3270

We reported previously that subsets of nucleus accumbens (Acb) neurons differentially encode information about goal-directed behaviors for "natural" (food and water) versus cocaine reward in animals well trained to self-administer the drug (Carelli et al., 2000). Here, we examined whether repeated exposure to cocaine is the crucial determinate of the selective encoding of cocaine versus water reinforcement by Acb neurons. Acb cells were recorded during a water-cocaine multiple schedule from the first day of cocaine exposure as well as during repeated sessions. Specifically, animals were initially trained to press a lever for water and were then surgically prepared for extracellular recording in the Acb. After 1 week, Acb cells were recorded during acquisition of the water-cocaine multiple schedule. Because behavioral responding for water was already established, training on the multiple schedule was divided into three components corresponding to acquisition of self-administration: (1) "initial" (day 1 of self-administration), (2) "reliable" (self-administration behavior was present but erratic), and (3) "stable" (cocaine responding was stable). During the initial component, the percentage of water-selective neurons was high compared with cocaine neurons. However, this became approximately equal with repeated self-administration experience (i.e., during the stable component). Remarkably, the percentage of neurons showing overlapping (similar) neuronal firing patterns during initial exposure to cocaine was low (<8%) and remained low during reliable and stable components. These findings support the view that separate neural circuits in the Acb differentially encode information about cocaine versus natural reward, and that this functional organization is not a direct consequence of chronic drug exposure.

Key words: accumbens; addiction; drug abuse; reward; self-administration; water

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Received Aug 28, 2003; revised October 6, 2003; accepted October 8, 2003.

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