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The Journal of Neuroscience, August 13, 2003, 23(19):7239-7245

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Persistent Cue-Evoked Activity of Accumbens Neurons after Prolonged Abstinence from Self-Administered Cocaine

Udi E. Ghitza, Anthony T. Fabbricatore, Volodymyr Prokopenko, Anthony P. Pawlak, and Mark O. West

Department of Psychology, Rutgers University, Piscataway, New Jersey 08854

Persistent neural processing of information regarding drug-predictive environmental stimuli may be involved in motivating drug abusers to engage in drug seeking after abstinence. The addictive effects of various drugs depend on the mesocorticolimbic dopamine system innervating the nucleus accumbens. We used single-unit recording in rats to test whether accumbens neurons exhibit responses to a discriminative stimulus (S^D) tone previously paired with cocaine availability during cocaine self-administration. Presentation of the tone after 3-4 weeks of abstinence resulted in a cue-induced relapse of drug seeking under extinction conditions. Accumbens neurons did not exhibit tone-evoked activity before cocaine self-administration training but exhibited significant S^D tone-evoked activity during extinction. Under extinction conditions, shell neurons exhibited significantly greater activity evoked by the S^D tone than that evoked by a neutral tone (i.e., never paired with reinforcement). In contrast, core neurons responded indiscriminately to presentations of the S^D tone or the neutral tone. Accumbens shell neurons exhibited significantly greater S^D tone-evoked activity than did accumbens core neurons. Although the onset of S^D tone-evoked activity occurred well before the earliest movements commenced (150 msec), this activity often persisted beyond the onset of tone-evoked movements. These results indicate that accumbens shell neurons exhibit persistent processing of information regarding reward-related stimuli after prolonged drug abstinence. Moreover, the accumbens shell appears to be involved in discriminating the motivational value of reward-related associative stimuli, whereas the accumbens core does not.

Key words: addiction; self-administration; drug; cocaine; psychomotor stimulant; nucleus accumbens; neuron; electrophysiology; reinforcement; reward; incentive motivation; relapse; cue; conditioning

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Received Apr. 9, 2003; revised Jun. 11, 2003; accepted Jun. 12, 2003.

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