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The Journal of Neuroscience, March 24, 2004, 24(12):2923-2933; doi:10.1523/JNEUROSCI.5282-03.2004

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Behavioral/Systems/Cognitive
The Ventral Tegmental Area Is Required for the Behavioral and Nucleus Accumbens Neuronal Firing Responses to Incentive Cues

Irene A. Yun,^1,2 Ken T. Wakabayashi,¹ Howard L. Fields,^1,3 and Saleem M. Nicola¹

¹Ernest Gallo Clinic and Research Center, University of California, San Francisco, Emeryville, California 94608, and ²Graduate Program in Neuroscience and ³Departments of Neurology and Physiology, and Wheeler Center for the Neurobiology of Addiction, University of California, San Francisco, California 94143

Reward-predictive cues exert powerful control over behavioral choice and may be a critical factor in drug addiction. Reward-seeking elicited by predictive cues is facilitated by the release of dopamine in the nucleus accumbens (NAc), yet the contribution of dopamine to the specific NAc firing patterns that underlie goal-directed behavior has remained elusive. We present evidence that subpopulations of NAc neurons that respond to predictive cues require the dopaminergic projection from the ventral tegmental area (VTA) to promote reward-seeking behavior. Rats trained to perform an operant response to a cue to obtain a sucrose reward were implanted with both multiunit recording electrodes in the NAc and microinjection cannulas in the VTA. Both the behavioral response to cues and the cue-evoked firing of NAc neurons were blocked by injection of the GABA_B agonist baclofen into the VTA. An additional group of rats was trained on the same task and then implanted with microinjection cannulas in the NAc. Like VTA baclofen injection, injection of dopamine receptor antagonists into the NAc profoundly reduced cue-elicited reward seeking. Together, these results support the conclusion that both the behavioral response to the cue and the specific NAc neuronal firing that promotes the response depend on dopamine release within the NAc. Our findings suggest a neural mechanism by which the dopamine-dependent firing of NAc neurons mediates goal-directed behavior.

Key words: dopamine; motivation; operant; reward; goal-directed behavior; nucleus accumbens; basal ganglia; ventral striatum; discriminative stimulus

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Received Aug 27, 2003; revised February 9, 2004; accepted February 9, 2004.

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