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Firing of Nucleus Accumbens Neurons During the Consummatory Phase of a Discriminative Stimulus Task Depends on Previous Reward Predictive Cues

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

Submitted 9 July 2003; accepted in final form 20 November 2003

The nucleus accumbens (NAc) plays an important role in both appetitive and consummatory behavior. To examine how NAc neurons encode information during reward consumption, we recorded the firing activity of rat NAc neurons during the performance of a discriminative stimulus task. In this task, the animal must make an operant response to an intermittently presented cue to obtain a sucrose reward delivered in a reward receptacle. Uncued entries to the receptacle were not rewarded. Both excitations and inhibitions during reward consumption were observed, but substantially more neurons were inhibited than excited. These excitations and inhibitions began when the animal entered the reward receptacle and ended when the animal exited the receptacle. Both excitations and inhibitions were much smaller or nonexistent when the animal made uncued entries into the reward receptacle. In one set of experiments, we randomly withheld the reward in some cued trials that would otherwise have been rewarded. Excitations and inhibitions were of similar magnitude whether or not the reward was delivered. This indicates that the sensory stimulus of reward does not drive these phasic responses; instead, the reward-associated responses may be driven by the conditioned stimuli associated with reward, or they may encode information about consummatory motor activity. Another population of NAc neurons was excited on exit from the reward receptacle. Many of these excitations persisted for tens of seconds after the receptacle exit and showed a significant inverse correlation with the rate of uncued operant responding. These findings are consistent with a contribution of NAc neurons to both reward consummatory and reward seeking behavior.

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