Influence of reward expectation on behavior-related neuronal activity in primate striatum

Abstract

Rewards constitute important goals for voluntary behavior. This study aimed to investigate how expected rewards influence behavior-related neuronal activity in the anterior striatum. In a delayed go-nogo task, monkeys executed or withheld a reaching movement and obtained liquid or sound as reinforcement. An initial instruction picture indicated the behavioral reaction to be performed and the reinforcer to be obtained after a subsequent trigger stimulus. Movements varied according to the reinforcers predicted by the instructions, suggesting that animals differentially expected the two outcomes. About 250 of nearly 1,500 neurons in anterior parts of caudate nucleus, putamen, and ventral striatum showed typical task-related activations that reflected the expectation of instructions and trigger, and the preparation, initiation, and execution of behavioral reactions. Strikingly, most task-related activations occurred only when liquid reward was delivered at trial end, rather than the reinforcing sound. Activations close to the time of reward showed similar preferences for liquid reward over the reinforcing sound, suggesting a relationship to the expectation or detection of the motivational outcome of the trial rather than to a "correct" or "end-of-trial" signal. By contrast, relatively few activations in the present task occurred irrespective of the type of reinforcement. In conclusion, many of the behavior-related neurons investigated in the anterior striatum were influenced by an upcoming primary liquid reward and did not appear to code behavioral acts in a motivationally neutral manner. Rather, these neurons incorporated information about the expected outcome into their behavior-related activity. The activations influenced by reward several seconds before its occurrence may constitute a neuronal basis for the retrograde effects of rewards on behavioral reactions.