Responses of Tonic Striatal Neurons to Conditioned Stimuli in Behaving Monkeys

Summary

Previous studies have shown that tonically discharging neurons in monkey striatum can be modulated by the onset of external stimuli, which are reliable predictors of a rewarding event. In this study, we investigated the responses of tonic neurons to visual stimuli presented in advance of the delivery of reward or without any subsequent reward. A total number of 158 tonic neurons with typical electrophysiological characteristics was recorded in the caudate nucleus and putamen of two monkeys under two behavioral conditions: (1) an active one, in which a specific arm movement triggered by a visual stimulus had to be performed to obtain a reward, (2) a passive one, in which a visual stimulus was consistently and automatically followed by a reward. With each of these conditions, the non-rewarded trials were run in separate sessions to check whether there were any reward-specific effects. Most of the neurons responded to the stimuli associated with reward both during the active and the passive conditions, suggesting that the responses were not specific to the type of behavioral reaction to be initiated. In some responding neurons, the responses remained present in the nonperforming condition when a stimulus not followed by the reward was repeatedly presented. Responses could also occur in the task performance condition when the stimulus was presented at a point that was out of the monkey’s reach. The fact that neuronal responses persisted in conditions in which the animal knew that he would not get a reward after detecting a stimulus suggests that the responses observed here were not specifically dependent on the reward components of the behavioral conditions. These results indicate that although there exist several lines of evidence showing that tonic striatal neurons respond to stimuli eliciting immediate behavioral reactions and predicting that a reward is forthcoming, these neurons may be involved in some more general aspects of the animals’ reactivity to environmental stimuli in a behavioral context.