Tonically Active Neurons in the Monkey Striatum are Sensitive to Sensory Events in a Manner that Reflects their Predictability in Time
It is now well established that tonically active neurons (TANs) in the monkey striatum respond to motivationally relevant sensory events, such as conditioned stimuli to which the animal had to react correctly to obtain reward. Recent findings obtained in our laboratory suggested that stimulus prediction may influence the responsiveness of the TANs. In the present study we specifically investigated the effects of temporal aspects of prediction on the responses of single TANs recorded both in the caudate nucleus and putamen of two macaque monkeys. Three different behavioral situations were employed: (1) an instrumental task, in which a visual stimulus triggering a rewarded movement was preceded by an instruction stimulus presented at a fixed interval of 1.5 s before the trigger onset; (2) a classically conditioned task, in which a visual stimulus was followed after a fixed interval of 1 s by the delivery of a liquid reward without requiring the monkey to react to the stimulus; (3) a free reward condition, in which a liquid reward was delivered at unpredictable times (5.5–8.5 s). Both monkeys received extensive training on the two tasks having a fixed time interval between the predictive cue and the trigger stimulus or reward. To study the effect of changes in the temporal predictability of stimuli, the interval between instruction and trigger stimuli was prolonged to 4.5 s in the instrumental task and the reward was given earlier (0.3 s) or later (2 s) than its usual time of delivery in the classically conditioned task. The percentage of TANs showing responses was increased when stimuli were less predictable in time, compared to the situations in which the onset time of stimuli was highly predictable. Responses to reward given outside of any task were reduced with repeated liquid delivery at the same 2 s intervals, further suggesting that the temporal predictability of stimuli was an important factor for eliciting neuronal responses. The present results demonstrate that the efficacy of stimuli to modulate the string of TANs is determined both by the motivational relevance of stimuli and by predictions about stimulus timing.
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