Reward unpredictability inside and outside of a task context as a determinant of the responses of tonically active neurons in the monkey striatum

Tonically active neurons (TANs) in the monkey striatum are involved in detecting motivationally relevant stimuli. We recently provided evidence that the timing of conditioned stimuli strongly influences the responsiveness of TANs, the source of which is likely to be the monkey's previous experience with particular temporal regularities in sequential task events. To extend these findings, we investigated the relationship of TAN responses to a primary liquid reward, the timing of which is more or less predictable to the monkey either outside of a task or during instrumental task performance. Reward predictability was indexed by the timing characteristics of the mouth movements. The responsiveness of TANs to reward increased with the range and variability of time periods before reward, notably when the liquid was delivered outside of a task. A change in the temporal order of events in a task context produced an increase of response to reward, suggesting an influence of the predicted nature of the event in addition to its time of occurrence. By contrast, we observed no substantial changes in neuronal activity at the expected time of reward when this event failed to occur, suggesting that these neurons do not appear to carry information about an error in reward prediction. These results demonstrate that TANs constitute a neuronal system that is involved in detecting unpredicted reward events, irrespective of the specific behavioral situation in which such events occur. The responses influenced by stimulus prediction may constitute a neuronal basis for the notion that striatal processing is crucial for habit learning.