Abstract
SummaryThe time of reward and the temporal structure of reward occurrence fundamentally influence behavioral reinforcement and decision processes [1–11]. However, despite knowledge about timing in sensory and motor systems [12–17], we know little about temporal mechanisms of neuronal reward processing. In this experiment, visual stimuli predicted different instantaneous probabilities of reward occurrence that resulted in specific temporal reward structures. Licking behavior demonstrated that the animals had developed expectations for the time of reward that reflected the instantaneous reward probabilities. Neurons in the amygdala, a major component of the brain's reward system [18–29], showed two types of reward signal, both of which were sensitive to the expected time of reward. First, the time courses of anticipatory activity preceding reward delivery followed the specific instantaneous reward probabilities and thus paralleled the temporal reward structures. Second, the magnitudes of responses following reward delivery covaried with the instantaneous reward probabilities, reflecting the influence of temporal reward structures at the moment of reward delivery. In being sensitive to temporal reward structure, the reward signals of amygdala neurons reflected the temporally specific expectations of reward. The data demonstrate an active involvement of amygdala neurons in timing processes that are crucial for reward function.
Highlights
Experimental Design We studied the activity of single amygdala neurons in two rhesus monkeys using a Pavlovian reward prediction task superimposed on an ocular fixation task
Further work may elucidate the nature and extent of time-sensitive prediction error responses of amygdala neurons. These data show that the temporal structure of reward occurrence influenced the activity of amygdala neurons
Responses following the reward were enhanced when a reward was either more likely or more surprising to occur. Both types of activity reflected predictability of instantaneous reward rate rather than overall sum of future reward. These modulations suggest that amygdala neurons have access to an internal clock that processes the time of future reward occurrence
Summary
The time of reward and the temporal structure of reward occurrence fundamentally influence behavioral reinforcement and decision processes [1–11]. Despite knowledge about timing in sensory and motor systems [12–17], we know little about temporal mechanisms of neuronal reward processing. In this experiment, visual stimuli predicted different instantaneous probabilities of reward occurrence that resulted in specific temporal reward structures. Licking behavior demonstrated that the animals had developed expectations for the time of reward that reflected the instantaneous reward probabilities. The time courses of anticipatory activity preceding reward delivery followed the specific instantaneous reward probabilities and paralleled the temporal reward structures. In being sensitive to temporal reward structure, the reward signals of amygdala neurons reflected the temporally specific expectations of reward. The data demonstrate an active involvement of amygdala neurons in timing processes that are crucial for reward function
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