Abstract
To learn, obtain reward and survive, humans and other animals must monitor, approach and act on objects that are associated with variable or unknown rewards. However, the neuronal mechanisms that mediate behaviours aimed at uncertain objects are poorly understood. Here we demonstrate that a set of neurons in an internal-capsule bordering regions of the primate dorsal striatum, within the putamen and caudate nucleus, signal the uncertainty of object–reward associations. Their uncertainty responses depend on the presence of objects associated with reward uncertainty and evolve rapidly as monkeys learn novel object–reward associations. Therefore, beyond its established role in mediating actions aimed at known or certain rewards, the dorsal striatum also participates in behaviours aimed at reward-uncertain objects.
Highlights
To learn, obtain reward and survive, humans and other animals must monitor, approach and act on objects that are associated with variable or unknown rewards
Our experiments showed that a subset of neurons, mostly in the internal-capsule bordering regions of the dorsal striatum (DS), was preferentially activated by visual objects associated with rewarduncertain outcomes
The internal-capsule bordering regions of the DS (icbDS) reward-uncertainty responses depended on the presence of visual objects associated with reward uncertainty because they were mostly ablated when the object was removed before the uncertain outcome was delivered
Summary
Obtain reward and survive, humans and other animals must monitor, approach and act on objects that are associated with variable or unknown rewards. We demonstrate that a set of neurons in an internal-capsule bordering regions of the primate dorsal striatum, within the putamen and caudate nucleus, signal the uncertainty of object– reward associations. Their uncertainty responses depend on the presence of objects associated with reward uncertainty and evolve rapidly as monkeys learn novel object–reward associations. During object–reward associative learning, icbDS neurons’ uncertainty responses evolved rapidly as monkeys learned novel object–reward associations These uncertainty responses identified object associations that were uncertain either due to the subjects’ lack of knowledge or due to known uncertainty ( called risk[18,19]). Our experiments suggest that uncertainty-sensitive neurons in the primate DS may play important roles in object-based behaviours under uncertainty
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