Reward Processing in Primate Orbitofrontal Cortex and Basal Ganglia

TLDR

Reward processing in primate orbitofrontal cortex and basal ganglia is a key neural substrate for encoding reward expectation and delivery. This review interprets neuronal activities related to reward expectation and delivery in the primate orbitofrontal cortex, comparing them with slowly discharging striatal neurons and midbrain dopamine neurons. Orbitofrontal neurons show reward‑predicting, expectation, and reward‑response activity that discriminates reward value; striatal neurons encode reward expectation and reward‑related movement; dopamine neurons signal reward and prediction errors, together indicating heterogeneous activations that support reward learning and goal‑directed behavior.

Abstract

This article reviews and interprets neuronal activities related to the expectation and delivery of reward in the primate orbitofrontal cortex, in comparison with slowly discharging neurons in the striatum (caudate, putamen and ventral striatum, including nucleus accumbens) and midbrain dopamine neurons. Orbitofrontal neurons showed three principal forms of reward-related activity during the performance of delayed response tasks, namely responses to reward-predicting instructions, activations during the expectation period immediately preceding reward and responses following reward. These activations discriminated between different rewards, often on the basis of the animals' preferences. Neurons in the striatum were also activated in relation to the expectation and detection of reward but in addition showed activities related to the preparation, initiation and execution of movements which reflected the expected reward. Dopamine neurons responded to rewards and reward-predicting stimuli, and coded an error in the prediction of reward. Thus, the investigated cortical and basal ganglia structures showed multiple, heterogeneous, partly simultaneous activations which were related to specific aspects of rewards. These activations may represent the neuronal substrates of rewards during learning and established behavioral performance. The processing of reward expectations suggests an access to central representations of rewards which may be used for the neuronal control of goaldirected behavior.