Abstract

Besides their fundamental movement function evidenced by Parkinsonian deficits, the basal ganglia are involved in processing closely linked non-motor, cognitive and reward information. This review describes the reward functions of three brain structures that are major components of the basal ganglia or are closely associated with the basal ganglia, namely midbrain dopamine neurons, pedunculopontine nucleus, and striatum (caudate nucleus, putamen, nucleus accumbens). Rewards are involved in learning (positive reinforcement), approach behavior, economic choices and positive emotions. The response of dopamine neurons to rewards consists of an early detection component and a subsequent reward component that reflects a prediction error in economic utility, but is unrelated to movement. Dopamine activations to non-rewarded or aversive stimuli reflect physical impact, but not punishment. Neurons in pedunculopontine nucleus project their axons to dopamine neurons and process sensory stimuli, movements and rewards and reward-predicting stimuli without coding outright reward prediction errors. Neurons in striatum, besides their pronounced movement relationships, process rewards irrespective of sensory and motor aspects, integrate reward information into movement activity, code the reward value of individual actions, change their reward-related activity during learning, and code own reward in social situations depending on whose action produces the reward. These data demonstrate a variety of well-characterized reward processes in specific basal ganglia nuclei consistent with an important function in non-motor aspects of motivated behavior.

Highlights

  • The functions of the basal ganglia are closely linked to movements

  • The motor functions of the basal ganglia known from clinical conditions extend into a more global role in actions that are performed to attain a rewarding goal or occur on a more automatic, habitual basis

  • The link from movement to reward is represented in neuronal signals in the basal ganglia and the pedunculopontine nucleus (PPN)

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Summary

Introduction

The functions of the basal ganglia are closely linked to movements. This view derives from deficits arising after lesions, from anatomical connections with other brain structures with well-understood motor functions, and from the neuronal activity recorded in behaving animals. After the stimulus identification by the second component, the reward representation stays on in dopamine neurons; this is evidenced by the prediction error response at the time of the reward, which reflects the predicted value at that moment (Fig. 1b) (Tobler et al 2003; Nomoto et al 2010).

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