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Multiple reward signals in the brain

Nature Reviews Neuroscience volume 1, pages 199–207 (2000)Cite this article

Key Points

  • This article describes how neurons detect rewards, learn to predict future rewards from past experience, and use reward information for learning, choosing, preparing and executing goal-directed behaviour. It also attempts to place the processing of drug rewards within a general framework of neuronal reward mechanisms.

  • Rewards are defined by their action on behaviour, and are crucial for the survival of the organism. They are vital in the control of homeostasis, sustain learning of new behaviours, the induction of approach behaviour and serve as goals for voluntary, intentional behaviour.

  • Various neurons detect the occurrence of rewards and reward-predicting stimuli, including those of the ascending dopamine systems, and neurons within the striatum, orbitofrontal cortex and amygdala. Some of these neurons seem to provide a reward prediction error signal that could be used for learning mechanisms, whereas others seem to be involved in the perception of individual rewards or objects that signal rewards.

  • Some neurons in the striatum and orbitofrontal cortex do not respond directly to rewards but seem to anticipate the occurrence of future rewards. Some neurons process reward information that is dependent on the relative motivational value of the reward.

  • Neurons in the striatum and different areas of frontal and parietal cortex incorporate information about expected rewards into neuronal activity involved in the production of behaviour leading to reward acquisition. They seem to code the goals of behaviour at the time the behaviour towards the goal is being prepared and executed. Some neurons are active before self-initiated, reward-directed movements and adapt their activity according to ongoing experience.

  • These studies show that different aspects of reward functions are processed by different neurons in different brain structures. The optimal use of reward information for learning and controlling behaviour requires cooperation between these neuronal reward signals.

  • The brain structures involved in the processing of natural rewards also seem to be the critical structures for the action of drugs of abuse. One may ask whether such drugs modify existing neuronal responses to natural rewards or constitute rewards in their own right, and as such engage existing neuronal reward mechanisms, directing subjects towards artificially rewarding goals.

  • This research describes the first steps towards an understanding of how rewards influence behaviour before their receipt and how the brain might use reward information to control learning and goal-directed behaviour.

Abstract

The fundamental biological importance of rewards has created an increasing interest in the neuronal processing of reward information. The suggestion that the mechanisms underlying drug addiction might involve natural reward systems has also stimulated interest. This article focuses on recent neurophysiological studies in primates that have revealed that neurons in a limited number of brain structures carry specific signals about past and future rewards. This research provides the first step towards an understanding of how rewards influence behaviour before they are received and how the brain might use reward information to control learning and goal-directed behaviour.

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Figure 1: Reward processing and the brain.
Figure 2: Primate dopamine neurons respond to rewards and reward-predicting stimuli.
Figure 3: Neuronal activity in primate striatum and orbitofrontal cortex related to the expectation of reward.
Figure 4: Behaviour-related activity in the primate caudate reflects future goals.

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Acknowledgements

The crucial contributions of the collaborators in my own cited work are gratefully acknowledged, as are the collegial interactions with Anthony Dickinson (Cambridge) and Masataka Watanabe (Tokyo). Our work was supported by the Swiss National Science Foundation, European Community, McDonnell–Pew Program, Roche Research Foundation and British Council, and by postdoctoral fellowships from the US NIMH, FRS Quebec, Fyssen Foundation and FRM Paris.

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  1. Institute of Physiology and Program in Neuroscience, University of Fribourg, Fribourg, CH-1700, Switzerland

    Wolfram Schultz

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ENCYCLOPEDIA OF LIFE SCIENCES

Dopamine

Glossary

GOAL-DIRECTED BEHAVIOUR

Behaviour controlled by representation of a goal or an understanding of a causal relationship between behaviour and attainment of a goal.

REINFORCERS

Positive reinforcers (rewards) increase the frequency of behaviour leading to their acquisition. Negative reinforcers (punishers) decrease the frequency of behaviour leading to their encounter and increase the frequency of behaviour leading to their avoidance.

PAVLOVIAN (CLASSICAL) CONDITIONING

Learning a predictive relationship between a stimulus and a reinforcer — does not require an action by the agent.

OPERANT (INSTRUMENTAL) CONDITIONING

Learning a relationship between a stimulus, an action and a reinforcer conditional on an action by the agent.

EXTINCTION

Reduction and cessation of a predictive relationship and behaviour following the omission of a reinforcer (negative prediction error).

MOTIVATIONAL VALUE

A measure of the effort an agent is willing to expend to obtain an object signalling reward or to avoid an object signalling punishment.

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Schultz, W. Multiple reward signals in the brain. Nat Rev Neurosci 1, 199–207 (2000). https://doi.org/10.1038/35044563

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