Decision theory proposes that humans and animals decide what to do in a given situation by assessing the relative value of each possible response. This assessment can be computed, in part, from the probability that each action will result in a gain and the magnitude of the gain expected. Here we show that the gain (or reward) a monkey can expect to realize from an eye-movement response modulates the activity of neurons in the lateral intraparietal area, an area of primate cortex that is thought to transform visual signals into eye-movement commands. We also show that the activity of these neurons is sensitive to the probability that a particular response will result in a gain. When animals can choose freely between two alternative responses, the choices subjects make and neuronal activation in this area are both correlated with the relative amount of gain that the animal can expect from each response. Our data indicate that a decision-theoretic model may provide a powerful new framework for studying the neural processes that intervene between sensation and action.

The midbrain dopamine neurons are hypothesized to provide a physiological correlate of the reward prediction error signal required by current models of reinforcement learning. We examined the activity of single dopamine neurons during a task in which subjects learned by trial and error when to make an eye movement for a juice reward. We found that these neurons encoded the difference between the current reward and a weighted average of previous rewards, a reward prediction error, but only for outcomes that were better than expected. Thus, the firing rate of midbrain dopamine neurons is quantitatively predicted by theoretical descriptions of the reward prediction error signal used in reinforcement learning models for circumstances in which this signal has a positive value. We also found that the dopamine system continued to compute the reward prediction error even when the behavioral policy of the animal was only weakly influenced by this computation.

We review and synthesize recent neurophysiological studies of decision-making in humans and non-human primates. From these studies, the basic outline of the neurobiological mechanism for primate choice is beginning to emerge. The identified mechanism is now known to include a multi-component valuation stage, implemented in ventromedial prefrontal cortex and associated parts of striatum, and a choice stage, implemented in lateral prefrontal and parietal areas. Neurobiological studies of decision-making are beginning to enhance our understanding of economic and social behavior, as well as our understanding of significant health disorders where people’s behavior plays a key role.

Choosing the most valuable course of action requires knowing the outcomes associated with the available alternatives. The striatum may be important for representing the values of actions. We examined this in monkeys performing an oculomotor choice task. The activity of phasically active neurons (PANs) in the striatum covaried with two classes of information: action-values and chosen-values. Action-value PANs were correlated with value estimates for one of the available actions, and these signals were frequently observed before movement execution. Chosen-value PANs were correlated with the value of the action that had been chosen, and these signals were primarily observed later in the task, immediately before or persistently after movement execution. These populations may serve distinct functions mediated by the striatum: some PANs may participate in choice by encoding the values of the available actions, while other PANs may participate in evaluative updating by encoding the reward value of chosen actions.

Behavioral studies suggest that making a decision involves representing the overall desirability of all available actions and then selecting that action that is most desirable. Physiological studies have proposed that neurons in the parietal cortex play a role in selecting movements for execution. To test the hypothesis that these parietal neurons encode the subjective desirability of making particular movements, we exploited Nash's game theoretic equilibrium, during which the subjective desirability of multiple actions should be equal for human players. Behavior measured during a strategic game suggests that monkeys' choices, like those of humans, are guided by subjective desirability. Under these conditions, activity in the parietal cortex was correlated with the relative subjective desirability of actions irrespective of the specific combination of reward magnitude, reward probability, and response probability associated with each action. These observations may help place many recent findings regarding the posterior parietal cortex into a common conceptual framework.