Dopamine plays a key role in motivation and reward. Dopaminergic neurons in the ventral tegmental area (VTA) signal the discrepancy between expected and actual rewards (i.e., reward prediction error, RPE)1-3, but how they compute such signals is unknown. We recorded the activity of VTA neurons while mice associated different odour cues with appetitive and aversive outcomes. We found three types of neurons based on responses to odours and outcomes: approximately half of the neurons (Type I, 52%) showed phasic excitation after reward-predicting odours and rewards in a manner consistent with RPE coding. The other half of neurons showed persistent activity during the delay between odour and outcome, that was modulated positively (Type II, 31%) or negatively (Type III, 17%) by the value of outcomes. While the activity of Type I neurons was sensitive to actual outcomes (i.e., when the reward was delivered as expected vs. unexpectedly omitted), the activity of Types II and III neurons was determined predominantly by reward-predicting odours. We “tagged” dopaminergic and GABAergic neurons with the light-sensitive protein channelrhodopsin-2 (ChR2) and identified them based on their responses to optical stimulation while recording. All identified dopaminergic neurons were of Type I and all GABAergic neurons were of Type II. These results show that VTA GABAergic neurons signal expected reward, a key variable for dopaminergic neurons to calculate RPE.

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Recent studies indicate that dopamine neurons in the ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) convey distinct signals. To explore this difference, we comprehensively identified each area's monosynaptic inputs using the rabies virus. We show that dopamine neurons in both areas integrate inputs from a more diverse collection of areas than previously thought, including autonomic, motor, and somatosensory areas. SNc and VTA dopamine neurons receive contrasting excitatory inputs: the former from the somatosensory/motor cortex and subthalamic nucleus, which may explain their short-latency responses to salient events; and the latter from the lateral hypothalamus, which may explain their involvement in value coding. We demonstrate that neurons in the striatum that project directly to dopamine neurons form patches in both the dorsal and ventral striatum, whereas those projecting to GABAergic neurons are distributed in the matrix compartment. Neuron-type-specific connectivity lays a foundation for studying how dopamine neurons compute outputs.

Humans and other animals must often make decisions on the basis of imperfect evidence. Statisticians use measures such as P values to assign degrees of confidence to propositions, but little is known about how the brain computes confidence estimates about decisions. We explored this issue using behavioural analysis and neural recordings in rats in combination with computational modelling. Subjects were trained to perform an odour categorization task that allowed decision confidence to be manipulated by varying the distance of the test stimulus to the category boundary. To understand how confidence could be computed along with the choice itself, using standard models of decision-making, we defined a simple measure that quantified the quality of the evidence contributing to a particular decision. Here we show that the firing rates of many single neurons in the orbitofrontal cortex match closely to the predictions of confidence models and cannot be readily explained by alternative mechanisms, such as learning stimulus-outcome associations. Moreover, when tested using a delayed reward version of the task, we found that rats' willingness to wait for rewards increased with confidence, as predicted by the theoretical model. These results indicate that confidence estimates, previously suggested to require 'metacognition' and conscious awareness are available even in the rodent brain, can be computed with relatively simple operations, and can drive adaptive behaviour. We suggest that confidence estimation may be a fundamental and ubiquitous component of decision-making.