Risk prediction error signaling: A two-component response?

Organisms use rewards to navigate and adapt to (uncertain) environments. Error-based learning about rewards is supported by the dopaminergic system, which is thought to signal reward prediction errors to make adjustments to past predictions. More recently, the phasic dopamine response was suggested to have two components: the first rapid component is thought to signal the detection of a potentially rewarding stimulus; the second, slightly later component characterizes the stimulus by its reward prediction error. Error-based learning signals have also been found for risk. However, whether the neural generators of these signals employ a two-component coding scheme like the dopaminergic system is unknown. Here, using human high density EEG, we ask whether risk learning, or more generally speaking surprise-based learning under uncertainty, is similarly comprised of two temporally dissociable components. Using a simple card game, we show that the risk prediction error is reflected in the amplitude of the P3b component. This P3b modulation is preceded by an earlier component, that is modulated by the stimulus salience. Source analyses are compatible with the idea that both the early salience signal and the later risk prediction error signal are generated in insular, frontal, and temporal cortex. The identified sources are parts of the risk processing network that receives input from noradrenergic cells in the locus coeruleus. Finally, the P3b amplitude modulation is mirrored by an analogous modulation of pupil size, which is consistent with the idea that both the P3b and pupil size indirectly reflect locus coeruleus activity.