Dissociable effects of reward and expectancy during evaluative feedback processing revealed by topographic ERP mapping analysis

Evaluative feedback provided during performance monitoring (PM) elicits either a positive or negative deflection similar to 250-300 ms after its onset in the event-related potential (ERP) depending on whether the outcome is reward-related or not, as well as expected or not. However, it remains currently unclear whether these two deflections reflect a unitary process, or rather dissociable effects arising from non-overlapping brain networks. To address this question, we recorded 64-channel EEG in healthy adult participants performing a standard gambling task where valence and expectancy were manipulated in a factorial design. We analyzed the feedback locked ERP data using a conventional ERP analysis, as well as an advanced topographic ERP mapping analysis supplemented with distributed source localization. Results reveal two main topographies showing opposing valence effects, and being differently modulated by expectancy. The first one was short-lived and sensitive to no reward irrespective of expectancy. Source-estimation associated with this topographic map comprised mainly regions of the dorsal anterior cingulate cortex. The second one was primarily driven by reward, had a prolonged time-course and was monotonically influenced by expectancy. Moreover, this reward-related topographical map was best accounted for by intracranial generators estimated in the posterior cingulate cortex. These new findings suggest the existence of dissociable brain systems depending on feedback valence and expectancy. More generally, they inform about the added value of using topographic ERP mapping methods, besides conventional ERP measurements, to characterize qualitative changes occurring in the spatio-temporal dynamic of reward processing during PM.