Anterior cingulate activity to monetary loss and basal ganglia activity to monetary gain uniquely contribute to the feedback negativity.

Objective: The feedback negativity (FN) is an event-related potential that differentiates unfavorable versus favorable outcomes. Although thought to reflect error-related activity within the anterior cingulate cortex, recent work indicates the FN may also reflect reward-related activity that has been linked to the basal ganglia. To date, it remains unclear how to reconcile these conflicting perspectives.

Methods: We decomposed the FN by applying time-frequency analysis to isolate activity unique to monetary losses and gains. The FN was recorded from 84 individuals during a laboratory gambling task.

Results: Two signals contributed to the FN elicited by unpredictable outcomes: theta activity (4-7Hz) was increased following monetary loss, and delta activity (<3Hz) was increased following monetary gain. Predictable outcomes elicited delta but not theta activity. Source analysis revealed distinct generators, with loss-related theta localized to the anterior cingulate cortex and gain-related delta to a possible source in the striatum. Symptoms of depression, anxiety, and stress reactivity were specifically associated with blunted gain-related delta.

Conclusions: The FN may be a composite of loss- and gain-related neural activity, reflecting distinct facets of reward processing.

Significance: Gain-related delta activity may provide unique information about reward dysfunction in major depression and other internalizing psychopathology.