Theta and high-beta networks for feedback processing: a simultaneous EEG-fMRI study in healthy male subjects

The reward system is important in assessing outcomes to guide behavior. To achieve these purposes, its core components interact with several brain areas involved in cognitive and emotional processing. A key mechanism suggested to subserve these interactions is oscillatory activity, with a prominent role of theta and high-beta oscillations. The present study used single-trial coupling of simultaneously recorded electroencephalography and functional magnetic resonance imaging data to investigate networks associated with oscillatory responses to feedback during a two-choice gambling task in healthy male participants (n = 19). Differential associations of theta and high-beta oscillations with non-overlapping brain networks were observed: Increase of high-beta power in response to positive feedback was associated with activations in a largely subcortical network encompassing core areas of the reward network. In contrast, theta-band power increase upon loss was associated with activations in a frontoparietal network that included the anterior cingulate cortex. Trait impulsivity correlated significantly with activations in areas of the theta-associated network. Our results suggest that positive and negative feedback is processed by separate brain networks associated with different cognitive functions. Communication within these networks is mediated by oscillations of different frequency, possibly reflecting different modes of dopaminergic signaling.