Event‐related potential activity in the basal ganglia differentiates rewards from nonrewards: Temporospatial principal components analysis and source localization of the feedback negativity

Originally, the feedback related negativity (FRN) event-related potential (ERP) component was considered to be a robust neural correlate of non-reward/punishment processing, with greater negative deflections observed following unfavourable outcomes. More recently, it has been suggested that this component is better conceptualised as a positive deflection following rewarding outcomes. The current study sought to elucidate the nature of the FRN, as well as another component associated with incentive-value processing, the P3b, through application of a spatiotemporal principal components analysis (PCA). Seventeen healthy controls played a computer electronic gaming machine (EGM) task and received feedback on credits won or lost on each trial, and ERPs were recorded. The distribution of reward/non-reward outcomes closely matched that of a real EGM, with frequent losses, and infrequent wins and near-wins. The PCA revealed that feedback elicited both a frontally maximal negative deflection to losses, and a positive deflection to wins (which was also sensitive to reward magnitude), implying that the neural generator/s of the FRN are differentially activated following these outcomes. As expected, greater P3b amplitudes were found for wins compared to losses. Interestingly, near-wins elicited significantly smaller FRN amplitudes than losses (with no differences in P3b amplitude), and may contribute to the maintenance of gambling behaviours on EGMs. The results of the current study are integrated into a response profile of healthy controls to outcomes of varying incentive value. This may provide a foundation for the future examination of individuals who exhibit abnormalities in reward/ punishment processing, such as problem gamblers. The PCA revealed that feedback elicited both a frontally maximal negative deflection to losses, and a positive deflection to wins (which was also sensitive to reward magnitude), implying that the neural generator/s of the FRN are differentially activated following these outcomes. As expected, greater P3b amplitudes were found for wins compared to losses.Interestingly, near-wins elicited significantly smaller FRN amplitudes than losses (with no differences in P3b amplitude), and may contribute to the maintenance of gambling behaviours on EGMs. The results of the current study are integrated into a response profile of healthy controls to outcomes of varying incentive value. This may provide a foundation for the future examination of individuals who exhibit abnormalities in reward/punishment processing, such as problem gamblers.

Models of reinforcement learning represent reward and punishment in terms of reward prediction errors (RPEs), quantitative signed terms describing the degree to which outcomes are better than expected (positive RPEs) or worse (negative RPEs). An electrophysiological component known as feedback related negativity (FRN) occurs at frontocentral sites 240-340 ms after feedback on whether a reward or punishment is obtained, and has been claimed to neurally encode an RPE. An outstanding question however, is whether the FRN is sensitive to the size of both positive RPEs and negative RPEs. Previous attempts to answer this question have examined the simple effects of RPE size for positive RPEs and negative RPEs separately. However, this methodology can be compromised by overlap from components coding for unsigned prediction error size, or "salience", which are sensitive to the absolute size of a prediction error but not its valence. In our study, positive and negative RPEs were parametrically modulated using both reward likelihood and magnitude, with principal components analysis used to separate out overlying components. This revealed a single RPE encoding component responsive to the size of positive RPEs, peaking at ~330 ms, and occupying the delta frequency band. Other components responsive to unsigned prediction error size were shown, but no component sensitive to negative RPE size was found.

Background Cognitive behavioral therapy (CBT) is a well-established treatment for anxiety and depression; however, response to CBT is heterogeneous across patients and many remain symptomatic after therapy, raising the need to identify prospective predictors for treatment planning. Altered neural processing of reward has been implicated in both depression and anxiety, and improving hedonic capacity is a goal of CBT. However, little is known about how neural response to reward relates to CBT outcomes in depression and anxiety. The current study used the reward positivity (RewP) event-related potential (ERP) component to examine whether neural reactivity to reward would predict CBT response in a sample of patients with anxiety without depression (n = 30) and comorbid anxiety and depression (CAD, n = 22). Methods Participants completed a guessing reward ERP paradigm before completing 12 weeks of standard CBT. Results The majority of the sample (68%; 35 of 52 patients) responded to treatment, and those with a reduced RewP at baseline were more likely to respond to treatment. A reduced RewP was also associated with a greater pre-to-post CBT reduction in depressive symptoms among individuals with CAD, but not among individuals with pure anxiety. Conclusions CBT may be most beneficial in reducing depressive symptoms for individuals who demonstrate decreased reward reactivity prior to treatment. CBT may target reward brain function, leading to greater improvement in symptoms. These effects may be strongest, and therefore most meaningful, for individuals with reward processing deficits prior to treatment.