The role of outcome expectations in the generation of the feedback‐related negativity

The feedback‐related negativity (FRN) is thought to index activity within the midbrain dopaminergic reward‐learning system, with larger FRN magnitudes observed when outcomes are worse than expected. This view holds that the FRN is an index of neural activity coding for prediction errors, and reflects activity that can be used to adaptively alter future performance. Untested to date, however, is a key prediction of this view: the FRN should not appear in response to negative outcomes when outcome expectations are not allowed to develop. The current study tests this assumption by eliciting FRNs to win and loss feedback in conditions of participant choice, participant observation of computer choice, and, critically, simple presentation of win or loss feedback in the absence of a predictive choice cue. Whereas FRNs were observed in each of the conditions in which there was time for an expectation to develop, no FRN was observed in conditions without sufficient time for the development of an expectation. These results provide empirical support for an untested but central tenet of the reinforcement learning account of the genesis of the FRN.     

A Developmental Study of the Feedback-Related Negativity From 10–17 Years: Age and Sex Effects for Reward Versus Non-Reward

We employed event-related potentials to examine the feedback-related negativity (FRN), during a non-learning reward versus non-reward task. We compared 10–12-year-old, 13–14-year-old, and 15–17-year-old youth (n?=?91). Age effects included a larger FRN for younger age groups, regardless of feedback type, and a decrease in peak latency for feedback, across age groups as a linear trend. Males showed larger responses irrespective of feedback type and longer latency for rewarded feedback. Source modeling revealed reward/non-reward differences in the anterior cingulate cortex (ACC) and orbitofrontal cortex, most strongly in the subgenual ACC. Males showed more subgenual ACC activity for feedback overall.     

Processing of expected and unexpected monetary performance outcomes in healthy older subjects

The feedback-related negativity (FRN), an event-related potential (ERP) component reflecting feedback processing in the anterior cingulate cortex (ACC), has consistently been found to be reduced in healthy aging, whereas behavioral findings regarding age-related changes in decision making and feedback-based learning are inconsistent. This study aimed to elucidate similarities and differences between healthy younger and older subjects in the processing of monetary performance feedback focusing on effects of reward expectancy. Eighteen younger and 20 older subjects completed a feedback learning task, in which a rule could be learned to predict the reward probabilities associated with particular stimuli. Older subjects showed evidence of slower learning than younger subjects. In both younger and older subjects, the amplitude difference between nonreward and reward in the FRN time window was larger for unexpected than expected outcomes, driven by modulations of negative feedback ERPs. Consistent with previous findings, the amplitude difference tended to be generally reduced in older subjects. P300 amplitude was larger for reward than nonreward in both groups, and interactions between valence and probability indicated that only the P300 for reward was modulated by expectancy. Despite general changes of outcome-related ERPs in healthy aging, older subjects show evidence of preserved effects of expectancy on the processing of monetary feedback.     

A target sample of adolescents and reward processing: same neural and behavioral correlates engaged in common paradigms?

Adolescence is a transition period that is assumed to be characterized by increased sensitivity to reward. While there is growing research on reward processing in adolescents, investigations into the engagement of brain regions under different reward-related conditions in one sample of healthy adolescents, especially in a target age group, are missing. We aimed to identify brain regions preferentially activated in a reaction time task (monetary incentive delay (MID) task) and a simple guessing task (SGT) in a sample of 14-year-old adolescents (N?=?54) using two commonly used reward paradigms. Functional magnetic resonance imaging was employed during the MID with big versus small versus no win conditions and the SGT with big versus small win and big versus small loss conditions. Analyses focused on changes in blood oxygen level?Cdependent contrasts during reward and punishment processing in anticipation and feedback phases. We found clear magnitude-sensitive response in reward-related brain regions such as the ventral striatum during anticipation in the MID task, but not in the SGT. This was also true for reaction times. The feedback phase showed clear reward-related, but magnitude-independent, response patterns, for example in the anterior cingulate cortex, in both tasks. Our findings highlight neural and behavioral response patterns engaged in two different reward paradigms in one sample of 14-year-old healthy adolescents and might be important for reference in future studies investigating reward and punishment processing in a target age group.     

Aging and electrocortical response to error feedback during a spatial learning task

Event-related potentials were collected as older and younger adults responded to error feedback in an adaptation of the Groton Maze Learning Test, an age-sensitive measure of spatial learning and executive skills expected to maximally involve anterior cingulate cortex (ACC). Older adults made more errors and produced smaller feedback-related negativities (FRNs) than young controls. LORETA source localization revealed that, for young adults, neural activation associated with the FRN was focused in ACC and was stronger to negative feedback. Older adults responded with less intense and less differentiated ACC activation, but FRN amplitudes did relate to error rate for the most difficult mazes. The feedback P3 was sensitive to negative feedback but played no role in the prediction of error for either group. These data reflect the selective age-related decline of ACC response but also its continued contribution to performance monitoring in aging.     

Approach‐motivated pregoal states enhance the reward positivity

Past work has demonstrated that the reward positivity (RewP) indexes a performance‐monitoring system sensitive to positive outcomes. However, studies have not investigated how approach‐motivated states occurring in goal pursuit influence performance monitoring. Using a modified monetary incentive delay task, participants played a reaction time game evoking approach‐motivated pregoal (reward trials) or neutral (no‐reward trials) states. Then, they received trial feedback resulting in monetary gain or no gain. Results revealed that the RewP was larger to win feedback on reward trials than win or no‐win feedback after neutral trials. P3 amplitudes were larger to infrequent feedback than frequent feedback, regardless of trial type or outcome. Furthermore, faster reaction times on reward trials related to larger RewP amplitudes after approach‐motivated pregoal states. Approach‐motivated pregoal states enhance RewP amplitudes for both successful and unsuccessful goal outcomes. Enhanced performance, as measured by faster reaction times, in approach‐motivated pregoal states relates to enhanced performance monitoring.     

Can event-related potentials serve as neural markers for wins,losses, and near-wins in a gambling task? A principal components analysis

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.     

Reward-Related Neural Activity and Adolescent Antisocial Behavior in a Community Sample

Behavioral research has found evidence supporting reward dominance in adolescence with externalizing disorders, but findings from neuroimaging studies have been largely heterogeneous. We examined the Feedback-Related Negativity (FRN) and P3b in relation to self-reported externalizing behavior among 78 adolescents (11–18 yrs) during a monetary gambling task with concurrent high-density electroencephalogram. As expected, the P3b and the FRN demonstrated greater evoked activity to reward and punishment, respectively. Further, high externalizing behavior was associated with greater P3b difference and reduced FRN difference in response to reward and punishment, suggesting that externalizing behaviors may be associated with both reward dominance and reduced feedback-monitoring.     

Impact of reward and punishment motivation on behavior monitoring as indexed by the error-related negativity

The error-related negativity (ERN) is thought to index a neural behavior monitoring system with its source in anterior cingulate cortex (ACC). While ACC is involved in a wide variety of cognitive and emotional tasks, there is debate as to what aspects of ACC function are indexed by the ERN. In one model the ERN indexes purely cognitive function, responding to mismatch between intended and executed actions. Another model posits that the ERN is more emotionally driven, elicited when an action is inconsistent with motivational goals. If the ERN indexes mismatch between intended and executed actions, then it should be insensitive to motivational valence, e.g. reward or punishment; in contrast if the ERN indexes the evaluation of responses relative to goals, then it might respond differentially under differing motivational valence. This study used a flanker task motivated by potential reward and potential punishment on different trials and also examined the N2 and P3 to the imperative stimulus, the response Pe, and the FRN and P3 to the outcome feedback to assess the impact of motivation valence on other stages of information processing in this choice reaction time task. Participants were slower on punishment motivated trials and both the N2 and ERN were larger on punishment motivated trials, indicating that loss aversion has an impact on multiple stages of information processing including behavior monitoring.     

Learning processes underlying avoidance of negative outcomes

Successful avoidance of a threatening event may negatively reinforce the behavior due to activation of brain structures involved in reward processing. Here, we further investigated the learning‐related properties of avoidance using feedback‐related negativity (FRN). The FRN is modulated by violations of an intended outcome (prediction error, PE), that is, the bigger the difference between intended and actual outcome, the larger the FRN amplitude is. Twenty‐eight participants underwent an operant conditioning paradigm, in which a behavior (button press) allowed them to avoid a painful electric shock. During two learning blocks, participants could avoid an electric shock in 80% of the trials by pressing one button (avoidance button), or by not pressing another button (punishment button). After learning, participants underwent two test blocks, which were identical to the learning ones except that no shocks were delivered. Participants pressed the avoidance button more often than the punishment button. Importantly, response frequency increased throughout the learning blocks but it did not decrease during the test blocks, indicating impaired extinction and/or habit formation. In line with a PE account, FRN amplitude to negative feedback after correct responses (i.e., unexpected punishment) was significantly larger than to positive feedback (i.e., expected omission of punishment), and it increased throughout the blocks. Highly anxious individuals showed equal FRN amplitudes to negative and positive feedback, suggesting impaired discrimination. These results confirm the role of negative reinforcement in motivating behavior and learning, and reveal important differences between high and low anxious individuals in the processing of prediction errors.     

Perceptual properties of feedback stimuli influence the feedback‐related negativity in the flanker gambling task

A negative deflection in the event‐related potential is enhanced following error‐ and loss‐related feedback in decision‐making and simple gambling tasks. Researchers have assumed that the perceptual properties of the feedback stimuli are unimportant in explaining these effects. This assumption was tested in the present study through a flanker gambling task, in which the perceptual properties of the feedback were manipulated. Consistent with previous studies, loss elicited a larger feedback‐related negativity (FRN) than gain feedback. However, this FRN reward effect was modulated by the perceptual properties of the feedback stimuli. When gain and loss feedback were perceptually similar to each other, the enhancement of the FRN following the loss feedback was smaller compared to when the gain and loss feedback were different from each other. In addition, incongruent feedback elicited a larger FRN than congruent feedback; this FRN congruency effect was larger following gain than loss feedback. These results suggested that perceptual properties of the feedback stimuli play a role in the elicitation of the FRN.     

Manipulation of feedback expectancy and valence induces negative and positive reward prediction error signals manifest in event-related brain potentials

The feedback-related negativity (FRN) has been hypothesized to be most sensitive to unexpected negative feedback. The present study investigated feedback expectancy and valence using a probabilistic gambling paradigm where subjects encountered expected or unexpected positive and negative feedback outcomes. In line with previous studies, FRN amplitude reflected a negative reward prediction error, but to a minor extent also a positive reward prediction error. Moreover, the P300 amplitude was largest after unexpected feedback, irrespective of valence. We propose to interpret the FRN in terms of a reinforcement learning signal which is detecting mismatch between internal and external representations indexed by the ACC to extract motivationally salient outcomes.     

Neural response to action and reward prediction errors: Comparing the error‐related negativity to behavioral errors and the feedback‐related negativity to reward prediction violations

The error‐related negativity (ERN) is thought to index an anterior cingulate (ACC) behavioral monitoring system. The feedback ERN (FRN) is elicited to error feedback when the correct response is not known, but also when a choice outcome is suboptimal and to passive reward prediction violation, suggesting that the monitoring system may not be restricted to actions. This study used principal components analysis to show that the ERN consists of a single central component whereas the reward prediction violation FRN is comprised of central and prefrontal components. A prefrontal component is also present in action monitoring but occurs later, at the error positivity latency. This suggests that ACC monitors both actions and events for reward prediction error. Prefrontal cortex may update reward expectation based on the prediction violation with the latency difference due to differential processing time for motor and perceptual information.     

Reward positivity: Reward prediction error or salience prediction error?

The reward positivity is a component of the human ERP elicited by feedback stimuli in trial‐and‐error learning and guessing tasks. A prominent theory holds that the reward positivity reflects a reward prediction error signal that is sensitive to outcome valence, being larger for unexpected positive events relative to unexpected negative events (Holroyd & Coles, 2002). Although the theory has found substantial empirical support, most of these studies have utilized either monetary or performance feedback to test the hypothesis. However, in apparent contradiction to the theory, a recent study found that unexpected physical punishments also elicit the reward positivity (Talmi, Atkinson, & El‐Deredy, 2013). The authors of this report argued that the reward positivity reflects a salience prediction error rather than a reward prediction error. To investigate this finding further, in the present study participants navigated a virtual T maze and received feedback on each trial under two conditions. In a reward condition, the feedback indicated that they would either receive a monetary reward or not and in a punishment condition the feedback indicated that they would receive a small shock or not. We found that the feedback stimuli elicited a typical reward positivity in the reward condition and an apparently delayed reward positivity in the punishment condition. Importantly, this signal was more positive to the stimuli that predicted the omission of a possible punishment relative to stimuli that predicted a forthcoming punishment, which is inconsistent with the salience hypothesis.     

A miss is as good as a mile? Processing of near and full outcomes in a gambling paradigm

Studies investigating the feedback‐related negativity (FRN) and the P300 following near misses, full misses, and wins have yielded inconsistent results. Furthermore, the P300 results were likely confounded by an oddball effect due to the probabilities of the different outcomes. We introduced a fourth outcome (narrow win), which allows for balanced outcome probabilities and thus rules out potential oddball effects. We measured the FRN and P300 as well as subjective ratings while participants were gambling on a wheel of fortune. The FRN was larger following misses compared to wins and larger following near compared to full outcomes. For the P300, we observed a larger positivity following wins compared to misses and full compared to near outcomes. These findings further corroborate that near and full outcomes are processed as distinct events even though they result in the same monetary outcomes.     

The feedback-related negativity reflects the binary evaluation of good versus bad outcomes

Electrophysiological studies have utilized event-related brain potentials to study neural processes related to the evaluation of environmental feedback. In particular, the feedback-related negativity (FRN) has been shown to reflect the evaluation of monetary losses and negative performance feedback. Two experiments were conducted to examine whether or not the FRN is sensitive to the magnitude of negative feedback. In both experiments, participants performed simple gambling tasks in which they could receive a range of potential outcomes on each trial. Relative to feedback indicating monetary gain, feedback indicating non-rewards was associated with a FRN in both experiments; however, the magnitude of the FRN did not demonstrate sensitivity to the magnitude of non-reward in either experiment. These data suggest that the FRN reflects the early appraisal of feedback based on a binary classification of good versus bad outcomes. These data are discussed in terms of contemporary theories of the FRN, as well as appraisal processes implicated in emotional processing.     

Expectancy affects the feedback‐related negativity (FRN) for delayed feedback in probabilistic learning

Learning from feedback is a prerequisite for adapting to the environment. Prediction error signals coded by midbrain dopamine (DA) neurons are projected to the basal ganglia and anterior cingulate cortex (ACC). It has been suggested that neuronal activity shifts away from the DA system when feedback is delayed. The feedback‐related negativity (FRN), an ERP that is generated in the ACC and has been shown to be sensitive to feedback valence and prediction error magnitude, was found to be reduced for delayed feedback. It has, however, not yet been investigated if the FRN for delayed feedback reflects a reward prediction error. In this study, effects of feedback delay (1 s vs. 7 s) on the processing of expected and unexpected positive and negative feedback were investigated in a between‐subjects design in healthy human participants conducting a probabilistic feedback learning task. FRN and P300 amplitudes were decreased for subjects learning from delayed compared to immediate feedback. Importantly, the FRN, extracted from the negative‐positive feedback difference wave, was significantly smaller for expected compared to unexpected feedback for both the immediate and delayed feedback conditions. Expectancy effects for the P300 were also seen, but did not interact with feedback valence. These results demonstrate an influence of feedback expectancy, and thus the prediction error, on early feedback processing even for delayed feedback, suggesting that neuronal structures underlying feedback processing are comparable for immediate and delayed feedback, at least to some extent. Modulations of the P300 by feedback delay may be linked to feedback salience.     

Goal relevance influences performance monitoring at the level of the FRN and P3 components

The feedback‐related negativity (FRN) provides a reliable ERP marker of performance monitoring (PM). It is usually larger for negative compared to positive feedback, and for unexpected relative to expected feedback. In two experiments, we assessed whether these effects could be modulated by goal relevance, defined as feedback informativeness (reliability) and/or impact on a person's goals. EEG (64‐channel) was recorded while 30 participants (in each experiment) performed a speeded go/no‐go task across blocks in which the feedback on task performance was deemed either relevant or not. At the ERP level, the FRN component was larger for (frequent) negative compared to (deviant) positive feedback exclusively when the feedback was relevant (Experiment 1). When the probability of positive and negative feedback was balanced (Experiment 2), this valence‐driven FRN effect was absent. However, across these two experiments, the FRN was always larger for irrelevant than relevant feedback. Moreover, the subsequent P300 component was larger for feedback in the relevant than the irrelevant blocks. This effect was valence unspecific in Experiment 1, while in Experiment 2 larger P3 amplitudes were recorded for negative than positive (relevant) feedback. Across the two experiments, a larger correct‐related negativity in the irrelevant than relevant context was also observed, suggesting that PM is flexible. These ERP findings indicate that goal relevance influences feedback (and response) processing during PM, with two nonoverlapping neurophysiological effects: It gates reward prediction error brain mechanisms (FRN effect), before enhancing subsequent motivational processes (P300 effect).     

Reward‐related neural dysfunction across depression and impulsivity: A dimensional approach

Recent theoretical models underline reward sensitivity as a potential endophenotype for major depressive disorder. Neural and behavioral evidence reveals depression is associated with reduced reward sensitivity. However, reward dysfunction is not unique to depression, as it is also common across disorders of poor impulse control. We examined the interrelationships of depression (Depression, Anxiety, and Stress Scale [DASS‐21]) and impulsivity (UPPS‐P Impulsive Behavior Scale) with reward sensitivity among a large, representative sample (N = 260). ERPs were recorded to isolate two neural indicators of consummatory reward processing: initial evaluation of rewards in the 250–350 ms time window postonset of feedback (reward positivity [RewP]), and salience to monetary outcomes (P3). Significant interactions were observed between depression and impulsivity facets across these two stages of reward processing: depression and positive urgency predicted RewP amplitude to reward outcomes (win vs. loss); depression and one other impulsivity trait, (lack of) premeditation, predicted P3 amplitude to monetary outcomes. Conversely, high symptoms of depression were related to three biobehavioral profiles: (1) blunted RewP in conjunction with high positive urgency, (2) combination of blunted RewP and low (lack of) premeditation, and (3) blunted P3 to monetary wins/losses, in conjunction with low (lack of) premeditation. Findings illustrate that reward‐related dysfunctions may be optimally conceptualized when examining the interactions between dimensions of internalizing and externalizing psychopathology.     

Temporal prediction modulates the evaluative processing of “good” action feedback: An electrophysiological study

The present study aimed to investigate whether or not the evaluative processing of action feedback can be modulated by temporal prediction. For this purpose, we examined the effects of the predictability of the timing of action feedback on an ERP effect that indexed the evaluative processing of action feedback, that is, an ERP effect that has been interpreted as a feedback‐related negativity (FRN) elicited by “bad” action feedback or a reward positivity (RewP) elicited by “good” action feedback. In two types of experimental blocks, the participants performed a gambling task in which they chose one of two cards and received an action feedback that indicated monetary gain or loss. In fixed blocks, the time interval between the participant's choice and the onset of the action feedback was fixed at 0, 500, or 1,000 ms in separate blocks; thus, the timing of action feedback was predictable. In mixed blocks, the time interval was randomly chosen from the same three intervals with equal probability; thus, the timing was less predictable. The results showed that the FRN/RewP was smaller in mixed than fixed blocks for the 0‐ms interval trial, whereas there was no difference between the two block types for the 500‐ms and 1,000‐ms interval trials. Interestingly, the smaller FRN/RewP was due to the modulation of gain ERPs rather than loss ERPs. These results suggest that temporal prediction can modulate the evaluative processing of action feedback, and particularly good feedback, such as that which indicates monetary gain.