It is less than you expected: The feedback-related negativity reflects violations of reward magnitude expectations

The anterior cingulate cortex (ACC) is involved in performance monitoring and in learning from performance feedback. Recent research suggests that the feedback-related negativity (FRN), an event-related potentials (ERP) component reflecting neural activity in the ACC, codes the size of a negative prediction error when reward probabilities are varied. There is as yet no clear evidence that the FRN is also sensitive to violations of reward magnitude expectations. In the present study, 20 healthy young subjects engaged in a learning task in which a coin had to be found on each trial. The value of the coin (the potential reward magnitude) was varied from trial to trial and amounted to 5 cent, 20 cent or 50 cent. Analysis of ERPs revealed that FRN amplitude differences between reward and non-reward were significantly modulated by (potential) reward magnitude. This effect was driven by the neural response to non-reward: the larger the potential reward, the larger was the FRN amplitude in response to non-reward. In contrast, the P300 was larger for positive outcomes and showed an effect of (potential) reward magnitude independent of valence. Together with evidence from previous studies, these results show that the FRN codes negative prediction errors in the context of varying reward probabilities and magnitudes. The findings are in line with recent results based on functional neuroimaging and lend further support to the idea of a key role of the ACC in the integration of information on different aspects of performance outcomes.     

Feedback and reward processing in high-functioning autism

Individuals with high-functioning autism often display deficits in social interactions and high-level cognitive functions. Such deficits may be influenced by poor ability to process feedback and rewards. The feedback-related negativity (FRN) is an event-related potential (ERP) that is more negative following losses than gains. We examined FRN amplitude in 25 individuals with Autism Spectrum Disorder (ASD) and 25 age- and IQ-matched typically developing control participants who completed a guessing task with monetary loss/gain feedback. Both groups demonstrated a robust FRN that was more negative to loss trials than gain trials; however, groups did not differ in FRN amplitude as a function of gain or loss trials. N1 and P300 amplitudes did not differentiate groups. FRN amplitude was positively correlated with age in individuals with ASD, but not measures of intelligence, anxiety, behavioral inhibition, or autism severity. Given previous findings of reduced-amplitude error-related negativity (ERN) in ASD, we propose that individuals with ASD may process external, concrete, feedback similar to typically developing individuals, but have difficulty with internal, more abstract, regulation of performance.     

Mediofrontal negativities in the absence of responding

The feedback-related negativity (FRN) is an event-related brain potential component that is elicited by feedback stimuli indicating unfavorable outcomes. Until recently, the FRN has been studied primarily using experimental paradigms in which outcomes appeared to be contingent upon the participants' behavior. The present study further addressed the question whether an FRN can be elicited by outcomes that are not contingent on any preceding choice or action. Participants took part in a simple slot-machine task in which they experienced monetary gains and losses in the absence of responses. In addition, they performed a time estimation task often used to study the FRN and a flanker task known to elicit the error-related negativity. Outcomes in the slot-machine task elicited an FRN-like mediofrontal negativity whose amplitude correlated with the amplitude of the FRN associated with negative feedback in the time estimation task. However, the mediofrontal negativity was observed both for (unfavorable) outcomes that averted a gain and for (favorable) outcomes that averted a loss of money. The results are discussed in the framework of current conceptions of the FRN and related electrophysiological components.     

The feedback-related negativity is modulated by feedback probability in observational learning

The feedback-related negativity (FRN), an event-related potentials (ERPs) component reflecting activity of the anterior cingulate cortex (ACC), has been shown to be modulated by feedback expectancy following active choices in feedback-based learning tasks. A general reduction of FRN amplitude has been described in observational feedback learning, raising the question whether FRN amplitude is modulated in a similar way in this type of learning. The present study investigated whether the FRN and the P300 - a second ERP component related to feedback processing - are modulated by feedback probability in observational learning. Thirty-two subjects participated in the experiment. They observed a virtual person choosing between two symbols and receiving positive or negative feedback. Learning about stimulus-specific feedback probabilities was assessed in active test trials without feedback. In addition, the bias to learn from positive or negative feedback and - in a subsample of 17 subjects - empathy scores were obtained. General FRN and P300 modulations by feedback probability were found across all subjects. Only for the FRN in learners, an interaction between probability and valence was observed. Larger FRN amplitudes for negative relative to positive feedback only emerged for the lowest outcome probability. The results show that feedback expectancy modulates FRN amplitude also in observational learning, suggesting a similar ACC function as in active learning. On the other hand, the modulation is only seen for very low feedback expectancy, which suggests that brain regions other than those of the reward system contribute to feedback processing in an observation setting.     

Individual differences in reward–prediction–error: extraversion and feedback-related negativity

Medial frontal scalp-recorded negativity occurring ∼200–300 ms post-stimulus [known as feedback-related negativity (FRN)] is attenuated following unpredicted reward and potentiated following unpredicted non-reward. This encourages the view that FRN may partly reflect dopaminergic ‘reward–prediction–error’ signalling. We examined the influence of a putatively dopamine-based personality trait, extraversion (N = 30), and a dopamine-related gene polymorphism, DRD2/ANKK1 (N = 24), on FRN during an associative reward-learning paradigm. FRN was most negative following unpredicted non-reward and least-negative following unpredicted reward. A difference wave contrasting these conditions was significantly more pronounced for extraverted participants than for introverts, with a similar but non-significant trend for participants carrying at least one copy of the A1 allele of the DRD2/ANKK1 gene compared with those without the allele. Extraversion was also significantly higher in A1 allele carriers. Results have broad relevance to neuroscience and personality research concerning reward processing and dopamine function.     

Learning-related changes in reward expectancy are reflected in the feedback-related negativity

The feedback-related negativity (FRN) has been hypothesized to be linked to reward-based learning. While many studies have shown that the FRN only occurs in response to unexpected negative outcomes, the relationship between the magnitude of negative prediction errors and FRN amplitude remains a matter of debate. The present study aimed to elucidate this relationship with a new behavioural procedure that allowed subjects to predict precise reward probabilities by learning an explicit rule. Insight into the rule did not only influence subjects' choice behaviour, but also outcome-related event-related potentials. After subjects had learned the rule, the FRN amplitude difference between non-reward and reward mirrored the magnitude of the negative prediction error, i.e. it was larger for less likely negative outcomes. Source analysis linked this effect to the anterior cingulate cortex. P300 amplitude was also modulated by outcome valence and expectancy. It was larger for positive and unexpected outcomes. It remains to be clarified, however, whether the P300 reflects a positive prediction error.     

To do or not to do? Action enlarges the FRN and P300 effects in outcome evaluation

Behavioral studies demonstrate that the outcome following an individual's action evokes stronger emotional responses than the same outcome following inaction. Here we use the event-related potential (ERP) technique to investigate how action affects the brain activity in outcome evaluation. In a gambling task, participants were asked to select a box from three boxes containing monetary reward and then to decide whether they would change their initial choice (i.e., action) or not (i.e., inaction). The feedback-related negativity (FRN), an evoked potential that peaks approximately 250 ms after receipt of feedback information, showed a larger differential effect between loss and win following action than following inaction. Similarly, the P300 showed a larger differential effect following action than following inaction, but now with the responses more positive to the win feedback than to the loss feedback. These results suggest that action may increase the expectancy towards the outcome and/or the motivational/emotional significance of the outcome, and that this action effect can be found in both the FRN and the P300 electrophysiological responses.     

Event-related components of the punishment and reward sensitivity

ObjectiveThe present study investigated the properties of feedback-related negativity (FRN) and P3 component of the event-related potentials (ERPs) and their neural sources localization as neurocognitive correlates of the behavioural inhibition and behavioural activation systems (BIS/BAS). The association between BIS/BAS function and anterior cortical asymmetry was tested.MethodsFifty right-handed women were investigated with 30-channel recordings during an instrumental Go/No-Go learning task. ERPs were elicited to feedback signals indicating monetary losses and monetary gains. Learning performance, FRN, and P3 amplitude and latency measures were calculated and related to BIS and BAS measures by means of ANOVA and correlation analysis. The neural sources of FRN and P3 components of the ERPs were estimated using LORETA software. A resting EEG-alpha-power (8–13 Hz) asymmetry measure was obtained.ResultsHigh levels of Reward Responsiveness (RR), a first order factor of the BAS, were associated with shorter RTs and enhanced positive feelings. The FRN was larger to signals indicating monetary Loss as compared to monetary Gain and enhanced with higher BIS and individual learning ability. Higher RR scores were related to greater left-sided resting frontal cortical asymmetry associated with approach orientation. High-RR subjects, as compared to Low-RR ones, had a smaller P3 amplitude for Go/Loss signals. The P3 latency to No-Go/Gain signals was the best positive predictor of RR. LORETA source localization for the FRN component displayed significantly higher brain electrical activity in left-fusiform gyrus and right superior temporal gyrus to monetary Loss in comparison to monetary Gain after incorrect No-Go responses. For the P3 wave, the monetary Loss produced significantly higher activations in the left superior parietal lobule, right postcentral gyrus, and in the ACC.ConclusionThe FRN was sensitive to cues of punishment and higher BIS was uniquely related to a larger FRN amplitude on No-Go/Loss trials, linking BIS with conflict monitoring and sensitivity to No-Go cues. Furthermore, the significant interaction found between BIS and RR on FRN amplitude together with the findings linking High-RR levels with shorter RTs, smaller P3 amplitudes and enhanced positive feelings are in line with the hypothesis that both BIS and BAS have the potential to influence punishment-mediated and reward-mediated behaviour.SignificanceResults open up new perspectives for future investigations on the relationship between BIS/BAS measures and ERP components to monetary reward during learning.     

Attitude toward money modulates outcome processing: An ERP study

Love of money (LOM) is concerned with the attitude toward money, which can be measured by the LOM scale through affective, behavioral, and cognitive dimensions. Research has observed that monetary attitude was tightly related to reward processing and could affect economic behavior. This study examined how monetary attitude modulated risky behavior and the underlying neural mechanisms of reward processing using event-related potential (ERP) technique. We compared both the risk level and brain responses of a high-level LOM (HLOM) group to a low-level LOM (LLOM) group using a simple gambling task. The behavioral results showed that the HLOM group was more risky than the LLOM group, particularly after loss. The feedback-related negativity (FRN) was measured as the difference wave (gain-related ERP was subtracted from loss-related ERP). The FRN difference wave was larger in the HLOM group than that in the LLOM group. The P3 in the HLOM group was more positive than that in the LLOM group. These results suggest that monetary attitude can modulate both the underlying neural mechanisms and behavioral performance in a reward-related task. The HLOM participants are more sensitive to gain/loss than the LLOM participants.     

Rapid electrophysiological brain responses are influenced by both valence and magnitude of monetary rewards

Abstract Negative outcomes, as identified from external feedback, cause a short-latency negative deflection in the event-related potential (ERP) waveform over medial frontal electrode sites. This brain response, which has been called an "error related negativity" (ERN) or "medial frontal negativity" (MFN), may reflect a coarse evaluation of performance outcomes, such as the valence of a reward within a monetary gambling task. Yet, for feedback to lead to the adaptive control of behavior, other information concerning reward outcomes besides experienced valence may also be important. Here, we used a gambling task in which subjects chose between two options that could vary in both outcome valence (gain or loss) and outcome magnitude (larger or smaller). We measured changes in brain ERP responses associated with the presentation of the outcomes. We found, as shown in prior studies, that valence of the chosen outcome has an early effect upon frontal ERPs, with maximal difference observed at approximately 250 msec. However, our results demonstrated that the early ERP responses to outcome feedback were driven not just by valence but by the combination of valence and magnitude for both chosen and unchosen options. Beginning even earlier, at around 150 msec, responses to high-consequence outcomes resulted in a greater, more centrally distributed, positive potential than those involving low-consequence outcomes, independent of valence. Furthermore, the amplitude of these early effects was significantly modulated by the sequence of outcomes in previous trials. These results indicate that early evaluation of feedback goes beyond simple identification of valence-it involves the consideration of multiple factors, including outcome magnitude, context of unchosen options, and prior history.     

The rewarding value of good motor performance in the context of monetary incentives

Whether an agent receives positive task feedback or a monetary reward, neural activity in their striatum increases. In the latter case striatal activity reflects extrinsic reward processing, while in the former, striatal activity reflects the intrinsically rewarding effects of performing well. There can be a "hidden cost of reward", which is a detrimental effect of extrinsic on intrinsic reward value. This raises the question how these two types of reward interact. To address this, we applied a monetary incentive delay task: in all trials participants received feedback depending on their performance. In half of the trials they could additionally receive monetary reward if they performed well. This resulted in high performance trials, which were monetarily rewarded and high performance trials that were not. This made it possible to dissociate the neural correlates of performance feedback from the neural correlates of monetary reward that comes with high performance. Performance feedback alone elicits activation increases in the ventral striatum. This activation increases due to additional monetary reward. Neural response in the dorsal striatum on the other hand is only significantly increased by feedback when a monetary incentive is present. The quality of performance does not significantly influence dorsal striatum activity. In conclusion, our results indicate that the dorsal striatum is primarily sensitive to optional or actually received external rewards, whereas the ventral striatum may be coding intrinsic reward due to positive performance feedback. Thus the ventral striatum is suggested to be involved in the processing of intrinsically motivated behavior.     

Telling good from bad news: ADHD differentially affects processing of positive and negative feedback during guessing

Neuroimaging studies on ADHD suggest abnormalities in brain regions associated with decision-making and reward processing such as the anterior cingulate cortex (ACC) and orbitofrontal cortex. Recently, event-related potential (ERP) studies demonstrated that the ACC is involved in processing feedback signals during guessing and gambling. The resulting negative deflection, the 'feedback-related negativity' (FRN) has been interpreted as reflecting an error in reward prediction. In the present study, ERPs elicited by positive and negative feedback were recorded in children with ADHD and normal controls during guessing. 'Correct' and 'incorrect' guesses resulted in respectively monetary gains and losses. The FRN amplitude to losses was more pronounced in the ADHD group than in normal controls. Positive and negative feedback differentially affected long latency components in the ERP waveforms of normal controls, but not ADHD children. These later deflections might be related to further emotional or strategic processing. The present findings suggest an enhanced sensitivity to unfavourable outcomes in children with ADHD, probably due to abnormalities in mesolimbic reward circuits. In addition, further processing, such as affective evaluation and the assessment of future consequences of the feedback signal seems to be altered in ADHD. These results may further help understanding the neural basis of decision-making deficits in ADHD.     

Outcome Prediction in Moderate and Severe Traumatic Brain Injury: A Focus on Computed Tomography Variables

Background

With this study we aimed to design validated outcome prediction models in moderate and severe traumatic brain injury (TBI) using demographic, clinical, and radiological parameters.

Methods

Seven hundred consecutive moderate or severe TBI patients were included in this observational prospective cohort study. After inclusion, clinical data were collected, initial head computed tomography (CT) scans were rated, and at 6 months outcome was determined using the extended Glasgow Outcome Scale. Multivariate binary logistic regression analysis was applied to evaluate the association between potential predictors and three different outcome endpoints. The prognostic models that resulted were externally validated in a national Dutch TBI cohort.

Results

In line with previous literature we identified age, pupil responses, Glasgow Coma Scale score and the occurrence of a hypotensive episode post-injury as predictors. Furthermore, several CT characteristics were associated with outcome; the aspect of the ambient cisterns being the most powerful. After external validation using Receiver Operating Characteristic (ROC) analysis our prediction models demonstrated adequate discriminative values, quantified by the area under the ROC curve, of 0.86 for death versus survival and 0.83 for unfavorable versus favorable outcome. Discriminative power was less for unfavorable outcome in survivors: 0.69.

Conclusions

Outcome prediction in moderate and severe TBI might be improved using the models that were designed in this study. However, conventional demographic, clinical and CT variables proved insufficient to predict disability in surviving patients. The information that can be derived from our prediction rules is important for the selection and stratification of patients recruited into clinical TBI trials.     

Detecting perceptual conflict by the feedback-related negativity in brain potentials

The feedback-related negativity (FRN) in brain potentials is typically observed for the outcome evaluation concerning one's performance or monetary reward. Using a task in which the participant guesses whether the first stimulus (S1) would have the same color as the subsequently presented second stimulus (S2), this study demonstrates that the FRN to S2, which serves as feedback to the guessing, is also sensitive to the conflict between perceptual representations of S1 and S2 in working memory. The FRN effect for the feedback concerning the correctness of one's performance is modulated by the congruency between perceptual properties of the stimuli. The anterior cingulate cortex, which generates the FRN, is thus a general conflict-monitoring device detecting both response and perceptual conflicts.     

Learning from experience: Event-related potential correlates of reward processing, neural adaptation, and behavioral choice

To behave adaptively, we must learn from the consequences of our actions. Studies using event-related potentials (ERPs) have been informative with respect to the question of how such learning occurs. These studies have revealed a frontocentral negativity termed the feedback-related negativity (FRN) that appears after negative feedback. According to one prominent theory, the FRN tracks the difference between the values of actual and expected outcomes, or reward prediction errors. As such, the FRN provides a tool for studying reward valuation and decision making. We begin this review by examining the neural significance of the FRN. We then examine its functional significance. To understand the cognitive processes that occur when the FRN is generated, we explore variables that influence its appearance and amplitude. Specifically, we evaluate four hypotheses: (1) the FRN encodes a quantitative reward prediction error; (2) the FRN is evoked by outcomes and by stimuli that predict outcomes; (3) the FRN and behavior change with experience; and (4) the system that produces the FRN is maximally engaged by volitional actions.     

Error-related negativity reflects detection of negative reward prediction error

Error-related negativity (ERN) is a negative deflection in the event-related potential elicited in error trials. To examine the function of ERN, we performed an experiment in which two within-participants factors were manipulated: outcome uncertainty and content of feedback. The ERN was largest when participants expected correct feedback but received error feedback. There were significant positive correlations between the ERN amplitude and the rate of response switching in the subsequent trial, and between the ERN amplitude and the trait version score on negative affect scale. These results suggest that ERN reflects detection of a negative reward prediction error and promotes subsequent response switching, and that individuals with high negative affect are hypersensitive to a negative reward prediction error.     

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

Event-related potential studies of reward processing have consistently identified the feedback negativity (FN), an early neural response that differentiates feedback indicating unfavorable versus favorable outcomes. Several important questions remain, however, about the nature of this response. In this study, the FN was recorded in response to monetary gains and losses during a laboratory gambling task, and temporospatial principal components analysis was used to separate the FN from overlapping responses. The FN was identified as a positive deflection at frontocentral recording sites that was enhanced for rewards compared with nonrewards. Furthermore, source localization techniques identified the striatum as a likely neural generator. These data indicate that this apparent FN reflects increased striatal activation in response to favorable outcomes that is reduced or absent for unfavorable outcomes, thereby providing unique information about the timing and nature of basal ganglia activity related to reward processing.     

Mentalizing in economic decision-making

In the Ultimatum Game, participants typically reject monetary offers they consider unfair even if the alternative is to gain no money at all. In the present study, ERPs were recorded while subjects processed different offers of a proposer. In addition to clearly fair and unfair offers, mid-value offers which cannot be easily classified as fair or unfair and therefore involve more elaborate decision making were analyzed. A fast initial distinction between fair and other kinds of offers was reflected by amplitude of the feedback related negativity (FRN). Mid-value offers were associated with longer RTs, and a larger N350 amplitude. In addition, source analyses revealed a specific involvement of the superior temporal gyrus and the inferior parietal lobule during processing of mid-value offers compared to offers categorized clearly as fair or unfair, suggesting a contribution of mentalizing about the intention of the proposer to the decision making process. Taken together, the present findings support the idea that economic decisions are significantly affected by non-rational factors, trying to narrow the gap between formal theory and the real decisional behaviour.     

Error processing in major depressive disorder: evidence from event-related potentials

In a previous study we showed that errors following errors activate a strategic (prefrontal) mechanism. In an error trial (trial n) following an erroneous previous trial (trial n - 1) healthy control subjects were found to have enlarged (more negative) amplitudes of the error related negativity (ERN)/error negativity (Ne), an electrophysiological correlate of response monitoring, in response to a negative feedback signal. Contrary to that, patients with major depressive disorder showed smaller (less negative) ERN/Ne amplitudes. It has been discussed controversially whether errors of choice (e.g., pressing an incorrect response button in an Eriksen flanker task) and errors of commission (e.g., pressing a button when one is not supposed to in a Go/Nogo task) are related to different ERN/Ne mechanisms. In the present study, we examined whether our previous result only holds for errors of choice in an Eriksen flankers task or extends to errors of commission in a Go/Nogo task, as well. Ten patients with DSM-IV major depressive disorder and 10 matched controls participated in a Go/Nogo task with performance feedback which signaled monetary reward. Patients with major depressive disorder again showed a less negative ERN/Ne amplitude in error trials following error trials. This result might reflect impaired response monitoring processes in major depressive disorder resulting from an impaired activation of a central reward pathway and/or a deficit in strategic reasoning.     

Feedback-related processes during a time-production task in young and older adults

ObjectiveWe examined whether the age-related decline in the integrity of the mid-brain dopamine system plays a role in the adaptation of precisely timed motor responses by feedback information.MethodsParticipants performed a time-production task with feedback given after each trial. They were encouraged to use the feedback for improving temporal response accuracy. Event-related potentials to the feedback were analyzed.ResultsOlder participants performed poorer than the young. Overall, high response accuracy was more favoured following positive than negative feedback. Older participants performed even worse after negative feedback than the younger. The feedback-related negativity (FRN) was of lower amplitude for older vs. young participants. FRN amplitude correlated significantly with response accuracy only for the young group.ConclusionsThe decreased response accuracy during time production of the older group may be related to a weakened fronto-striatal dopamine system and thus a reduced ability to use feedback information for improving temporal aspects of the motor response.SignificanceThe study points to difficulties especially for older participants to process error feedback, and it underlines the importance of positive feedback in order to improve temporal response accuracy. Suggestions can be drawn for the design of feedback information especially for older adults in motor learning environments.