Feedback-related Negativity Amplitude Research Articles

Feedback-related negativity is enhanced in adolescence during a gambling task with and without probabilistic reinforcement learning.

Feedback-related negativity (FRN) is a negative deflection that appears around 250 ms after the gain or loss of feedback to chosen alternatives in a gambling task in frontocentral regions following outcomes. Few studies have reported FRN enhancement in adolescents compared with adults in a gambling task without probabilistic reinforcement learning, despite the fact that learning from positive or negative consequences is crucial for decision-making during adolescence. Therefore, the aim of the present research was to identify differences in FRN amplitude and latency between adolescents and adults on a gambling task with favorable and unfavorable probabilistic reinforcement learning conditions, in addition to a nonlearning condition with monetary gains and losses. Higher rate scores of high-magnitude choices during the final 30 trials compared with the first 30 trials were observed during the favorable condition, whereas lower rates were observed during the unfavorable condition in both groups. Higher FRN amplitude in all conditions and longer latency in the nonlearning condition were observed in adolescents compared with adults and in relation to losses. Results indicate that both the adolescents and the adults improved their performance in relation to positive and negative feedback. However, the FRN findings suggest an increased sensitivity to external feedback to losses in adolescents compared with adults, irrespective of the presence or absence of probabilistic reinforcement learning. These results reflect processing differences on the neural monitoring system and provide new perspectives on the dynamic development of an adolescent's brain.

Context-sensitivity of the feedback-related negativity for zero-value feedback outcomes

The present study investigated whether the same visual stimulus indicating zero-value feedback (€0) elicits feedback-related negativity (FRN) variation, depending on whether the outcomes correspond with expectations or not.Thirty-one volunteers performed a monetary incentive delay (MID) task while EEG was recorded. FRN amplitudes were comparable and more negative when zero-value outcome deviated from expectations than with expected gain or loss, supporting theories emphasising the impact of unexpectedness and salience on FRN amplitudes. Surprisingly, expected zero-value outcomes elicited the most negative FRNs. However, source localisation showed that such outcomes evoked less activation in cingulate areas than unexpected zero-value outcomes.Our study illustrates the context dependency of identical zero-value feedback stimuli. Moreover, the results indicate that the incentive cues in the MID task evoke different reward prediction error signals. These prediction signals differ in FRN amplitude and neuronal sources, and have to be considered in the design and interpretation of future studies.

Probabilistic reward learning in adults with Attention Deficit Hyperactivity Disorder—An electrophysiological study

Attention Deficit Hyperactivity Disorder (ADHD) is hypothesized to be characterized by altered reinforcement sensitivity. The main aim of the present study was to assess alterations in the electrophysiological correlates of monetary reward processing in adult patients with ADHD of the combined subtype. Fourteen adults with ADHD of the combined subtype and 14 healthy control participants performed an active and an observational probabilistic reward-based learning task while an electroencephalogramm (EEG) was recorded. Regardless of feedback valence, there was a general feedback-related negativity (FRN) enhancement in combination with reduced learning performance during both active and observational reward learning in patients with ADHD relative to healthy controls. Other feedback-locked potentials such as the P200 and P300 and response-locked potentials were unaltered in the patients. There were no significant correlations between learning performance, FRN amplitudes and clinical symptoms, neither in the overall group involving all participants, nor in patients or controls considered separately. This pattern of findings might reflect generally impaired reward prediction in adults with ADHD of the combined subtype. We demonstrated for the first time that patients with ADHD of the combined subtype show not only deficient active reward learning but are also impaired when learning by observing other people׳s outcomes.

Reward and punishment hyposensitivity in problem gamblers: A study of event-related potentials using a principal components analysis

ObjectiveTo investigate whether the latent neural correlates of incentive processing differ between problem gamblers (PGs) and healthy controls (HCs). MethodsEvent-related potential (ERP) data were derived while 16 PGs and 20 HCs played a computer electronic gaming machine (EGM) task. Psychophysiological responses to outcomes commonly encountered during EGM gambling, including Large wins, Small wins, Near-wins, and Losses, were examined using a spatiotemporal principal components analysis (PCA). Subjects also completed questionnaires that assessed their levels of impulsivity, attraction to appetitive stimuli, and avoidance of aversive stimuli. ResultsLosses elicited a feedback-related negativity (FRN), whereas wins elicited a feedback-related positivity (FRP) at the same latency and topography. PGs exhibited both attenuated FRN amplitudes following Losses and FRP amplitudes following Wins. Greater P3b amplitudes were found following Wins compared to Losses. FRN amplitudes following Near-wins were significantly reduced compared to Losses for both PGs and HCs. Trends for reduced P3b amplitudes following all outcome types, and for similar P3b amplitudes following Large and Small wins, were found for the PG group. ConclusionsWe provide evidence that PGs are hyposensitive to both positive and negative outcomes. SignificanceThe finding that PGs are hyposensitive to reward and punishment provides valuable insight into the nature of deficit in this disorder, and provides a foundation for future research and clinical interventions.

From Feedback- to Response-based Performance Monitoring in Active and Observational Learning

Humans can adapt their behavior by learning from the consequences of their own actions or by observing others. Gradual active learning of action-outcome contingencies is accompanied by a shift from feedback- to response-based performance monitoring. This shift is reflected by complementary learning-related changes of two ACC-driven ERP components, the feedback-related negativity (FRN) and the error-related negativity (ERN), which have both been suggested to signal events "worse than expected," that is, a negative prediction error. Although recent research has identified comparable components for observed behavior and outcomes (observational ERN and FRN), it is as yet unknown, whether these components are similarly modulated by prediction errors and thus also reflect behavioral adaptation. In this study, two groups of 15 participants learned action-outcome contingencies either actively or by observation. In active learners, FRN amplitude for negative feedback decreased and ERN amplitude in response to erroneous actions increased with learning, whereas observational ERN and FRN in observational learners did not exhibit learning-related changes. Learning performance, assessed in test trials without feedback, was comparable between groups, as was the ERN following actively performed errors during test trials. In summary, the results show that action-outcome associations can be learned similarly well actively and by observation. The mechanisms involved appear to differ, with the FRN in active learning reflecting the integration of information about own actions and the accompanying outcomes.

Neural Correlates of Feedback Processing in Toddlers

External feedback provides essential information for successful learning. Feedback is especially important for learning in early childhood, as toddlers strongly rely on external signals to determine the consequences of their actions. In adults, many electrophysiological studies have elucidated feedback processes using a neural marker called the feedback-related negativity (FRN). The neural generator of the FRN is assumed to be the ACC, located in medial frontal cortex. As frontal brain regions are the latest to mature during brain development, it is unclear when in early childhood a functional feedback system develops. Is feedback differentiated on a neural level in toddlers and in how far is neural feedback processing related to children's behavioral adjustment? In an EEG experiment, we addressed these questions by measuring the brain activity and behavioral performance of 2.5-year-old toddlers while they played a feedback-guided game on a touchscreen. Electrophysiological results show differential brain activity for feedback with a more negative deflection for incorrect than correct outcomes, resembling the adult FRN. This provides the first neural evidence for feedback processing in toddlers. Notably, FRN amplitudes were predictive of adaptive behavior: the stronger the differential brain activity for feedback, the better the toddlers' adaptive performance during the game. Thus, already in early childhood toddlers' feedback-guided performance directly relates to the functionality of their neural feedback processing. Implications for early feedback-based learning as well as structural and functional brain development are discussed.

The effect of learning on feedback-related potentials in adolescents with dyslexia: an EEG-ERP study.

IntroductionIndividuals with dyslexia exhibit associated learning deficits and impaired executive functions. The Wisconsin Card Sorting Test (WCST) is a learning-based task that relies heavily on executive functioning, in particular, attention shift and working memory. Performance during early and late phases of a series within the task represents learning and implementation of a newly learned rule. Here, we aimed to examine two event-related potentials associated with learning, feedback-related negativity (FRN)-P300 complex, in individuals with dyslexia performing the WCST.MethodsAdolescents with dyslexia and age-matched typical readers performed the Madrid card sorting test (MCST), a computerized version of the WCST. Task performance, reading measures, and cognitive measures were collected. FRN and the P300 complex were acquired using the event-related potentials methodology and were compared in early vs late errors within a series.ResultsWhile performing the MCST, both groups showed a significant reduction in average reaction times and a trend toward decreased error rates. Typical readers performed consistently better than individuals with dyslexia. FRN amplitudes in early phases were significantly smaller in dyslexic readers, but were essentially equivalent to typical readers in the late phase. P300 amplitudes were initially smaller among readers with dyslexia and tended to decrease further in late phases. Differences in FRN amplitudes for early vs late phases were positively correlated with those of P300 amplitudes in the entire sample.ConclusionIndividuals with dyslexia demonstrate a behavioral and electrophysiological change within single series of the MCST. However, learning patterns seem to differ between individuals with dyslexia and typical readers. We attribute these differences to the lower baseline performance of individuals with dyslexia. We suggest that these changes represent a fast compensatory mechanism, demonstrating the importance of learning strategies on reading among individuals with dyslexia.

Feedback-Related Negativity in Children with Two Subtypes of Attention Deficit Hyperactivity Disorder

ObjectiveThe current model of ADHD suggests abnormal reward and punishment sensitivity, although differences in ADHD subgroups are unclear. This study aimed to investigate the effect of feedback valence (reward or punishment) and punishment magnitude (small or large) on Feedback-Related Negativity (FRN) and Late Positive Potential (LPP) in two subtypes of ADHD (ADHD-C and ADHD-I) compared to typically developing children (TD) during a children's gambling task.MethodsChildren with ADHD-C (n = 16), children with ADHD-I (n = 15) and typically developing children (n = 15) performed a children's gambling task under three feedback conditions: large losses, small losses and gains. FRN and LPP components in brain potentials were recorded and analyzed.ResultsIn TD children and children with ADHD-C, large loss feedback evoked more negative FRN amplitudes than small loss feedback, suggesting that brain sensitivity to the punishment and its magnitude is not impaired in children with ADHD-C. In contrast to these two groups, the FRN effect was absent in children with ADHD-I. The LPP amplitudes were larger in children with ADHD-C in comparison with those with ADHD-I, regardless of feedback valence and magnitude.ConclusionChildren with ADHD-C exhibit intact brain sensitivity to punishment similar to TD children. In contrast, children with ADHD-I are significantly impaired in neural sensitivity to the feedback stimuli and in particular, to punishment, compared to TD and ADHD-C children. Thus, FRN, rather than LPP, is a reliable index of the difference in reward and punishment sensitivity across different ADHD-subcategories.

Feedback Processing in Adolescence: An Event-Related Potential Study of Age and Gender Differences

Adolescence has frequently been characterized as a period of increased risk taking, which may be largely driven by maturational changes in neural areas that process incentives. To investigate age- and gender-related differences in reward processing, we recorded event-related potentials (ERPs) from 80 participants in a gambling game, in which monetary wins and losses were either large or small. We measured two ERP components: the feedback-related negativity (FRN) and the feedback P3 (fP3). The FRN was sensitive to the size of a win in both adult (aged 23-35 years) and adolescent (aged 13-17 years) males, but not in females. Small wins appeared to be less rewarding for males than for females, which may in part explain more approach-driven behavior in males in general. Furthermore, adolescent boys showed both delayed FRNs to high losses and less differentiation in FRN amplitude between wins and losses in comparison to girls. The fP3, which is thought to index the salience of the feedback at a more conscious level than the FRN, was also larger in boys than in girls. Taken together, these results imply that higher levels of risk taking that are commonly reported in adolescent males may be driven both by hypersensitivity to high rewards and insensitivity to punishment or losses.

Acute stress modulates feedback processing in men and women: differential effects on the feedback-related negativity and theta and beta power.

Sex-specific prevalence rates in mental and physical disorders may be partly explained by sex differences in physiological stress responses. Neural networks that might be involved are those underlying feedback processing. Aim of the present EEG study was to investigate whether acute stress alters feedback processing, and whether stress effects differ between men and women. Male and female participants performed a gambling task, in a control and a stress condition. Stress was induced by exposing participants to a noise stressor. Brain activity was analyzed using both event-related potential and time-frequency analyses, measuring the feedback-related negativity (FRN) and feedback-related changes in theta and beta oscillatory power, respectively. While the FRN and feedback-related theta power were similarly affected by stress induction in both sexes, feedback-related beta power depended on the combination of stress induction condition and sex. FRN amplitude and theta power increases were smaller in the stress relative to the control condition in both sexes, demonstrating that acute noise stress impairs performance monitoring irrespective of sex. However, in the stress but not in the control condition, early lower beta-band power increases were larger for men than women, indicating that stress effects on feedback processing are partly sex-dependent. Our findings suggest that sex-specific effects on feedback processing may comprise a factor underlying sex-specific stress responses.

External Error Monitoring in Subclinical Obsessive-Compulsive Subjects: Electrophysiological Evidence from a Gambling Task

BackgroundFeedback-related negativity (FRN) is believed to be an important electrophysiology index of “external” negative feedback processing. Previous studies on FRN in obsessive-compulsive (OC) individuals are scarce and controversial. In these studies, anxiety symptoms were not evaluated in detail. However, OC disorders have a number of radical differences from anxiety disorders. It is necessary to study FRN and its neuroanatomical correlates in OC individuals without anxious symptoms.MethodsA total of 628 undergraduate students completed an OC questionnaire. We chose 14 students who scored in the upper 10% and 14 students who scored in the lowest 10% without anxiety symptoms as a subclinical OC group (SOC) and a low obsessive-compulsive group (LOC). The students all performed the revised Iowa Gambling Task. We used the event-related potentials (ERP) and standardized low-resolution brain electromagnetic tomography (sLORETA) to track external negative feedback processing and its substrate in the brain.ResultsOur study revealed poorer decision-making ability and greater FRN amplitudes in SOC subjects compared with LOC controls. The SOC subjects displayed anterior prefrontal cortex (aPFC) hyperactivation during the loss feedback condition. Specifically, we found an intercorrelation of current source density during the loss condition between the dorsal anterior cingulate cortex (dACC) and aPFC in the LOC subjects but not in the SOC group.ConclusionsOur results support the notion that overactive external feedback error processing may reflect a candidate endophenotype of OC. We also provide important information on the dysfunction in the interaction between aPFC and dACC in populations with OC. Nevertheless, the findings support that OC may be distinguished from other anxiety disorders using a new electrophysiology perspective.

The dark side of monetary incentive

It was widely believed that incentives could effectively enhance the motivation of both students and employees. However, psychologists reported that extrinsic reward actually could undermine individuals' intrinsic motivation to a given interesting task, which challenged viewpoints from traditional incentive theories. Numerous studies have been carried out to test and explain the undermining effect; however, the neural basis of this effect is still elusive. Here, we carried out an electrophysiological study with a simple but interesting stopwatch task to explore to what extent the performance-based monetary reward undermines individuals' intrinsic motivation toward the task. The electrophysiological data showed that the differentiated feedback-related negativity amplitude toward intrinsic success failure divergence was prominently reduced once the extrinsic reward was imposed beforehand. However, such a difference was not observed in the control group, in which no extrinsic reward was provided throughout the experiment. Furthermore, such a pattern was not observed for P300 amplitude. Therefore, the current results indicate that extrinsic reward demotivates the intrinsic response of individuals toward success-failure outcome, which was reflected in the corresponding reduced motivational-related differentiated feedback-related negativity, but not in amplitude of P300.

Reduced feedback-related negativity amplitude elicited by social and non-social error feedback in traumatic brain injury patients compared with controls

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Feedback-related negativity codes outcome valence, but not outcome expectancy, during reversal learning

Optimal behavior depends on the ability to assess the predictive value of events and to adjust behavior accordingly. Outcome processing can be studied by using its electrophysiological signatures--that is, the feedback-related negativity (FRN) and the P300. A prominent reinforcement-learning model predicts an FRN on negative prediction errors, as well as implying a role for the FRN in learning and the adaptation of behavior. However, these predictions have recently been challenged. Notably, studies so far have used tasks in which the outcomes have been contingent on the response. In these paradigms, the need to adapt behavioral responses is present only for negative, not for positive feedback. The goal of the present study was to investigate the effects of positive as well as negative violations of expectancy on FRN amplitudes, without the usual confound of behavioral adjustments. A reversal-learning task was employed in which outcome value and outcome expectancy were orthogonalized; that is, both positive and negative outcomes were equally unexpected. The results revealed a double dissociation, with effects of valence but not expectancy on the FRN and, conversely, effects of expectancy but not valence on the P300. While FRN amplitudes were largest for negative-outcome trials, irrespective of outcome expectancy, P300 amplitudes were largest for unexpected-outcome trials, irrespective of outcome valence. These FRN effects were interpreted to reflect an evaluation along a good-bad dimension, rather than reflecting a negative prediction error or a role in behavioral adaptation. By contrast, the P300 reflects the updating of information relevant for behavior in a changing context.

Blocked versus randomized presentation modes differentially modulate feedback-related negativity and P3b amplitudes

ObjectiveElectrophysiological studies on feedback processing typically use a wide range of feedback stimuli which might not always be comparable. The current study investigated whether two indicators of feedback processing – feedback-related negativity (FRN) and P3b – differ for feedback stimuli with explicit (facial expressions) or assigned valence information (symbols). In addition, we assessed whether presenting feedback in either a trial-by-trial or a block-wise fashion affected these ERPs. MethodsEEG was recorded in three experiments while participants performed a time estimation task and received two different types of performance feedback. ResultsOnly P3b amplitudes varied consistently in response to feedback type for both presentation types. Moreover, the blocked feedback type presentation yielded more distinct FRN peaks, higher effect sizes, and a significant relation between FRN amplitudes and behavioral task performance measures. ConclusionBoth stimulus type and presentation mode may provoke systematic changes in feedback-related ERPs. The current findings point at important potential confounds that need to be controlled for when designing FRN or P3b studies. SignificanceStudies investigating P3b amplitudes using mixed types of stimuli have to be interpreted with caution. Furthermore, we suggest implementing a blocked presentation format when presenting different feedback types within the same experiment.

Active and observational reward learning in adults with autism spectrum disorder: relationship with empathy in an atypical sample

IntroductionAutism spectrum disorders (ASDs) are characterised by disturbances in social behaviour. A prevailing hypothesis suggests that these problems are related to deficits in assigning rewarding value to social stimuli. The present study aimed to examine monetary reward processing in adults with ASDs by means of event-related potentials (ERPs).MethodsTen individuals with mild ASDs (Asperger's syndrome and high-functioning autism) and 12 healthy control subjects performed an active and an observational probabilistic reward-learning task.ResultsBoth groups showed similar overall learning performance. With respect to reward processing, subjects with ASDs exhibited a general reduction in feedback-related negativity (FRN) amplitude, irrespective of feedback valence and type of learning (active or observational). Individuals with ASDs showed lower scores for cognitive empathy, while affective empathy did not differ between groups. Correlation analyses revealed that higher empathy (both cognitive and affective) negatively affected performance in observational learning in controls and in active learning in ASDs (only cognitive empathy). No relationships were seen between empathy and ERPs.ConclusionsReduced FRN amplitudes are discussed in terms of a deficit in fast reward processing in ASDs, which may indicate altered reward system functioning.

The feedback-related negativity (FRN) revisited: New insights into the localization, meaning and network organization

Changes in response contingencies require adjusting ones assumptions about outcomes of behaviors. Such adaptation processes are driven by reward prediction error (RPE) signals which reflect the inadequacy of expectations. Signals resembling RPEs are known to be encoded by mesencephalic dopamine neurons projecting to the striatum and frontal regions. Although regions that process RPEs, such as the dorsal anterior cingulate cortex (dACC), have been identified, only indirect evidence links timing and network organization of RPE processing in humans. In electroencephalography (EEG), which is well known for its high temporal resolution, the feedback-related negativity (FRN) has been suggested to reflect RPE processing. Recent studies, however, suggested that the FRN might reflect surprise, which would correspond to the absolute, rather than the signed RPE signals. Furthermore, the localization of the FRN remains a matter of debate.In this simultaneous EEG–functional magnetic resonance imaging (fMRI) study, we localized the FRN directly using the superior spatial resolution of fMRI without relying on any spatial constraint or other assumption. Using two different single-trial approaches, we consistently found a cluster within the dACC. One analysis revealed additional activations of the salience network. Furthermore, we evaluated the effect of signed RPEs and surprise signals on the FRN amplitude. We considered that both signals are usually correlated and found that only surprise signals modulate the FRN amplitude. Last, we explored the pathway of RPE signals using dynamic causal modeling (DCM). We found that the surprise signals are directly projected to the source region of the FRN. This finding contradicts earlier theories about the network organization of the FRN, but is in line with a recent theory stating that dopamine neurons also encode surprise-like saliency signals.Our findings crucially advance the understanding of the FRN. We found compelling evidence that the FRN originates from the dACC. Furthermore, we clarified the functional role of the FRN, and determined the role of the dACC within the RPE network. These findings should enable us to study the processing of surprise and adjustment signals in the dACC in healthy and also in psychiatric patients.

Empathy and feedback processing in active and observational learning

The feedback-related negativity (FRN) and the P300 have been related to the processing of one's own and other individuals' feedback during both active and observational learning. The aim of the present study was to elucidate the role of trait-empathic responding with regard to the modulation of the neural correlates of observational learning in particular. Thirty-four healthy participants completed an active and an observational learning task. On both tasks, the participants' aim was to maximize their monetary gain by choosing from two stimuli the one that showed the higher probability of reward. Participants gained insight into the stimulus-reward contingencies according to monetary feedback presented after they had made an active choice or by observing the choices of a virtual partner. Participants showed a general improvement in learning performance on both learning tasks. P200, FRN, and P300 amplitudes were larger during active, as compared with observational, learning. Furthermore, nonreward elicited a significantly more negative FRN than did reward in the active learning task, while only a trend was observed for observational learning. Distinct subcomponents of trait cognitive empathy were related to poorer performance and smaller P300 amplitudes for observational learning only. Taken together, both the learning performance and event-related potentials during observational learning are affected by different aspects of trait cognitive empathy, and certain types of observational learning may actually be disrupted by a higher tendency to understand and adopt other people's perspectives.

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.

Fearless Dominance and reduced feedback-related negativity amplitudes in a time-estimation task – Further neuroscientific evidence for dual-process models of psychopathy

Dual-process models of psychopathy postulate two etiologically relevant processes. Their involvement in feedback processing and its neural correlates has not been investigated so far. Multi-channel EEG was collected while healthy female volunteers performed a time-estimation task and received negative or positive feedback in form of signs or emotional faces. The affective-interpersonal factor Fearless Dominance, but not Self-Centered Impulsivity, was associated with reduced feedback-related negativity (FRN) amplitudes. This neural dissociation extends previous findings on the impact of psychopathy on feedback processing and further highlights the importance of distinguishing psychopathic traits and extending previous (neuroscientific) models of psychopathy.