Discrepancy between feedback negativity and subjective evaluation in gambling

Feedback negativity is a negative event-related potential elicited by feedback indicating incorrect performance or monetary loss. It is unclear whether this negativity is elicited by neutral feedback (e.g. a draw in gambling) or is affected by the subjective rating of punishment. To investigate these issues, we performed a modified and computerized game of 'rock-paper-scissors' as a gambling task and measured feedback negativity in response to feedback indicating the outcome, which was accompanied by a monetary reward. The data demonstrated that feedback negativity was elicited not only by a monetary loss but also by an even outcome and was independent of the magnitude of monetary loss. Our results suggest feedback negativity is not always specific to both monetary loss and subjective rating of punishment.     

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.     

Neural correlates of error detection and correction in a semantic retrieval task

Event-related potentials (ERPs) were used to investigate the cognitive and neural substrates of immediate and 1-week delayed error correction in a semantic retrieval task. In particular, we pursued the basis for the 'hypercorrection' effect, the finding that erroneous responses endorsed as correct with high confidence are more likely than low-confidence errors to be corrected at retest. Presentation of negative, but not positive feedback about the accuracy of one's response elicited a fronto-central negativity, similar to the ERN, which was somewhat sensitive to the degree to which negative feedback violated expectation. A fronto-central positivity, similar to the novelty-P3/P3a, more generally indexed detection of a metamemory error, given that it was larger in conditions of high metamemory mismatch than in conditions of low metamemory mismatch, irrespective of absolute task accuracy. For errors, amplitude of the fronto-central positivity, but not the preceding negativity, was correlated with correction on an immediate retest. Thus, to the extent that the fronto-central positivity indexes an orienting response, this response appears to facilitate initial encoding processes, but does not play a key role in memory consolidation. In contrast, a broad, inferior-temporal negativity occurring 300-600 ms after presentation of the correct answer was sensitive to subsequent memory performance at both immediate and delayed retests, but only for answers containing familiar semantic information. This negativity may reflect processes involved in the formation of an association between the question and pre-existing semantic information.     

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.     

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.     

The influence of emotional words on sentence processing: Electrophysiological and behavioral evidence

Whereas most previous studies on emotion in language have focussed on single words, we investigated the influence of the emotional valence of a word on the syntactic and semantic processes unfolding during sentence comprehension, by means of event-related brain potentials (ERP). Experiment 1 assessed how positive, negative, and neutral adjectives that could be either syntactically correct or incorrect (violation of number agreement) modulate syntax-sensitive ERP components. The amplitude of the left anterior negativity (LAN) to morphosyntactic violations increased in negative and decreased in positive words in comparison to neutral words. In Experiment 2, the same sentences were presented but positive, negative, and neutral adjectives could be either semantically correct or anomalous given the sentence context. The N400 to semantic anomalies was not significantly affected by the valence of the violating word. However, positive words in a sentence seemed to influence semantic correctness decisions, also triggering an apparent N400 reduction irrespective of the correctness value of the word. Later linguistic processes, as reflected in the P600 component, were unaffected in either experiment. Overall, our results indicate that emotional valence in a word impacts the syntactic and semantic processing of sentences, with differential effects as a function of valence and domain.     

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.     

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.     

Negative affect induced by derogatory verbal feedback modulates the neural signature of error detection

The present study examines the influence of induced affective state on performance monitoring. The electroencephalogram was recorded while human participants engaged in a speeded choice-reaction time task commonly used to examine performance monitoring processes. Prior to the experiment, participants were randomly allocated to receive either encouraging or derogatory feedback during task execution. Feedback was based on each participant''s reaction times. Affective state was assessed prior and after the experiment with a state questionnaire. Although participants of both feedback groups loaded high on items describing tiredness in the state questionnaire, only those with derogatory feedback loaded higher on negative state items and lower on positive state items after completion of the experiment. The error-related negativity (ERN) as an index of performance monitoring was increased after derogatory feedback; this difference was not seen at the beginning of the experiment. Negative state correlated significantly with ERN amplitude. The error positivity, a later component following errors, did not differ between feedback groups. This study provides further evidence that changes in affective state influence how we monitor ongoing behavior.     

The effect of accomplishment and failure on P300 potentials evoked by neutral stimuli

The effects of emotional states of 'being successful' vs. 'being unsuccessful' were studied by measuring the P300 component of event-related potentials (ERPs). Nine subjects were instructed to reduce their P300 amplitude using feedback. Feedback was random but the relative probability of different signals created the situations of 'being successful' or 'being unsuccessful'. The probability of 'small' feedback was 0.7 in 'successful' and 0.15 in 'unsuccessful' trials. ERPs recorded without the feedback were used as a reference. Potentials, evoked by light stimuli in a standard 'odd-ball' procedure, were recorded from Fz, Cz and Pz scalp sites. The amplitudes of P300 components were reduced in 'unsuccessful' trials whereas in 'successful' trials they did not differ significantly from responses recorded without the feedback. There were no significant differences in peak latencies. These findings indicate that tonic emotional states affect the processing of neutral stimuli and that late components of ERPs can be useful indices in the analysis of these alterations. The results also indicate that the effects of positive and negative emotional states are not always reciprocal. Manipulated feedback is suggested as an useful model in the studies of emotions. Data can also facilitate the interpretation of the real feedback effects.     

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.     

Problem gamblers exhibit reward hypersensitivity in medial frontal cortex during gambling

Problem gambling (PG) is increasingly conceptualized as an addiction akin to substance abuse, rather than an impulse control disorder, however the mechanism of addiction remains unclear. Neuroimaging investigations have supported a “reward deficiency” hypothesis for PG by suggesting a blunted response to gambling, particularly in the striatum. Here we describe electrophysiological evidence of a hypersensitive response to gambling feedback in problem gamblers. Previous research in healthy participants has shown that feedback during gambling tasks triggers stereotypical neural responses including the Feedback-Related Mediofrontal Negativity (FRN), the feedback-related P300, and an increase in induced theta-band (4-8 Hz) power. We tested the theory that abnormal feedback processing characterizes brain activity in problem gamblers while gambling. EEG was recorded from non-gamblers and self-identified gamblers as they engaged in a computerized version of the Iowa Gambling Task. Feedback about valence (win vs. loss) triggered a FRN in both groups, but in gamblers this was preceded by an early-latency hypersensitive fronto-central difference to feedback. This early FRN was correlated with gambling severity and was localized to medial frontal cortex using distributed source imaging (CLARA). Gamblers also differed in responses to risk, showing a blunted P300 component and less EEG power in the theta band. Here we suggest that a more nuanced interpretation of reward deficiency is called for with respect to PG. For certain aspects of brain function, gamblers may exhibit hypersensitivity to reward feedback more akin to drug sensitization than reward deficiency. Our results also suggest that the neurologically normal brain employs dissociable systems in the processing of feedback from tasks involving risky decision making.     

Parental presence with encouragement alters feedback processing in preschoolers: An ERP study

External feedback plays an important role in adapting to the environment; however, feedback processing in preschoolers has not been fully understood. The present event-related brain potential (ERP) study sought to understand the influence of parental presence with encouragement on feedback processing by focusing on reward positivity (RewP: mean amplitude between 200–350 ms). Five-year-old children (N = 21) completed an animal search task both alone (the alone condition) and with a parent who offered words of encouragement (the with a parent condition). ERPs were recorded while they received negative and positive feedback. We found a larger RewP amplitude in response to positive feedback in the with a parent condition relative to in the alone condition. In addition, differences in RewP between positive and negative feedback were only observed in the with a parent condition. These findings suggest that everyday parental encouragement has the potential to promote differential positive and negative feedback processing possibly by enhancing the reward value of positive feedback.     

Processing of performance errors predicts memory formation: Enhanced feedback‐related negativities for corrected versus repeated errors in an associative learning paradigm

Learning from errors or negative feedback is crucial for adaptive behavior. FMRI studies have demonstrated enhanced anterior cingulate cortex activity for errors that were later corrected versus repeated errors even when a substantial delay between the error and the opportunity to correct was introduced. We aimed at identifying the electrophysiological correlates of these processes by investigating the feedback‐related negativity (FRN) and stimulus‐locked P3. Participants had to learn and recall the location of 2‐digit targets over consecutive rounds. Feedback was provided in two steps, first a color change indicated a correct or incorrect response (feedback phase) followed by presentation of the correct digit information (re‐encoding phase). Behaviorally, participants improved performance from the first to the third round. FRN amplitudes time‐locked to feedback were enhanced for corrected compared to repeated errors. The P3 in response to re‐encoding did not differ between the two error types. The finding that FRN amplitudes positively predicted memory performance is consistent with the idea that the FRN reflects prediction errors and the need for enhanced cognitive control. Interestingly, this happens early during feedback processing and not at a later time point when re‐encoding of correct information takes place. The prediction error signal reflected in the FRN is usually elicited by performance errors, but may thus also play a role in preparing/optimizing the system for memory formation. This supports the existence of a close link between action control and memory processes even when there is a substantial delay between error feedback and the opportunity to correct the error.     

Neural evidence for enhanced error detection in major depressive disorder

OBJECTIVE: Anomalies in error processing have been implicated in the etiology and maintenance of major depressive disorder. In particular, depressed individuals exhibit heightened sensitivity to error-related information and negative environmental cues, along with reduced responsivity to positive reinforcers. The authors examined the neural activation associated with error processing in individuals diagnosed with and without major depression and the sensitivity of these processes to modulation by monetary task contingencies. METHOD: The error-related negativity and error-related positivity components of the event-related potential were used to characterize error monitoring in individuals with major depressive disorder and the degree to which these processes are sensitive to modulation by monetary reinforcement. Nondepressed comparison subjects (N=17) and depressed individuals (N=18) performed a flanker task under two external motivation conditions (i.e., monetary reward for correct responses and monetary loss for incorrect responses) and a nonmonetary condition. After each response, accuracy feedback was provided. The error-related negativity component assessed the degree of anomaly in initial error detection, and the error positivity component indexed recognition of errors. RESULTS: Across all conditions, the depressed participants exhibited greater amplitude of the error-related negativity component, relative to the comparison subjects, and equivalent error positivity amplitude. In addition, the two groups showed differential modulation by task incentives in both components. CONCLUSIONS: These data implicate exaggerated early error-detection processes in the etiology and maintenance of major depressive disorder. Such processes may then recruit excessive neural and cognitive resources that manifest as symptoms of depression.     

Learning-related changes in brain activity following errors and performance feedback in schizophrenia

In previous studies of self-monitoring in schizophrenia, patients have exhibited reductions in the amplitude of the error-related negativity (ERN), a component of the event-related brain potential (ERP) elicited most prominently immediately following the execution of incorrect responses. In the current study, we examined the ERN and a related component, the feedback negativity (FBN) in 26 schizophrenia outpatients and 27 psychiatrically healthy comparison subjects during a probabilistic learning task in which participants could learn stimulus-response pairs by attending to feedback indicating response accuracy. The validity of the feedback varied in three conditions. In one condition, accuracy feedback was entirely consistent (i.e., a left response to one of the stimuli in this condition was always correct and a right response was always incorrect). In the second condition, feedback was valid on only 80% of the trials, and in the third condition, accuracy feedback was random. Changes in ERP amplitudes accompanying learning of stimulus-response pairs were examined. Schizophrenia patients exhibited reduced ERN amplitude compared to healthy subjects in all conditions. This finding extends the previously reported impairment to include disruption of self-monitoring on a task in which participants learn stimulus-response mappings by trial and error, rather than being told the mappings explicitly. Schizophrenia patients also exhibited reduced FBN amplitude compared to healthy subjects in the 100% condition during early trials when the feedback was essential for accurate performance. These findings suggest that reward-related brain activity is weakened in schizophrenia, perhaps reflecting diminished sensitivity to whether ongoing events are better or worse than expected.     

Auditory P300 amplitude as a state marker for positive symptoms in schizophrenia: cross-sectional and retrospective longitudinal studies

The amplitude of the P300 component of the auditory event-related brain potential (ERP) is consistently reduced in schizophrenia. To determine whether this P300 abnormality can be used as a state marker to reflect the severity of symptoms, we examined both cross-sectionally and longitudinally the relationship between auditory P300 amplitude and symptom severity in patients with schizophrenia. For the cross-sectional study, ERP was elicited by an auditory oddball paradigm, and symptom severity was quantitatively measured by means of the Positive and Negative Syndrome Scale in 93 patients with schizophrenia or schizophreniform disorder (DSM-III-R). For the longitudinal study, ERP and psychopathology measured twice at an average interval of 238 days for 20 patients were retrospectively analyzed. The cross-sectional data showed that P300 amplitude correlated negatively with the positive but not with the negative syndrome scale score. The longitudinal data also showed a significant negative correlation between changes in P300 amplitude and in the positive syndrome scores of the first and second tests. In particular, P300 amplitude recorded at the left, but not right, posterior temporal region significantly correlated with the positive syndrome in both the cross-sectional and longitudinal studies. These findings support the hypotheses that auditory P300 amplitude recorded in the left hemisphere can be used as a state marker to reflect the severity of the positive symptoms and that the positive symptoms may be caused by a possible left-hemisphere deficit in schizophrenia.     

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.     

Influence of emotional words on human visual recognition and brain asymmetry.

To investigate the number of correct responses, the reaction time and the event-related brain potentials, effects of positive and negative verbal reinforcement on the visuo-spatial recognition of simple geometric figures, in condition of backward masking, were studied in healthy subjects and patients with chronic alcoholism. It was found that in performing the mental construction of geometrical figures from pairs of fragments, the number of correct responses by alcoholics, unlike the control group, was greater and the reaction time was lesser in the tests after positive verbal reinforcement than after negative verbal reinforcement. The latter in healthy subjects produce reduction of the latency and increase in the amplitude of N200-P300 potentials, particularly in the right parietal lobe. These changes were not observed in alcoholics. Moreover, negative verbal reinforcement, unlike positive, produced an emotional reaction, which underlay the worsening in recognition by alcoholics. The patients' lesser ability to perform the visuo-spatial tasks could be explained by the general reduction in the event-related potentials and the disappearance of the brain asymmetry. The verbal feedback mechanisms of reinforcement play an important role in the dynamic changes in the hemispheric lateralization of the human brain.     

Brain potentials related to self-generated and external information used for performance monitoring.

OBJECTIVE: Humans need to supervise and adjust their own behavior by means of an error detection and correction system as well as by using externally available information. The purpose of the present study was to compare the electrophysiological effects related to self-generated internal and to external (feedback) information used for performance monitoring. METHODS: Fourteen young normal subjects learned to associate each of several line-drawings with either a left-hand or right-hand response. In the experiment proper multi-channel ERPs were obtained time-locked to (a) the line-drawings, (b) the button-press, and (c) subsequent feedback stimuli. Feedback was either affirmative, negative, or equivocal. Event-related potentials were quantified and statistically evaluated using standard methodology. RESULTS: Response-locked ERPs showed a typical error-related negativity (ERN) for erroneous responses. ERPs to negative and equivocal feedback stimuli contained a negativity with a more posterior distribution than that of the ERN, which occurred earlier and had a higher peak amplitude in the equivocal condition. Dipole modeling suggests that this feedback-related negativity is generated by medial prefrontal and posterior cingulate cortex areas. CONCLUSIONS: Different brain systems support the use of internal and external information necessary for performance monitoring and modification. SIGNIFICANCE: The flexible use of internal and external information for performance control is a core executive function. The delineation of the corresponding brain correlates will further our understanding of executive dysfunction in neurological disorders.