Knowing good from bad: differential activation of human cortical areas by positive and negative outcomes

Previous research has identified a component of the event-related brain potential (ERP), the feedback-related negativity, that is elicited by feedback stimuli associated with unfavourable outcomes. In the present research we used event-related functional magnetic resonance imaging (fMRI) and electroencephalographic (EEG) recordings to test the common hypothesis that this component is generated in the caudal anterior cingulate cortex. The EEG results indicated that our paradigm, a time estimation task with trial-to-trial performance feedback, elicited a large feedback-related negativity (FRN). Nevertheless, the fMRI results did not reveal any area in the caudal anterior cingulate cortex that was differentially activated by positive and negative performance feedback, casting doubt on the notion that the FRN is generated in this brain region. In contrast, we found a number of brain areas outside the posterior medial frontal cortex that were activated more strongly by positive feedback than by negative feedback. These included areas in the rostral anterior cingulate cortex, posterior cingulate cortex, right superior frontal gyrus, and striatum. An anatomically constrained source model assuming equivalent dipole generators in the rostral anterior cingulate, posterior cingulate, and right superior frontal gyrus produced a simulated scalp distribution that corresponded closely to the observed scalp distribution of the FRN. These results support a new hypothesis regarding the neural generators of the FRN, and have important implications for the use of this component as an electrophysiological index of performance monitoring and reward processing.     

Enhanced negative feedback responses in remitted depression

Major depressive disorder (MDD) is characterized by hypersensitivity to negative feedback that might involve frontocingulate dysfunction. MDD patients exhibit enhanced electrophysiological responses to negative internal (errors) and external (feedback) cues. Whether this dysfunction extends to remitted depressed (RD) individuals with a history of MDD is currently unknown. To address this issue, we examined the feedback-related negativity in RD and control participants using a probabilistic punishment learning task. Despite equivalent behavioral performance, RD participants showed larger feedback-related negativities to negative feedback relative to controls; group differences remained after accounting for residual anxiety and depressive symptoms. The present findings suggest that abnormal responses to negative feedback extend to samples at increased risk for depressive episodes in the absence of current symptoms.     

Role of depressive symptoms in early adolescents' online emotional responding to a peer evaluation challenge

Background: Problems regulating emotions effectively (emotion dysregulation) are implicated in many psychological problems. Depression in particular has been increasingly conceptualized as a disorder of emotion regulation. Methods: This study examines the linkage between children's depressive symptoms and the activation and regulation of positive and negative affect in response to an manipulated peer evaluation outcome. Participants (N=142) aged 10–13 played a computer contest (“Survivor”) and were randomized to either a negative (i.e., receiving the lowest “likeability” score from a group of peer judges), a positive (i.e., highest score), or a neutral peer evaluation outcome. Positive and negative affect were assessed at baseline, immediately post‐feedback, and after a 5 min post‐feedback waiting period. Results: No linkage was observed between depressive symptoms and emotional activation in response to either success or failure feedback. Consistent with expectations, we observed a negative linkage between depressive symptoms and children's up‐regulation of positive affect subsequent to receiving negative peer feedback. No such linkage was observed for the maintenance of mood improvement over time. Conclusions: Results suggest that depressive symptoms in children are not linked with deficits or excesses in the overall magnitude of emotional reactivity. However, it appears that elevated depressive symptoms interfere with the ability to swiftly transition out of negative affective states. Depression and Anxiety, 2009. © 2008 Wiley‐Liss, Inc.     

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.     

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.     

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.     

Resting anterior cingulate activity and abnormal responses to errors in subjects with elevated depressive symptoms: a 128-channel EEG study

Depression has been associated with dysfunctional executive functions and abnormal activity within the anterior cingulate cortex (ACC), a region critically involved in action regulation. Prior research invites the possibility that executive deficits in depression may arise from abnormal responses to negative feedback or errors, but the underlying neural substrates remain unknown. We hypothesized that abnormal reactions to error would be associated with dysfunctional rostral ACC activity, a region previously implicated in error detection and evaluation of the emotional significance of events. To test this hypothesis, subjects with low and high Beck Depression Inventory (BDI) scores performed an Eriksen Flanker task. To assess whether tonic activity within the rostral ACC predicted post-error adjustments, 128-channel resting EEG data were collected before the task and analyzed with low-resolution electromagnetic tomography (LORETA) using a region-of-interest approach. High BDI subjects were uniquely characterized by significantly lower accuracy after incorrect than correct trials. Mirroring the behavioral findings, high BDI subjects had significantly reduced pretask gamma (36.5-44 Hz) current density within the affective (rostral; BA24, BA25, BA32) but not cognitive (dorsal; BA24', BA32') ACC subdivision. For low, but not high, BDI subjects pretask gamma within the affective ACC subdivision predicted post-error adjustments even after controlling for activity within the cognitive ACC subdivision. Abnormal responses to errors may thus arise due to lower activity within regions subserving affective and/or motivational responses to salient cues. Because rostral ACC regions have been implicated in treatment response in depression, our findings provide initial insight into putative mechanisms fostering treatment response.     

Feedback-related brain potential activity complies with basic assumptions of associative learning theory

Feedback-related negativity (FRN) is an ERP component that distinguishes positive from negative feedback. FRN has been hypothesized to be the product of an error signal that may be used to adjust future behavior. In addition, associative learning models assume that the trial-to-trial learning of cue-outcome mappings involves the minimization of an error term. This study evaluated whether FRN is a possible electrophysiological correlate of this error term in a predictive learning task where human subjects were asked to learn different cue-outcome relationships. Specifically, we evaluated the sensitivity of the FRN to the course of learning when different stimuli interact or compete to become a predictor of certain outcomes. Importantly, some of these cues were blocked by more informative or predictive cues (i.e., the blocking effect). Interestingly, the present results show that both learning and blocking affect the amplitude of the FRN component. Furthermore, independent analyses of positive and negative feedback event-related signals showed that the learning effect was restricted to the ERP component elicited by positive feedback. The blocking test showed differences in the FRN magnitude between a predictive and a blocked cue. Overall, the present results show that ERPs that are related to feedback processing correspond to the main predictions of associative learning models.     

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.     

Increased anterior cingulate cortex and hippocampus activation in Complex PTSD during encoding of negative words

Post-traumatic stress disorder (PTSD) is associated with impaired memory performance coupled with functional changes in brain areas involved in declarative memory and emotion regulation. It is not yet clear how symptom severity and comorbidity affect neurocognitive functioning in PTSD. We performed a functional magnetic resonance imaging (fMRI) study with an emotional declarative memory task in 28 Complex PTSD patients with comorbid depressive and personality disorders, and 21 healthy non-trauma-exposed controls. In Complex PTSD patients—compared to controls—encoding of later remembered negative words vs baseline was associated with increased blood oxygenation level dependent (BOLD) response in the left ventral anterior cingulate cortex (ACC) and dorsal ACC extending to the dorsomedial prefrontal cortex (dmPFC) together with a trend for increased left hippocampus activation. Patients tended to commit more False Alarms to negative words compared to controls, which was associated with enhanced left ventrolateral prefrontal and orbitofrontal cortex (vlPFC/OFC) responses. Severity of child abuse was positively correlated with left ventral ACC activity and severity of depression with (para) hippocampal and ventral ACC activity. Presented results demonstrate functional abnormalities in Complex PTSD in the frontolimbic brain circuit also implicated in fear conditioning models, but generally in the opposite direction, which may be explained by severity of the trauma and severity of comorbid depression in Complex PTSD.     

Different neural pathways to negative affect in youth with pediatric bipolar disorder and severe mood dysregulation

Questions persist regarding the presentation of bipolar disorder (BD) in youth and the nosological significance of irritability. Of particular interest is whether severe mood dysregulation (SMD), characterized by severe non-episodic irritability, hyper-arousal, and hyper-reactivity to negative emotional stimuli, is a developmental presentation of pediatric BD and, therefore, whether the two conditions are pathophysiologically similar. We administered the affective Posner paradigm, an attentional task with a condition involving blocked goal attainment via rigged feedback. The sample included 60 youth (20 BD, 20 SMD, and 20 controls) ages 8–17. Magnetoencephalography (MEG) examined neuronal activity (4–50 Hz) following negative versus positive feedback. We also examined reaction time (RT), response accuracy, and self-reported affect. Both BD and SMD youth reported being less happy than controls during the rigged condition. Also, SMD youth reported greater arousal following negative feedback than both BD and controls, and they responded to negative feedback with significantly greater activation of the anterior cingulate cortex (ACC) and medial frontal gyrus (MFG) than controls. Compared to SMD and controls, BD youth displayed greater superior frontal gyrus (SFG) activation and decreased insula activation following negative feedback. Data suggest a greater negative affective response to blocked goal attainment in SMD versus BD and control youth. This occurs in tandem with hyperactivation of medial frontal regions in SMD youth, while BD youth show dysfunction in the SFG and insula. Data add to a growing empirical base that differentiates pediatric BD and SMD and begin to elucidate potential neural mechanisms of irritability.     

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.     

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.     

Distress tolerance moderates the relationship between negative affect intensity with borderline personality disorder levels

A number of studies have suggested that negative emotionality and negative affect intensity play key roles in the development and maintenance of borderline personality disorder (BPD). However, more recent research indicates that one's response to affective discomfort may be an even more important variable in the pathogenesis of BPD than either negative emotionality or negative affect intensity per se. As such, the current study aimed to empirically test the moderating role of 2 well-validated laboratory measures of the ability to tolerate psychological distress (distress tolerance) in the relationship of negative emotionality and negative affect intensity with BPD levels. Results provide laboratory-based evidence for a moderating effect of distress tolerance on the relationship of negative emotionality and negative affect intensity with levels of BPD. Specifically, the 2 former variables were related to levels of BPD among those with low distress tolerance. The current results add support to existing developmental frameworks of BPD and suggest the importance of modifying one's response to affective distress along with levels of negative emotionality in treatment settings.     

Error-related hyperactivity of the anterior cingulate cortex in obsessive-compulsive disorder.

BACKGROUND: Hyperactivity of the anterior cingulate cortex (ACC) in patients with obsessive-compulsive disorder (OCD) has been shown to increase with symptom provocation and to normalize with treatment-induced symptom reduction. Although the functional significance of anterior cingulate involvement in OCD remains unknown, electrophysiological evidence has linked this region to error-processing abnormalities in patients with OCD. In this functional magnetic resonance imaging (fMRI) study, we sought to further localize error-processing differences within the ACC of OCD patients compared with healthy subjects. METHODS: Event-related fMRI data were collected for eight OCD patients and seven healthy subjects during the performance of a simple cognitive task designed to elicit errors but not OCD symptoms. RESULTS: Both OCD patients and healthy subjects demonstrated dorsal ACC activation during error commission. The OCD patients exhibited significantly greater error-related activation of the rostral ACC than comparison subjects. Activity in this region was positively correlated with symptom severity in the patients. CONCLUSIONS: Error-processing abnormalities within the rostral anterior cingulate occur in the absence of symptom expression in patients with OCD.     

Reward context sensitivity impairment following severe TBI: an event-related potential investigation.

Many rehabilitation protocols following traumatic brain injury (TBI) utilize reinforcement and reward to influence behavior and facilitate recovery; however, previous studies suggest survivors of severe TBI demonstrate impairments in contingency utilization and sensitivity. The precise neurobiological mechanisms underlying these deficits have not been thoroughly explored, but can be examined using the "feedback-related negativity" (FRN)--an event-related potential (ERP) component evoked following performance or response feedback (e.g., whether a monetary reward is obtained) with a larger FRN following unfavorable than favorable outcomes--particularly when unfavorable feedback occurs in the context of high reward probability. We examined ERPs elicited by favorable (monetary gain: "reward") and unfavorable (no monetary gain: "non-reward") feedback during a guessing task where probability of reward outcome was manipulated in survivors of severe TBI and demographically matched healthy participants. Consistent with previous findings, controls showed larger amplitude FRN to non-reward feedback and the largest amplitude FRN following a non-reward when reward probability context was greatest. In contrast, FRN in TBI participants did not significantly differentiate non-reward from reward trials and their FRN was largest to reward trials in the low reward probability context. Findings implicate an electrophysiological marker of impaired reward context sensitivity following severe TBI.     

Emotion blocks the path to learning under stereotype threat

Gender-based stereotypes undermine females’ performance on challenging math tests, but how do they influence their ability to learn from the errors they make? Females under stereotype threat or non-threat were presented with accuracy feedback after each problem on a GRE-like math test, followed by an optional interactive tutorial that provided step-wise problem-solving instruction. Event-related potentials tracked the initial detection of the negative feedback following errors [feedback related negativity (FRN), P3a], as well as any subsequent sustained attention/arousal to that information [late positive potential (LPP)]. Learning was defined as success in applying tutorial information to correction of initial test errors on a surprise retest 24-h later. Under non-threat conditions, emotional responses to negative feedback did not curtail exploration of the tutor, and the amount of tutor exploration predicted learning success. In the stereotype threat condition, however, greater initial salience of the failure (FRN) predicted less exploration of the tutor, and sustained attention to the negative feedback (LPP) predicted poor learning from what was explored. Thus, under stereotype threat, emotional responses to negative feedback predicted both disengagement from learning and interference with learning attempts. We discuss the importance of emotion regulation in successful rebound from failure for stigmatized groups in stereotype-salient environments.     

A preliminary study of the neural mechanisms of frustration in pediatric bipolar disorder using magnetoencephalography

Background: Irritability is prevalent and impairing in pediatric bipolar disorder (BD) but has been minimally studied using neuroimaging techniques. We used magnetoencephalography (MEG) to study theta band oscillations in the anterior cingulate cortex (ACC) during frustration in BD youth. ACC theta power is associated with attention to emotional stimuli, and the ACC may mediate responses to frustrating stimuli. Methods: We used the affective Posner task, an attention paradigm that uses rigged feedback to induce frustration, to compare 20 medicated BD youth (14.9±2.0 years; 45% male) and 20 healthy controls (14.7±1.7 years; 45% male). MEG measured neuronal activity after negative and positive feedback; we also compared groups on reaction time, response accuracy, and self‐reported affect. Patients met strict DSM‐IV BD criteria and were euthymic. Controls had no psychiatric history. Results: BD youth reported more negative affective responses than controls. After negative feedback, BD subjects, relative to controls, displayed greater theta power in the right ACC and bilateral parietal lobe. After positive feedback, BD subjects displayed lower theta power in the left ACC than did controls. Correlations between MEG, behavior, and affect were nonsignificant. Conclusion: In this first MEG study of BD youth, BD youth displayed patterns of theta oscillations in the ACC and parietal lobe in response to frustration‐inducing negative feedback that differed from healthy controls. These data suggest that BD youth may display heightened processing of negative feedback and exaggerated self‐monitoring after frustrating emotional stimuli. Future studies are needed with unmedicated bipolar youth, and comparison ADHD and anxiety groups. Depression and Anxiety, 2010. © 2009 Wiley‐Liss, Inc.     

Oscillatory responses to reward processing in borderline personality disorder

Objectives. Previous electrophysiological studies have confirmed impaired reward processing in patients with BPD. However, it is not clear which aspects of reward processing are affected and which brain regions are involved. The present study investigated both evoked and induced event-related oscillations (EROs) to feedback events (thought to represent different aspects of feedback processing), and used source localization (sLORETA) to assess activity in two areas known to contribute to reward processing, the dorsomedial prefrontal/anterior cingulate cortex (dmPFC/ACC) and the orbitofrontal cortex (OFC). Methods. Eighteen patients with BPD and 22 healthy controls performed a gambling task, while 64-channel electroencephalographic activity was recorded. Evoked and induced theta and high-beta band EROs as well as activity in the two regions of interest were investigated depending on the valence and magnitude of feedback events. Results. Theta-band responses to negative feedback were reduced in BPD, an effect that involved only evoked responses and the dmPFC/ ACC region, and was associated with trait impulsivity in patients. sLORETA analyses revealed disturbed evoked responses depending on feedback magnitude in the theta (OFC) and high-beta (dmPFC/ACC and OFC) frequency range. Conclusions. The results indicate multiple dysfunctions of feedback processing in patients with BPD, implicating several distinct subsets of reward-processing mechanisms.     

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.