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

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

The effect of expressive writing on the error‐related negativity among individuals with chronic worry

The error‐related negativity (ERN), an ERP elicited immediately after errors, is enlarged among individuals with anxiety. The relationship between anxiety and enlarged ERN has spurred interest in understanding potential therapeutic benefits of decreasing its amplitude within anxious individuals. The current study used a tailored intervention—expressive writing—in an attempt to reduce the ERN among a sample of individuals with chronic worry. Consistent with hypotheses, the ERN was reduced in the expressive writing group compared to an unrelated writing control group. Findings provide experimental support that the ERN can be reduced among anxious individuals with tailored interventions. Expressive writing may serve to “offload” worries from working memory, therefore relieving the distracting effects of worry on cognition as reflected in a decreased ERN.     

On the number of trials necessary for stabilization of error‐related brain activity across the life span

The minimum number of trials necessary to accurately characterize the error‐related negativity (ERN) and the error positivity (Pe) across the life span was investigated using samples of preadolescent children, college‐age young adults, and older adults. Event‐related potentials and task performance were subsequently measured during a modified flanker task. Response‐locked averages were created using sequentially increasing errors of commission in blocks of two. Findings indicated that across all age cohorts ERN and Pe were not significantly different relative to the within‐participants grand average after six trials. Further, results indicated that the ERN and Pe exhibited excellent internal reliability in preadolescent children and young adults after six trials, but older adults required eight trials to reach similar reliability. These data indicate that the ERN and Pe may be accurately quantified with as few as six to eight commission error trials across the life span.     

Psychometric properties of the error‐related negativity in children and adolescents

Error processing is frequently examined using the error‐related negativity (ERN), a negative‐going event‐related potential occurring after the commission of an error at frontal‐central sites, and has been suggested as a neural biomarker that may be useful in characterizing trajectories of risk for anxiety. While the ERN has been shown to have excellent psychometric properties in adults, few studies have examined psychometric properties of the ERN in children and adolescents. The current study examined the 2‐year test‐retest reliability of the ERN in a sample of children and adolescents, and the convergent validity of the ERN using a flanker and go/no‐go task. Results suggest that the ERN is both reliable and stable across 2 years and across tasks. However, results also indicate that the internal consistency obtained using the flanker task is greater than the internal consistency obtained using the go/no‐go task.     

Brief Reports: Temporal stability of the error‐related negativity (ERN) and post‐error positivity (Pe): The role of number of trials

The error‐related negativity (ERN) and post‐error positivity (Pe) components of the event‐related potential (ERP) are relatively stable over time. The current study further assessed the temporal reliability of ERN and Pe amplitudes for random samples of 2 to 14 trials per participant and the grand mean over a 2‐week retest interval. In a replication of previous results, intraclass and zero‐order correlations revealed moderate to good temporal stability for participants' (N=20) grand mean ERN and Pe component amplitudes. Adding trials increased test–retest reliabilities; however, the temporal stability of ERN and Pe amplitudes with 14 or fewer trials were modest at best and considerably lower than that for the grand means. Overall, data support the temporal stability of grand‐mean ERN and Pe amplitudes and suggest that more than 14 trials are needed to include in ERN and Pe averages for adequate test–retest reliability.     

The role of hand of error and stimulus orientation in the relationship between worry and error‐related brain activity: Implications for theory and practice

Anxious apprehension/worry is associated with exaggerated error monitoring; however, the precise mechanisms underlying this relationship remain unclear. The current study tested the hypothesis that the worry‐error monitoring relationship involves left‐lateralized linguistic brain activity by examining the relationship between worry and error monitoring, indexed by the error‐related negativity (ERN), as a function of hand of error (Experiment 1) and stimulus orientation (Experiment 2). Results revealed that worry was exclusively related to the ERN on right‐handed errors committed by the linguistically dominant left hemisphere. Moreover, the right‐hand ERN‐worry relationship emerged only when stimuli were presented horizontally (known to activate verbal processes) but not vertically. Together, these findings suggest that the worry‐ERN relationship involves left hemisphere verbal processing, elucidating a potential mechanism to explain error monitoring abnormalities in anxiety. Implications for theory and practice are discussed.     

Feedback delay gradually affects amplitude and valence specificity of the feedback‐related negativity (FRN)

Processing of performance‐related feedback is an essential prerequisite for adaptive behavior. Even though in everyday life feedback is rarely immediate, to date very few studies have investigated whether the feedback‐related negativity (FRN), a relative negativity in the ERP approximately 200 to 300 ms after feedback that is sensitive to feedback valence and predictability, is modulated by feedback timing, and findings are inconsistent. The present study investigated effects of gradually increasing feedback delays on feedback processing in the FRN time window. Subjects completed a probabilistic learning task in which feedback was provided after short, intermediate, or long delays. Difference wave‐based analyses showed that amplitudes decreased linearly with increasing feedback delay. A distinct pattern was observed for the FRN as defined in the original waveforms, with FRN amplitudes being largest for long and smallest for short delays. This pattern of results is consistent with the notion that the neural systems underlying feedback processing vary depending on feedback timing. The gradually reduced difference wave signal might reflect a gradual shift away from processing in frontostriatal circuits toward medial temporal involvement. To what extent increased signal amplitudes for longer delays in the original waveforms are related to processing in certain brain structures will need to be determined in future studies.     

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

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

The impact of emotion on respiratory‐related evoked potentials

Emotion influences the perception of respiratory sensations, although the specific mechanism underlying this modulation is not yet clear. We examined the impact of viewing pleasant, neutral, and unpleasant affective pictures on the respiratory‐related evoked potential (RREP) elicited by a short inspiratory occlusion in healthy volunteers. Reduced P3 amplitude of the RREP was found for respiratory probes presented when viewing pleasant or unpleasant series, when compared to those presented during the neutral series. Earlier RREP components, such as Nf, P1, N1, and P2, showed no modulation by emotion. The results suggest that emotion impacts the perception of respiratory sensations by reducing the attentional resources available for processing afferent respiratory sensory signals.     

Memory performance and the apolipoprotein E polymorphism in a community sample of middle‐aged adults

The apolipoprotein E genotype (APOE) is an established risk factor for Alzheimer disease, with the age‐at‐onset occurring earlier in individuals having at least one APOE ϵ4 allele, relative to the APOE ϵ3 or APOE ϵ2 isoforms. Moreover, nondemented older adults with the APOE ϵ4 allele also show diminished cognitive performance, particularly on tests of learning and memory, and an accelerated decline in memory performance with increasing age. The current investigation extends the study of the APOE ϵ4 allele and cognitive performance to healthy, middle‐aged adults. A community sample of 220 non‐Hispanic Caucasian men and women, aged 24–60 (average age = 46), were genotyped for the APOE polymorphism and completed a battery of neuropsychological tests. Multivariate analyses were conducted on measures of verbal learning and memory (e.g., learning a list of words and recalling them 30 min later), visual memory (e.g., reproducing a previously copied figure from memory), and attention span (e.g., repeating long lists of digits), after adjustments for age, and estimated IQ. Results indicated that performance on learning and memory tasks was significantly poorer in adults having any APOE ϵ4 allele, relative to adults with APOE ϵ2 and ϵ3 genotypes (P < .01). Attention span did not differ by genotype. These findings, the first in a sample of middle‐aged adults, suggest that the APOE polymorphism is a marker for age‐related decline in memory (detectable prior to overt, clinical manifestations of memory loss), and/or a marker for individual differences in memory ability across the life span. Am. J. Med. Genet. (Neuropsychiatr. Genet.) 96:707–711, 2000. © 2000 Wiley‐Liss, Inc.     

A parietal‐to‐frontal shift in the P300 is associated with compensation of tactile discrimination deficits in late middle‐aged adults

Tactile perception declines with age on both behavioral and neurophysiological levels. Less well understood is how neurophysiological changes relate to tactile discrimination performance in middle adulthood. A tactile discrimination task was conducted while ERPs were measured in three groups of healthy adults aged 20 to 66 years. Accuracy was lowest in late middle adulthood (56–66 years) while somatosensory ERP components (P50, N70, P100, N140) were comparable across age groups. The cognitive P300 revealed age‐related differences in scalp distribution typical for older adults to already be present in late middle adulthood. Increased recruitment of frontal cognitive processes was positively related to performance in later middle adulthood. Our results further the understanding of age‐related differences in tactile perception during middle adulthood and the importance of cognitive processes to compensate for age‐related decline.     

Stability and reliability of error‐related electromyography over the corrugator supercilii with increasing trials

Electromyographic activity over the corrugator supercilii (cEMG), the primary facial muscle involved in negative emotions, is increased during the commission of errors on speeded reaction‐time tasks. In the present paper, data from two previously published studies were reanalyzed to investigate the reliability and stability of error‐related, correct‐related, and difference cEMG across increasing numbers of trials. For a modified go/no‐go and a flanker task, we found that error‐related cEMG was highly stable and reliable in 14 trials, and correct‐related cEMG between 56 and 82 trials, respectively. Given the typical number of trials used in studies of cognitive control, these findings suggest that many investigations of error monitoring are already sufficient to obtain acceptable error‐ and correct‐related cEMG signals. Error‐related cEMG activity is relatively easy to measure and, as such, it shows great promise for future research investigating the cognitive and affective mechanisms of error monitoring.     

The erring brain: Error‐related negativity as an endophenotype for OCD—A review and meta‐analysis

Obsessive‐compulsive disorder (OCD) is a complex and heterogeneous disorder that is associated with high personal and societal costs. Feelings of doubt, worry, and repetitive behavior, key symptoms of OCD, have been linked to hyperactive error signals in the brain. The error‐related negativity (ERN) represents a validated marker of error processing in the ERP. Increased ERN amplitudes in OCD have been reported very robustly over the last 20 years. This article integrates results from 38 studies analyzing the ERN in OCD, using a quantitative meta‐analysis. Meta‐regressions were used to examine potential moderators such as task type, symptom severity, age, and sample size. The meta‐analysis reveals a robust increase of ERN in OCD patients compared to healthy participants in response‐conflict tasks (SMD ?0.55) that is not modulated by symptom severity and age. No increase in ERN in OCD was observed in tasks that do not induce response conflict (SMD ?0.10). In addition to the meta‐analysis, the current article reviews evidence supporting that increased ERN amplitudes in OCD fulfill central criteria for an endophenotype. Further, the specificity of increased ERN amplitudes for OCD and its suitability as a potential transdiagnostic endophenotype is discussed. Finally, the clinical utility and clinical applications are examined. Overall, the evidence that increased ERN amplitudes represent a promising endophenotype indicating vulnerability for OCD is compelling. Furthermore, alterations in ERN are not limited to OCD and may constitute a transdiagnostic endophenotype. Altered neural error signals might serve as a diagnostic or predictive marker and represent a promising target for interventions.     

The way of our errors: Theme and variations

Negative feedback, either internal or external, is a fundamental guide to human learning and performance. The neural system that underlies the monitoring of performance and the adjustment of behavior has been subject to multiple neuroimaging investigations that uniformly implicate the anterior cingulate cortex and other prefrontal structures as crucial to these executive functions. The present article describes a series of experiments that employed event-related potentials to study a variety of processes associated with internal or external feedback. Three medial-frontal negativities (error-related negativity, correct-response negativity, feedback-related negativity) are highlighted, each of which plays an important role in the monitoring and dynamic adjustment of behavior. Extensions of basic research on these ERPs to questions relevant to clinical-science are also provided.     

An event‐related source localization study of response monitoring and social impairments in autism spectrum disorder

A number of studies suggest anterior cingulate cortex (ACC) abnormalities in autism spectrum disorder (ASD), which might underlie response monitoring and social impairments exhibited by children and adolescents with ASD. The goal of the present study was to extend this work by examining error and correct response monitoring using event‐related potentials (ERN, Pe, CRN) and LORETA source localization in high functioning adults with ASD and controls. Adults with ASD showed reduced ERN and Pe amplitudes and reduced rostral ACC activation compared with controls. Adults with ASD also showed less differentiation between error and correct ERP components. Social impairments and higher overall autism symptoms were related to reduced rostral ACC activity at the time of the ERN, particularly in adults with ASD. These findings suggest that reduced ACC activity may reflect a putative brain mechanism involved in the origins and maintenance of social impairments and raise the possibility of the presence of stable brain‐behavior relation impairment across development in some individuals with ASD.     

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

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

Developmental trends of performance monitoring measures in 7‐ to 25‐year‐olds: Unraveling the complex nature of brain measures

This study explores how trial‐to‐trial latency variability contributes to the developmental trends observed in ERN amplitude found in the incorrect trials of a performance monitoring task, the visual flanker task. An Adaptive Woody filter was used to measure and correct for the trial‐to‐trial latency variability of the ERN in 240 participants aged 7–25 years. Using three measures of latency variability, the degree of trial‐to‐trial latency variability was shown to decrease as the age of the participants increased from 7 to 25 years. The success of the Adaptive Woody filter technique to remove the trial‐to‐trial latency variability was demonstrated in a straightforward manner by the significant changes in the measures of fit and intraindividual variability obtained before and after applying the filter. After the latency variability effects were removed and adjusted averaged ERPs were obtained, a more subtle but significant nonlinear developmental trend was still found in the amplitude of the ERN component.     

The distractor positivity (Pd) signals lowering of attentional priority: Evidence from event‐related potentials and individual differences

We investigated the effects of task demands and individual differences on the allocation of attention. Using the same stimuli, participants indicated the orientation of a line contained in a shape singleton (identification task) or the presence of singletons (detection task). Shape singletons in the identification task elicited a contralateral negativity (N2pc) whereas shape singletons in the detection task elicited a contralateral positivity (Pd). We suggest that the reduction of attentional priority of a salient stimulus, reflected by the Pd, occurred more rapidly with the less demanding detection task. Further, fewer distractible participants showed a larger N2pc to lateral color distractors than highly distractible participants. We suggest that highly distractible participants developed compensatory mechanisms to suppress distracting stimuli.