Mal-Adaptation of Event-Related EEG Responses Preceding Performance Errors

Recent EEG and fMRI evidence suggests that behavioral errors are foreshadowed by systematic changes in brain activity preceding the outcome by seconds. In order to further characterize this type of error precursor activity, we investigated single-trial event-related EEG activity from 70 participants performing a modified Eriksen flanker task, in particular focusing on the trial-by-trial dynamics of a fronto-central independent component that previously has been associated with error and feedback processing. The stimulus-locked peaks in the N2 and P3 latency range in the event-related averages showed expected compatibility and error-related modulations. In addition, a small pre-stimulus negative slow wave was present at erroneous trials. Significant error-preceding activity was found in local stimulus sequences with decreased conflict in the form of less negativity at the N2 latency (310–350 ms) accumulating across five trials before errors; concomitantly response times were speeding across trials. These results illustrate that error-preceding activity in event-related EEG is associated with the performance monitoring system and we conclude that the dynamics of performance monitoring contribute to the generation of error-prone states in addition to the more remote and indirect effects in ongoing activity such as posterior alpha power in EEG and default mode drifts in fMRI

Feedback-related EEG dynamics separately reflect decision parameters, biases, and future choices

Optimal decision making in complex environments requires dynamic learning from unexpected events. To speed up learning, we should heavily weight information that indicates state-action-outcome contingency changes and ignore uninformative fluctuations in the environment. Often, however, unrelated information is hard to ignore and can potentially bias our learning. Here we used computational modelling and EEG to investigate learning behaviour in a modified probabilistic choice task that introduced two task-irrelevant factors that were uninformative for optimal task performance, but nevertheless could potentially bias learning: pay-out magnitudes were varied randomly and, occasionally, feedback presentation was enhanced by visual surprise. We found that participants’ overall good learning performance was biased by distinct effects of these non-normative factors. On the neural level, these parameters are represented in a dynamic and spatiotemporally dissociable sequence of EEG activity. Later in feedback processing the different streams converged on a central to centroparietal positivity reflecting a signal that is interpreted by downstream learning processes that adjust future behaviour

Interactions of focal cortical lesions with error processing: Evidence from event-related brain potentials

Electrophysiological and hemodynamic studies have suggested that structures in the vicinity of the anterior cingulate cortex are involved in performance monitoring, particularly in detection of errors. Bidirectional interactions between the frontomedian system involved in performance monitoring and the lateral prefrontal cortex as well as the orbitofrontal cortex have been proposed, but few studies have directly addressed this issue. The authors used a speeded flankers task to investigate error-related event-related potentials in 3 patient groups with different focal cortical lesions. Whereas bilateral frontopolar lesions involving the orbitofrontal cortex as well as temporal lesions did not alter the error-related negativity (ERN), lesions of the lateral frontal cortex resulted in an abolition of the ERN and in a reduction of the error positivity

Disentangling performance-monitoring signals encoded in feedback-related EEG dynamics

The feedback-related negativity (FRN) is a well-established electrophysiological correlate of feedback-processing. However, there is still an ongoing debate whether the FRN is driven by negative or positive reward prediction errors (RPE), valence of feedback, or mere surprise. Our study disentangles independent contributions of valence, surprise, and RPE on the feedback-related neuronal signal including the FRN and P3 components using the statistical power of a sample of N = 992 healthy individuals. The participants performed a modified time-estimation task, while EEG from 64 scalp electrodes was recorded. Our results show that valence coding is present during the FRN with larger amplitudes for negative feedback. The FRN is further modulated by surprise in a valence-dependent way being more positive-going for surprising positive outcomes. The P3 was strongly driven by both global and local surprise, with larger amplitudes for unexpected feedback and local deviants. Behavioral adaptations after feedback and FRN just show small associations. Results support the theory of the FRN as a representation of a signed RPE. Additionally, our data indicates that surprising positive feedback enhances the EEG response in the time window of the P3. These results corroborate previous findings linking the P3 to the evaluation of PEs in decision making and learning tasks

Surprise and error: Common neuronal architecture for the processing of errors and novelty

According to recent accounts, the processing of errors and generally infrequent, surprising (novel) events share a common neuroanat-omical substrate. Direct empirical evidence for this common processing network in humans is, however, scarce. To test this hypothesis, we administered a hybrid error-monitoring/novelty-oddball task in which the frequency of novel, surprising trials was dynamically matched to the frequency of errors. Using scalp electroencephalographic recordings and event-related functional magnetic resonance imaging (fMRI), we compared neural responses to errors with neural responses to novel events. In Experiment 1, independent component analysis of scalp ERP data revealed a common neural generator implicated in the generation of both the error-related negativity (ERN) and the novelty-related frontocentral N2. In Experiment 2, this pattern was confirmed by a conjunction analysis of event-related fMRI, which showed significantly elevated BOLD activity following both types of trials in the posterior medial frontal cortex, including the anterior midcingulate cortex (aMCC), the neuronal generator of the ERN. Together, these findings provide direct evidence of a common neural system underlying the processing of errors and novel events. This appears to be at odds with prominent theories of the ERN and aMCC. Inparticular, there inforcement learning theory of the ERN may need to be modified because it may not suffice as a fully integrative model of aMCC function. Whenever course and outcome of anaction violates expectancies (not necessarily related to reward), the aMCC seems to be engaged in evaluating the necessity of behavioral adaptation. © 2012 the authors

Gender influences on brain responses to errors and post-error adjustments

Sexual dimorphisms have been observed in many species, including humans, and extend to the prevalence and presentation of important mental disorders associated with performance monitoring malfunctions. However, precisely which underlying differences between genders contribute to the alterations observed in psychiatric diseases is unknown. Here, we compare behavioural and neural correlates of cognitive control functions in 438 female and 436 male participants performing a flanker task while EEG was recorded. We found that males showed stronger performance-monitoring-related EEG amplitude modulations which were employed to predict subjects’ genders with ~72% accuracy. Females showed more post-error slowing, but both samples did not differ in regard to response-conflict processing and coupling between the error-related negativity (ERN) and consecutive behavioural slowing. Furthermore, we found that the ERN predicted consecutive behavioural slowing within subjects, whereas its overall amplitude did not correlate with post-error slowing across participants. These findings elucidate specific gender differences in essential neurocognitive functions with implications for clinical studies. They highlight that within- and between-subject associations for brain potentials cannot be interpreted in the same way. Specifically, despite higher general amplitudes in males, it appears that the dynamics of coupling between ERN and post-error slowing between men and women is comparable

INTERPRETATION OF P300 AMPLITUDE CHANGES BY THE USE OF ADAPTATION LEVEL THEORY

Commentary on Rolf Verleger (1988). Event-related potentials and cognition: A critique of the context updating hypothesis and an alternative interpretation of P3. BBS 11: 343–427

Reducing speed and sight: how adaptive is post-error slowing?

After errors, humans and monkeys dynamically change decision boundaries which results in posterror slowing of decisions. Simultaneously decreased sensitivity to sensory information counteracts post-error increases in accuracy. Early post-error adjustments thus reflect rather a general orienting reflex than goal-directed adaptation