Claudia Danielmeier

Post-error adjustments

When our brain detects an error, this process changes how we react on ensuing trials. People show post-error adaptations, potentially to improve their performance in the near future. At least three types of behavioral post-error adjustments have been observed. These are post-error slowing (PES), post-error reduction of interference, and post-error improvement in accuracy (PIA). Apart from these behavioral changes, post-error adaptations have also been observed on a neuronal level with functional magnetic resonance imaging and electroencephalography. Neuronal post-error adaptations comprise activity increase in task-relevant brain areas, activity decrease in distracter-encoding brain areas, activity modulations in the motor system, and mid-frontal theta power increases. Here, we review the current literature with respect to these post-error adjustments, discuss under which circumstances these adjustments can be observed, and whether the different types of adjustments are linked to each other. We also evaluate different approaches for explaining the functional role of PES. In addition, we report reanalyzed and follow-up data from a flanker task and a moving dots interference task showing (1) that PES and PIA are not necessarily correlated, (2) that PES depends on the response–stimulus interval, and (3) that PES is reliable on a within-subject level over periods as long as several months.

Neurophysiology of Performance Monitoring and Adaptive Behavior

Successful goal-directed behavior requires not only correct action selection, planning, and execution but also the ability to flexibly adapt behavior when performance problems occur or the environment changes. A prerequisite for determining the necessity, type, and magnitude of adjustments is to continuously monitor the course and outcome of ones actions. Feedback-control loops correcting deviations from intended states constitute a basic functional principle of adaptation at all levels of the nervous system. Here, we review the neurophysiology of evaluating action course and outcome with respect to their valence, i.e., reward and punishment, and initiating short- and long-term adaptations, learning, and decisions. Based on studies in humans and other mammals, we outline the physiological principles of performance monitoring and subsequent cognitive, motivational, autonomic, and behavioral adaptation and link them to the underlying neuroanatomy, neurochemistry, psychological theories, and computational models. We provide an overview of invasive and noninvasive systemic measures, such as electrophysiological, neuroimaging, and lesion data. We describe how a wide network of brain areas encompassing frontal cortices, basal ganglia, thalamus, and monoaminergic brain stem nuclei detects and evaluates deviations of actual from predicted states indicating changed action costs or outcomes. This information is used to learn and update stimulus and action values, guide action selection, and recruit adaptive mechanisms that compensate errors and optimize goal achievement.

Posterior medial frontal cortex activity predicts post-error adaptations in task-related visual and motor areas.

As Seneca the Younger put it, “To err is human, but to persist is diabolical.” To prevent repetition of errors, human performance monitoring often triggers adaptations such as general slowing and/or attentional focusing. The posterior medial frontal cortex (pMFC) is assumed to monitor performance problems and to interact with other brain areas that implement the necessary adaptations. Whereas previous research showed interactions between pMFC and lateral-prefrontal regions, here we demonstrate that upon the occurrence of errors the pMFC selectively interacts with perceptual and motor regions and thereby drives attentional focusing toward task-relevant information and induces motor adaptation observed as post-error slowing. Functional magnetic resonance imaging data from an interference task reveal that error-related pMFC activity predicts the following: (1) subsequent activity enhancement in perceptual areas encoding task-relevant stimulus features; (2) activity suppression in perceptual areas encoding distracting stimulus features; and (3) post-error slowing-related activity decrease in the motor system. Additionally, diffusion-weighted imaging revealed a correlation of individual post-error slowing and white matter integrity beneath pMFC regions that are connected to the motor inhibition system, encompassing right inferior frontal gyrus and subthalamic nucleus. Thus, disturbances in task performance are remedied by functional interactions of the pMFC with multiple task-related brain regions beyond prefrontal cortex that result in a broad repertoire of adaptive processes at perceptual as well as motor levels.

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 neuroanatomical 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. In particular, the reinforcement 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 an action violates expectancies (not necessarily related to reward), the aMCC seems to be engaged in evaluating the necessity of behavioral adaptation.

Error awareness revisited: Accumulation of multimodal evidence from central and autonomic nervous systems

The differences between erroneous actions that are consciously perceived as errors and those that go unnoticed have recently become an issue in the field of performance monitoring. In EEG studies, error awareness has been suggested to influence the error positivity (Pe) of the response-locked event-related brain potential, a positive voltage deflection prominent approximately 300 msec after error commission, whereas the preceding error-related negativity (ERN) seemed to be unaffected by error awareness. Erroneous actions, in general, have been shown to promote several changes in ongoing autonomic nervous system (ANS) activity, yet such investigations have only rarely taken into account the question of subjective error awareness. In the first part of this study, heart rate, pupillometry, and EEG were recorded during an antisaccade task to measure autonomic arousal and activity of the CNS separately for perceived and unperceived errors. Contrary to our expectations, we observed differences in both Pe and ERN with respect to subjective error awareness. This was replicated in a second experiment, using a modified version of the same task. In line with our predictions, only perceived errors provoke the previously established post-error heart rate deceleration. Also, pupil size yields a more prominent dilatory effect after an erroneous saccade, which is also significantly larger for perceived than unperceived errors. On the basis of the ERP and ANS results as well as brain–behavior correlations, we suggest a novel interpretation of the implementation and emergence of error awareness in the brain. In our framework, several systems generate input signals (e.g., ERN, sensory input, proprioception) that influence the emergence of error awareness, which is then accumulated and presumably reflected in later potentials, such as the Pe.

Error awareness and the insula: Links to neurological and psychiatric diseases

Becoming aware of errors that one has committed might be crucial for strategic behavioral and neuronal adjustments to avoid similar errors in the future. This review addresses conscious error perception (“error awareness”) in healthy subjects as well as the relationship between error awareness and neurological and psychiatric diseases. We first discuss the main findings on error awareness in healthy subjects. A brain region, that appears consistently involved in error awareness processes, is the insula, which also provides a link to the clinical conditions reviewed here. Then we focus on a neurological condition whose core element is an impaired awareness for neurological consequences of a disease: anosognosia for hemiplegia (AHP). The insular cortex has been implicated in both error awareness and AHP, with anterior insular regions being involved in conscious error processing and more posterior areas being related to AHP. In addition to cytoarchitectonic and connectivity data, this reflects a functional and structural gradient within the insula from anterior to posterior. Furthermore, studies dealing with error awareness and lack of insight in a number of psychiatric diseases are reported. Especially in schizophrenia, attention-deficit hyperactivity disorder, (ADHD) and autism spectrum disorders (ASD) the performance monitoring system seems impaired, thus conscious error perception might be altered.

Modulation of the error-related negativity by response conflict

An arrow version of the Eriksen flanker task was employed to investigate the influence of conflict on the error-related negativity (ERN). The degree of conflict was modulated by varying the distance between flankers and the target arrow (CLOSE and FAR conditions). Error rates and reaction time data from a behavioral experiment were used to adapt a connectionist model of this task. This model was based on the conflict monitoring theory and simulated behavioral and event-related potential data. The computational model predicted an increased ERN amplitude in FAR incompatible (the low-conflict condition) compared to CLOSE incompatible errors (the high-conflict condition). A subsequent ERP experiment confirmed the model predictions. The computational model explains this finding with larger post-response conflict in far trials. In addition, data and model predictions of the N2 and the LRP support the conflict interpretation of the ERN.

Adaptive coding of action values in the human rostral cingulate zone

Correctly selecting appropriate actions in an uncertain environment requires gathering experience about the available actions by sampling them over several trials. Recent findings suggest that the human rostral cingulate zone (RCZ) is important for the integration of extended action–outcome associations across multiple trials and in coding the subjective value of each action. During functional magnetic resonance imaging, healthy volunteers performed two versions of a probabilistic reversal learning task with high (HP) or low (LP) reward probabilities that required them to integrate action–outcome relations over lower or higher numbers of trials, respectively. In the HP session, subjects needed fewer trials to adjust their behavior in response to a reversal of response–reward contingencies. Similarly, the learning rate derived from a reinforcement learning model was higher in the HP condition. This was accompanied by a stronger response of the RCZ to negative feedback upon reversals in the HP condition. Furthermore, RCZ activity related to negative reward prediction errors varied as a function of the learning rate, which determines to what extent the prediction error is used to update action values. These data show that RCZ responses vary as a function of the information content provided by the environment. The more likely a negative event indicates the need for behavioral adaptations, the more prominent is the response of the RCZ. Thus, both the window of trials over which reinforcement information is integrated and adjustment of action values in the RCZ covary with the stochastics of the environment.

Human anterior intraparietal and ventral premotor cortices support representations of grasping with the hand or a novel tool

Humans display a remarkable capacity to use tools instead of their biological effectors. Yet, little is known about the mechanisms that support these behaviors. Here, participants learned to grasp objects, appearing in a variety of orientations, with a novel, handheld mechanical tool. Following training, psychophysical functions relating grip preferences (i.e., pronated vs. supinated) to stimulus orientations indicate a reliance on distinct, effector-specific internal representations when planning grasping actions on the basis of the tool versus the hands. Accompanying fMRI data show that grip planning in both hand and tool conditions was associated with similar increases in activity within the same regions of the anterior intraparietal and caudal ventral premotor cortices, a putative homologue of the macaque anterior intraparietal–ventral premotor (area F5) “grasp circuit.” These findings suggest that tool use is supported by effector-specific representations of grasping with the tool that are functionally independent of previously existing representations of the hand and yet occur within the same parieto-frontal regions involved in manual prehension. These levels of representation are critical for accurate planning and execution of actions in a manner that is sensitive to the respective properties of these effectors. These effector-specific representations likely coexist with effector-independent representations. The latter were recently reported in macaque F5 [Umiltà, M. A., Escola, L., Intskirveli, I., Grammont, F., Rochat, M., Caruana, F., et al. When pliers become fingers in the monkey motor system. Proceedings of the National Academy of Sciences, U.S.A., 105, 2209–2213, 2008] and appear to be established by tool use training through modification of existing representations of grasping with the hand. These more abstract levels of representation may facilitate the transfer of skills between hand and tool.

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.