Cortical ß Power Reflects a Neural Implementation of Decision Boundary Collapse in Speeded Decisions.

A prominent account of decision-making assumes that information is accumulated until a fixed response threshold is crossed. However, many decisions require weighting of information appropriately against time. Collapsing response thresholds are a mathematically optimal solution to this decision problem. However, our understanding of the neurocomputational mechanisms underlying dynamic response thresholds remains significantly incomplete. To investigate this issue, we used a multistage drift-diffusion model (DDM) and also analyzed EEG ß power lateralization (BPL). The latter served as a neural proxy for decision signals. We analyzed a large dataset (n = 863; 434 females and 429 males) from a speeded flanker task and data from an independent confirmation sample (n = 119; 70 females and 49 males). We showed that a DDM with collapsing decision thresholds, a process wherein the decision boundary reduces over time, captured participants' time-dependent decision policy more accurately than a model with fixed thresholds. Previous research suggests that BPL over motor cortices reflects features of a decision signal and that its peak, coinciding with the motor response, may serve as a neural proxy for the decision threshold. We show that BPL around the response decreased with increasing RTs. Together, our findings offer compelling evidence for the existence of collapsing decision thresholds in decision-making processes.

Unbiased post-error slowing in interference tasks: A confound and a simple solution.

We typically slow down after committing an error, an effect termed post-error slowing (PES). Traditionally, PES has been calculated by subtracting post-correct from post-error RTs. Dutilh et al. (Journal of Mathematical Psychology, 56(3), 208-216, 2012), however, showed PES values calculated in this way are potentially biased. Therefore, they proposed to compute robust PES scores by subtracting pre-error RTs from post-error RTs. Based on data from a large-scale study using the flanker task, we show that both traditional and robust PES estimates can be biased. The source of the bias are differential imbalances in the percentage of congruent vs. incongruent post-correct, pre-error, and post-error trials. Specifically, we found that post-correct, pre-error, and post-error trials were more likely to be congruent than incongruent, with the size of the imbalance depending on the trial type as well as the length of the response-stimulus interval (RSI). In our study, for trials preceded by a 700-ms RSI, the percentages of congruent trials were 62% for post-correct trials, 66% for pre-error trials, and 56% for post-error trials. Relative to unbiased estimates, these imbalances inflated traditional PES estimates by 37% (9 ms) and robust PES estimates by 42% (16 ms) when individual-participant means were calculated. When individual-participant medians were calculated, the biases were even more pronounced (40% and 50% inflation, respectively). To obtain unbiased PES scores for interference tasks, we propose to compute unweighted individual-participant means by initially calculating mean RTs for congruent and incongruent trials separately, before averaging congruent and incongruent mean RTs to calculate means for post-correct, pre-error and post-error trials.

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 one's 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.

Neural and behavioral traces of error awareness.

Monitoring for errors and behavioral adjustments after errors are essential for daily life. A question that has not been addressed systematically yet, is whether consciously perceived errors lead to different behavioral adjustments compared to unperceived errors. Our goal was to develop a task that would enable us to study different commonly observed neural correlates of error processing and post-error adjustments in their relation to error awareness and accuracy confidence in a single experiment. We assessed performance in a new number judgement error awareness task in 70 participants. We used multiple, robust, single-trial EEG regressions to investigate the link between neural correlates of error processing (e.g., error-related negativity (ERN) and error positivity (Pe)) and error awareness. We found that only aware errors had a slowing effect on reaction times in consecutive trials, but this slowing was not accompanied by post-error increases in accuracy. On a neural level, error awareness and confidence had a modulating effect on both the ERN and Pe, whereby the Pe was most predictive of participants' error awareness. Additionally, we found partial support for a mediating role of error awareness on the coupling between the ERN and behavioral adjustments in the following trial. Our results corroborate previous findings that show both an ERN/Pe and a post-error behavioral adaptation modulation by error awareness. This suggests that conscious error perception can support meta-control processes balancing the recruitment of proactive and reactive control. Furthermore, this study strengthens the role of the Pe as a robust neural index of error awareness.

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.

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.

Frontal neural metabolite changes in schizophrenia and their association with cognitive control: A systematic review.

A large proportion of patients with schizophrenia exhibit deficits in cognitive control functions including working memory, processing speed and inhibitory control, which have been associated with frontal brain areas. In this systematic review, we investigated differences between chronic schizophrenia patients, first-episode (FEP) patients and healthy control groups in the neurometabolite levels of GABA, glutamate, glutamine and Glx in frontal brain areas. Additionally, we reviewed correlations between cognitive control functions or negative symptoms and these neurometabolite levels. Several studies reported decreased GABA or glutamate concentrations in frontal lobe areas, particularly in chronic schizophrenia patients, while the results were mixed for FEP patients. Working memory performance and prediction errors have been associated with frontal GABA and glutamate levels, and processing speed with frontomedial GABA levels in chronic patients. The relationship between metabolites and negative symptom severity was somewhat inconsistent. Future studies should take the participants' age, medication status or responsivity, disease stage and precise anatomical location of the voxel into account when comparing neurometabolite levels between schizophrenia patients and healthy controls.

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.

Setting the frame: the human brain activates a basic low-frequency network for language processing.

Low-frequency fluctuations (LFFs) are a major source of variation in fMRI data. This has been established in numerous experiments-particularly in the resting state. Here we investigate LFFs in a task-dependent setting. We hypothesized that LFFs may contain information about cognitive networks that are specific to the overall task domain without being time locked to stimulus onsets. We analyzed data of 6 fMRI experiments, 4 of which belonged to the language domain. After regressing out specifics of the experimental design and low-pass filtering (<0.1 Hz), we found that the 4 language experiments produced a correlational pattern that was not present in the 2 nonlanguage studies. Specifically, a region in the posterior part of the left superior temporal sulcus/gyrus was consistently correlated with both the left Brodmann's area 44 and the left frontal operculum in all 4 language studies, whereas this correlation was not found in the 2 other experiments. This finding indicates the existence of a basic network that acts as a general framework for language processing. In contrast to networks obtained by a conventional conjunction analysis of activation maps, this network is independent of experimental specifics such as stimulus onsets and exists in the low-frequency range.

High Schizotypy Predicts Emotion Recognition Independently of Negative Affect.

Introduction: Deficits in Emotion Recognition (ER) contribute significantly to poorer functional outcomes in people with schizophrenia. However, rather than reflecting a core symptom of schizophrenia, reduced ER has been suggested to reflect increased mood disorder co-morbidity and confounds of patient status such as medication. We investigated whether ER deficits are replicable in psychometrically defined schizotypy, and whether this putative association is mediated by increased negative affect. Methods: Two hundred and nine participants between the ages of 18 and 69 (66% female) were recruited from online platforms: 80% held an undergraduate qualification or higher, 44% were current students, and 46% were in current employment. Participants were assessed on psychometric schizotypy using the O-LIFE which maps onto the same symptoms structure (positive, negative, and disorganised) as schizophrenia. Negative affect was assessed using the Depression Anxiety and Stress Scale (DASS-21). Emotion Recognition of both positive and negative emotions was assessed using the short version of the Geneva Emotion Recognition Task (GERT-S). Results: Negative schizotypy traits predicted poorer ER accuracy to negative emotions (ß = -0.192, p = 0.002) as predicted. Unexpectedly, disorganised schizotypy traits predicted improved performance to negative emotions (ß = 0.256, p = 0.007) (primarily disgust). Negative affect was found to be unrelated to ER performance of either valence (both p > 0.591). No measure predicted ER accuracy of positive emotions. Positive schizotypy traits were not found to predict either positive or negative ER accuracy. However, positive schizotypy predicted increased confidence in decisions and disorganised schizotypy predicted reduced confidence in decisions. Discussion: The replication of ER deficits in non-clinical negative schizotypy suggests that the association between negative symptoms and ER deficits in clinical samples may be independent of confounds of patient status (i.e., anti-psychotic medication). The finding that this association was independent of negative affect further suggests ER deficits in patients may also be independent of mood disorder co-morbidity. This association was not demonstrated for the positive symptom dimension of the O-LIFE, which may be due to low levels of this trait in the current sample.

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.

Cortical beta power reflects decision dynamics and uncovers multiple facets of post-error adaptation.

Adapting to errors quickly is essential for survival. Reaction slowing after errors is commonly observed but whether this slowing is adaptive or maladaptive is unclear. Here, we analyse a large dataset from a flanker task using two complementary approaches: a multistage drift-diffusion model, and the lateralisation of EEG beta power as a time-resolved index of choice formation. Fitted model parameters and their independently measured neuronal proxies in beta power convergently show a complex interplay of multiple mechanisms initiated after mistakes. Suppression of distracting evidence, response threshold increase, and reduction of evidence accumulation cause slow and accurate post-error responses. This data provides evidence for both adaptive control and maladaptive orienting after errors yielding an adaptive net effect - a decreased likelihood to repeat mistakes. Generally, lateralised beta power provides a non-invasive readout of action selection for the study of speeded cognitive control processes.

Electrophysiological Correlates of Error Monitoring and Feedback Processing in Second Language Learning.

Humans monitor their behavior to optimize performance, which presumably relies on stable representations of correct responses. During second language (L2) learning, however, stable representations have yet to be formed while knowledge of the first language (L1) can interfere with learning, which in some cases results in persistent errors. In order to examine how correct L2 representations are stabilized, this study examined performance monitoring in the learning process of second language learners for a feature that conflicts with their first language. Using EEG, we investigated if L2 learners in a feedback-guided word gender assignment task showed signs of error detection in the form of an error-related negativity (ERN) before and after receiving feedback, and how feedback is processed. The results indicated that initially, response-locked negativities for correct (CRN) and incorrect (ERN) responses were of similar size, showing a lack of internal error detection when L2 representations are unstable. As behavioral performance improved following feedback, the ERN became larger than the CRN, pointing to the first signs of successful error detection. Additionally, we observed a second negativity following the ERN/CRN components, the amplitude of which followed a similar pattern as the previous negativities. Feedback-locked data indicated robust FRN and P300 effects in response to negative feedback across different rounds, demonstrating that feedback remained important in order to update memory representations during learning. We thus show that initially, L2 representations may often not be stable enough to warrant successful error monitoring, but can be stabilized through repeated feedback, which means that the brain is able to overcome L1 interference, and can learn to detect errors internally after a short training session. The results contribute a different perspective to the discussion on changes in ERN and FRN components in relation to learning, by extending the investigation of these effects to the language learning domain. Furthermore, these findings provide a further characterization of the online learning process of L2 learners.

Reducing Speed and Sight: How Adaptive Is Post-Error Slowing?

After errors, decision boundaries change, which results in post-error slowing of decisions. Purcell and Kiani (2016) report simultaneously decreased sensitivity to sensory information counteracts post-error increases in accuracy. Early post-error adjustments reflect a general orienting reflex rather than goal-directed adaptation.

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.

Acetylcholine mediates behavioral and neural post-error control.

Humans often commit errors when they are distracted by irrelevant information and no longer focus on what is relevant to the task at hand. Adjustments following errors are essential for optimizing goal achievement. The posterior medial frontal cortex (pMFC), a key area for monitoring errors, has been shown to trigger such post-error adjustments by modulating activity in visual cortical areas. However, the mechanisms by which pMFC controls sensory cortices are unknown. We provide evidence for a mechanism based on pMFC-induced recruitment of cholinergic projections to task-relevant sensory areas. Using fMRI in healthy volunteers, we found that error-related pMFC activity predicted subsequent adjustments in task-relevant visual brain areas. In particular, following an error, activity increased in those visual cortical areas involved in processing task-relevant stimulus features, whereas activity decreased in areas representing irrelevant, distracting features. Following treatment with the muscarinic acetylcholine receptor antagonist biperiden, activity in visual areas was no longer under control of error-related pMFC activity. This was paralleled by abolished post-error behavioral adjustments under biperiden. Our results reveal a prominent role of acetylcholine in cognitive control that has not been recognized thus far. Regaining optimal performance after errors critically depends on top-down control of perception driven by the pMFC and mediated by acetylcholine. This may explain the lack of adaptivity in conditions with reduced availability of cortical acetylcholine, such as Alzheimer's disease.

Where action impairs visual encoding: an event-related fMRI study.

Behavioral experiments revealed an impairment in a perceptual task when a motor task has to be planned in parallel. In two event-related fMRI experiments healthy participants performed a GO-NOGO motor task and a visual identification task. Thus, we were able to investigate the influence of a motor task on visual identification. The paradigm allowed to compare visually identical trials with and without a concurrently performed motor response. In Experiment 1, the visual task focused on shape identification, whereas in Experiment 2, the visual task focused on color identification. We found an action-dependent BOLD response modulation in extrastriate visual areas (V3, V3A in Experiment 1 and additionally V4 in Experiment 2). Thus, results demonstrate that the planning of an action has modulatory effects in brain areas concerned with early processes in visual encoding.

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.