Markus Ullsperger

Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring

Goal-directed behavior requires the continuous monitoring and dynamic adjustment of ongoing actions. Here, we report a direct coupling between the event-related electroencephalogram (EEG), functional magnetic resonance imaging (fMRI), and behavioral measures of performance monitoring in humans. By applying independent component analysis to EEG signals recorded simultaneously with fMRI, we found the single-trial error-related negativity of the EEG to be systematically related to behavior in the subsequent trial, thereby reflecting immediate behavioral adjustments of a cognitive performance monitoring system. Moreover, this trial-by-trial EEG measure of performance monitoring predicted the fMRI activity in the rostral cingulate zone, a brain region thought to play a key role in processing of response errors. We conclude that investigations of the dynamic coupling between EEG and fMRI provide a powerful approach for the study of higher order brain functions.

Prediction of human errors by maladaptive changes in event-related brain networks

Humans engaged in monotonous tasks are susceptible to occasional errors that may lead to serious consequences, but little is known about brain activity patterns preceding errors. Using functional MRI and applying independent component analysis followed by deconvolution of hemodynamic responses, we studied error preceding brain activity on a trial-by-trial basis. We found a set of brain regions in which the temporal evolution of activation predicted performance errors. These maladaptive brain activity changes started to evolve ≈30 sec before the error. In particular, a coincident decrease of deactivation in default mode regions of the brain, together with a decline of activation in regions associated with maintaining task effort, raised the probability of future errors. Our findings provide insights into the brain network dynamics preceding human performance errors and suggest that monitoring of the identified precursor states may help in avoiding human errors in critical real-world situations.

Single-trial EEG-fMRI reveals the dynamics of cognitive function

Two major non-invasive techniques in cognitive neuroscience, electroencephalography (EEG) and functional magnetic resonance imaging (fMRI), have complementary advantages with regard to their spatial and temporal resolution. Recent hardware and software developments have made it feasible to acquire EEG and fMRI data simultaneously. We emphasize the potential of simultaneous EEG and fMRI recordings to pursue new strategies in cognitive neuroimaging. Specifically, we propose that, by exploiting the combined spatiotemporal resolution of the methods, the integration of EEG and fMRI recordings on a single-trial level enables the rich temporal dynamics of information processing to be characterized within spatially well-defined neural networks.

Neural correlates of error awareness

Error processing results in a number of consequences on multiple levels. The posterior frontomedian cortex (pFMC) is involved in performance monitoring and signalling the need for adjustments, which can be observed as post-error speed-accuracy shifts at the behavioural level. Furthermore autonomic reactions to an error have been reported. The role of conscious error awareness for this processing cascade has received little attention of researchers so far. We examined the neural correlates of conscious error perception in a functional magnetic resonance imaging (fMRI) study. An antisaccade task known to yield sufficient numbers of aware and unaware errors was used. Results from a metaanalysis were used to guide a region of interest (ROI) analysis of the fMRI data. Consistent with previous reports, error-related activity in the rostral cingulate zone (RCZ), the pre-supplementary motor area (pre-SMA) and the insular cortex bilaterally was found. Whereas the RCZ activity did not differentiate between aware and unaware errors, activity in the left anterior inferior insular cortex was stronger for aware as compared to unaware errors. This could be due to increased awareness of the autonomic reaction to an error, or the increased autonomic reaction itself. Furthermore, post-error adjustments were only observed after aware errors and a correlation between post-error slowing and the hemodynamic activity in the RCZ was revealed. The data suggest that the RCZ activity alone is insufficient to drive error awareness. Its signal appears to be useful for post-error speed-accuracy adjustments only when the error is consciously perceived.

Conscious perception of errors and its relation to the anterior insula

To detect erroneous action outcomes is necessary for flexible adjustments and therefore a prerequisite of adaptive, goal-directed behavior. While performance monitoring has been studied intensively over two decades and a vast amount of knowledge on its functional neuroanatomy has been gathered, much less is known about conscious error perception, often referred to as error awareness. Here, we review and discuss the conditions under which error awareness occurs, its neural correlates and underlying functional neuroanatomy. We focus specifically on the anterior insula, which has been shown to be (a) reliably activated during performance monitoring and (b) modulated by error awareness. Anterior insular activity appears to be closely related to autonomic responses associated with consciously perceived errors, although the causality and directions of these relationships still needs to be unraveled. We discuss the role of the anterior insula in generating versus perceiving autonomic responses and as a key player in balancing effortful task-related and resting-state activity. We suggest that errors elicit reactions highly reminiscent of an orienting response and may thus induce the autonomic arousal needed to recruit the required mental and physical resources. We discuss the role of norepinephrine activity in eliciting sufficiently strong central and autonomic nervous responses enabling the necessary adaptation as well as conscious error perception.

The conflict adaptation effect: it's not just priming.

Analyses of trial sequences in flanker tasks have revealed cognitive adaptation, reflected in a reduced interference effect following incompatible trials (Gratton, Coles, & Donchin, 1992). These effects have been explained on the basis of the response conflict monitoring model of Botvinick, Braver, Barch, Carter, and Cohen (2001), who proposed that preceding response conflict triggers stronger topdown control, leading to performance improvements on subsequent trials of similar context. A recent study (Mayr, Awh, & Laurey, 2003) has challenged this account, suggesting that the behavioral adaptations are confined to trial sequences of exact trial repetitions and can therefore be explained by repetition priming. Here, we present two experiments in which the sequential dependency effect was present even on trial sequences that did not involve stimulus repeats. We discuss the data with respect to the conflict-monitoring and repetition-priming accounts.

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.

Neuroimaging of performance monitoring: Error detection and beyond

The ability to monitor performance and behavior is crucial for goal-directed, adaptive behavior in a changing environment. Performance monitoring has been extensively investigated using behavioral, electrophysiological and hemodynamic measures, and is still in the focus of many research projects. This paper gives an overview on neuroimaging of performance monitoring and the models which arose from several research approaches, taking into account the knowledge stemming from electrophysiological and lesion studies. Particular emphasis is put on error detection and response conflict monitoring, but also at motivational factors. Furthermore, the paper presents and discusses data from an fMRI study investigating the influence of error relevance on the hemodynamic correlates of error processing. By instruction and financial reward manipulation, the relevance of errors were block-wise modulated in a flanker paradigm. The results suggest that the engagement of the posterior frontomedian wall (pFMC) previously shown to be involved in performance monitoring is dependent on error relevance.

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.

Who Comes First? The Role of the Prefrontal and Parietal Cortex in Cognitive Control

Cognitive control processes enable us to adjust our behavior to changing environmental demands. Although neuropsychological studies suggest that the critical cortical region for cognitive control is the prefrontal cortex, neuro-imaging studies have emphasized the interplay of prefrontal and parietal cortices. This raises the fundamental question about the different contributions of prefrontal and parietal areas in cognitive control. It was assumed that the prefrontal cortex biases processing in posterior brain regions. This assumption leads to the hypothesis that neural activity in the prefrontal cortex should precede parietal activity in cognitive control. The present study tested this assumption by combining results from functional magnetic resonance imaging (fMRI) providing high spatial resolution and event-related potentials (ERPs) to gain high temporal resolution. We collected ERP data using a modified task-switching paradigm. In this paradigm, a situation where the same task was indicated by two different cues was compared with a situation where two cues indicated different tasks. Only the latter condition required updating of the task set. Task-set updating was associated with a midline negative ERP deflection peaking around 470 msec. We placed dipoles in regions activated in a previous fMRI study that used the same paradigm (left inferior frontal junction, right inferior frontal gyrus, right parietal cortex) and fitted their directions and magnitudes to the ERP effect. The frontal dipoles contributed to the ERP effect earlier than the parietal dipole, providing support for the view that the prefrontal cortex is involved in updating of general task representations and biases relevant stimulus-response associations in the parietal cortex.