William J. Gehring

A Neural System for Error Detection and Compensation

Humans can monitor actions and compensate for errors. Analysis of the human event-related brain potentials (ERPs) accompanying errors provides evidence for a neural process whose activity is specifically associated with monitoring and compensating for erroneous behavior. This error-related activity is enhanced when subjects strive for accurate performance but is diminished when response speed is emphasized at the expense of accuracy. The activity is also related to attempts to compensate for the erroneous behavior.

Prefrontal-cingulate interactions in action monitoring

We found that medial frontal cortex activity associated with action monitoring (detecting errors and behavioral conflict) depended on activity in the lateral prefrontal cortex. We recorded the error-related negativity (ERN), an event-related brain potential proposed to reflect anterior cingulate action monitoring, from individuals with lateral prefrontal damage or age-matched or young control participants. In controls, error trials generated greater ERN activity than correct trials. In individuals with lateral prefrontal damage, however, correct-trial ERN activity was equal to error-trial ERN activity. Lateral prefrontal damage also affected corrective behavior. Thus the lateral prefrontal cortex seemed to interact with the anterior cingulate cortex in monitoring behavior and in guiding compensatory systems.

Action-Monitoring Dysfunction in Obsessive-Compulsive Disorder

Evidence suggests that a hyperactive frontal-striatal-thalamic-frontal circuit is associated with the symptoms of obsessive-compulsive disorder (OCD), but there is little agreement about the function of the exaggerated activity. We report electrophysiological evidence suggesting that part of this system monitors events and generates error signals when the events conflict with an individuals internal standards or goals. Nine individuals with OCD and 9 age-, sex-, and education-matched control participants performed a speeded reaction time task. The error-related negativity, an event-related brain potential component that reflects action-monitoring processes, was enhanced in the individuals with OCD. The magnitude of this enhancement correlated with symptom severity. Dipole modeling suggested that the locus of the enhancement corresponded to medial frontal regions, possibly the anterior cingulate cortex.

Functions of the Medial Frontal Cortex in the Processing of Conflict and Errors

A principal function of the medial frontal cortex, in particular the anterior cingulate cortex (ACC), is to monitor action. The error-related negativity (ERN, or NE), an event-related brain potential, reflects medial frontal action-monitoring processes. Specifically, the error-detection theory of the ERN states that the ERN reflects ACC processing that is directly related to detecting the error. This theory predicts that ERN and ACC activity should increase directly with the dissimilarity of the error from the correct response, with similarity defined with respect to the common movement features of the responses. In contrast, the conflict-detection theory claims that ACC and ERN activity represent the detection of response conflict. This theory predicts that the activity should increase directly with the similarity of the error and the correct response. To test these theories, we investigated the effects of response similarity and conflict on the ERN, using a task that involved hand and foot movements. ERN activity was largest under conditions of high response conflict, where the error was similar to the correct response. This finding favors the conflict-detection theory over the error-detection theory, although the ERN was not associated with posterror slowing, as predicted by proponents of both theories. Discrepancies between our results and those of past studies may stem from the use in previous studies of four-finger response tasks which are subject to unique physiological and biomechanical constraints. We conclude that the ERN reflects medial frontal activity involved in the detection or affective processing of response conflict.

Error-related hyperactivity of the anterior cingulate cortex in obsessive-compulsive disorder

BACKGROUND Hyperactivity of the anterior cingulate cortex (ACC) in patients with obsessive-compulsive disorder (OCD) has been shown to increase with symptom provocation and to normalize with treatment-induced symptom reduction. Although the functional significance of anterior cingulate involvement in OCD remains unknown, electrophysiological evidence has linked this region to error-processing abnormalities in patients with OCD. In this functional magnetic resonance imaging (fMRI) study, we sought to further localize error-processing differences within the ACC of OCD patients compared with healthy subjects. METHODS Event-related fMRI data were collected for eight OCD patients and seven healthy subjects during the performance of a simple cognitive task designed to elicit errors but not OCD symptoms. RESULTS Both OCD patients and healthy subjects demonstrated dorsal ACC activation during error commission. The OCD patients exhibited significantly greater error-related activation of the rostral ACC than comparison subjects. Activity in this region was positively correlated with symptom severity in the patients. CONCLUSIONS Error-processing abnormalities within the rostral anterior cingulate occur in the absence of symptom expression in patients with OCD.

Neural Systems for Error Monitoring Recent Findings and Theoretical Perspectives

Complex behavior requires a flexible system that maintains task performance in the context of specific goals, evaluating behavioral progress, adjusting behavior as needed, and adapting to changing contingencies. Generically referred to as performance monitoring, a key component concerns the identification and correction of differences between an intended and an executed response (i.e., an error). Brain mapping experiments have now identified the temporal and spatial components of a putative error-processing system in the large-scale networks of the human brain. Most of this work has focused on the medial frontal cortex and an associated electrophysiological component known as the error-related negativity (or error negativity). Although the precise role, or roles, of this region still remain unknown, investigations of error processing have identified a cluster of modules in the medial frontal cortex involved in monitoring/maintaining ongoing behavior and motivating task sets. Other regions include bilateral anterior insula/inferior operculum and lateral prefrontal cortex. Recent work has begun to uncover how individual differences might affect the modules recruited for a task, in addition to the identification of associations between pathological states and aberrant error signals, leading to insights about possible mechanisms of neuropsychiatric illness. NEUROSCIENTIST 13(2):160—172, 2007.

Probability effects on stimulus evaluation and response processes

This study investigated the effects of probability information on response preparation and stimulus evaluation. Eight subjects responded with one hand to the target letter H and with the other to the target letter S. The target letter was surrounded by noise letters that were either the same as or different from the target letter. In 2 conditions, the targets were preceded by a warning stimulus unrelated to the target letter. In 2 other conditions, a warning letter predicted that the same letter or the opposite letter would appear as the imperative stimulus with .80 probability. Correct reaction times were faster and error rates were lower when imperative stimuli confirmed the predictions of the warning stimulus. Probability information affected (a) the preparation of motor responses during the foreperiod, (b) the development of expectancies for a particular target letter, and (c) a process sensitive to the identities of letter stimuli but not to their locations.

A functional neuroimaging study of motivation and executive function.

Executive functions, such as working memory, must intersect with functions that determine value for the organism. Functional imaging work in humans and single-unit recordings in non-human primates provide evidence that PFC might integrate motivational context with working memory. With functional magnetic resonance imaging (fMRI), we addressed the question of motivation and working memory, using a trial-related design in an object-working memory task. The design permitted the analysis of BOLD signal at separate stages, corresponding to encoding, maintenance, and retrieval. Subjects were motivated by a financial incentive during the task, such that they could gain a high or a low reward. The two different levels of reward also entailed greater or lesser risk of losing money for incorrect responses. In the high, relative to the low, reward condition, subjects shifted response bias, and showed a trend to greater sensitivity. We found main effects in fMRI BOLD signal for reward, which overlapped with BOLD effects for maintenance of information, in the right superior frontal sulcus and bilateral intraparietal sulcus. We also found an interaction between reward and retrieval from working memory in the right dorsolateral prefrontal cortex. Main effects of load and reward occurred in adjacent regions of the ventrolateral PFC during retrieval. The data demonstrate that when subjects perform a simple working memory task, financial incentives motivate performance and interact with some of the same neural networks that process various stages of working memory. Areas of overlap and interaction may integrate information about value, or they may represent a general effect of motivation increasing neural effort.

Medial Frontal Cortex Activity and Loss-Related Responses to Errors

Making an error elicits activity from brain regions that monitor performance, especially the medial frontal cortex (MFC). However, uncertainty exists about whether the posterior or anterior/rostral MFC processes errors and to what degree affective responses to errors are mediated in the MFC, specifically the rostral anterior cingulate cortex (rACC). To test the hypothesis that rACC mediates a type of affective response, we conceptualized affect in response to an error as a reaction to loss and amplified this response with a monetary penalty. While subjects performed a cognitive interference task during functional magnetic resonance imaging, hemodynamic activity in the rACC was significantly greater when subjects lost money as a result of an error compared with errors that did not lead to monetary loss. A significant interaction between the incentive conditions and error events demonstrated that the effect was not merely attributable to working harder to win (or not lose) money, although an effect of motivation was noted in the mid-MFC. Activation foci also occurred in similar regions of the posterior MFC for error and interference processing, which were not modulated by the incentive conditions. However, at the level of the individual subject, substantial functional variability occurred along the MFC during error processing, including foci in the rostral/anterior extent of the MFC not appearing in the group analysis. The findings support the hypothesis that the rostral extent of the MFC (rACC) processes loss-related responses to errors, and individual differences may account for some of the reported variation of error-related foci in the MFC.

Decomposing ERP time–frequency energy using PCA

OBJECTIVE Time-frequency transforms (TFTs) offer rich representations of event-related potential (ERP) activity, and thus add complexity. Data reduction techniques for TFTs have been slow to develop beyond time analysis of detail functions from wavelet transforms. Cohens class of TFTs based on the reduced interference distribution (RID) offer some benefits over wavelet TFTs, but do not offer the simplicity of detail functions from wavelet decomposition. The objective of the current approach is a data reduction method to extract succinct and meaningful events from both RID and wavelet TFTs. METHODS A general energy-based principal components analysis (PCA) approach to reducing TFTs is detailed. TFT surfaces are first restructured into vectors, recasting the data as a two-dimensional matrix amenable to PCA. PCA decomposition is performed on the two-dimensional matrix, and surfaces are then reconstructed. The PCA decomposition method is conducted with RID and Morlet wavelet TFTs, as well as with PCA for time and frequency domains separately. RESULTS Three simulated datasets were decomposed. These included Gabor logons and chirped signals. All simulated events were appropriately extracted from the TFTs using both wavelet and RID TFTs. Varying levels of noise were then added to the simulated data, as well as a simulated condition difference. The PCA-TFT method, particularly when used with RID TFTs, appropriately extracted the components and detected condition differences for signals where time or frequency domain analysis alone failed. Response-locked ERP data from a reaction time experiment was also decomposed. Meaningful components representing distinct neurophysiological activity were extracted from the ERP TFT data, including the error-related negativity (ERN). CONCLUSIONS Effective TFT data reduction was achieved. Activity that overlapped in time, frequency, and topography were effectively separated and extracted. Methodological issues involved in the application of PCA to TFTs are detailed, and directions for further development are discussed. SIGNIFICANCE The reported decomposition method represents a natural but significant extension of PCA into the TFT domain from the time and frequency domains alone. Evaluation of many aspects of this extension could now be conducted, using the PCA-TFT decomposition as a basis.