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.

[1]  H. Garavan,et al.  Dissociable Executive Functions in the Dynamic Control of Behavior: Inhibition, Error Detection, and Correction , 2002, NeuroImage.

[2]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[3]  A. Engel,et al.  Trial-by-Trial Coupling of Concurrent Electroencephalogram and Functional Magnetic Resonance Imaging Identifies the Dynamics of Performance Monitoring , 2005, The Journal of Neuroscience.

[4]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[5]  D. Meyer,et al.  A Neural System for Error Detection and Compensation , 1993 .

[6]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[7]  Raymond J. Dolan,et al.  Anterior cingulate activity during error and autonomic response , 2005, NeuroImage.

[8]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[9]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[10]  P. Rabbitt Errors and error correction in choice-response tasks. , 1966, Journal of experimental psychology.

[11]  H. Critchley,et al.  Neural Activity Relating to Generation and Representation of Galvanic Skin Conductance Responses: A Functional Magnetic Resonance Imaging Study , 2000, The Journal of Neuroscience.

[12]  J. Hohnsbein,et al.  ERP components on reaction errors and their functional significance: a tutorial , 2000, Biological Psychology.

[13]  B. Fischer,et al.  Separate populations of visually guided saccades in humans: reaction times and amplitudes , 2004, Experimental Brain Research.

[14]  D. Yves von Cramon,et al.  Neuroimaging of Performance Monitoring: Error Detection and Beyond , 2004, Cortex.

[15]  Katja Fiehler,et al.  Cardiac responses to error processing and response conflict , 2004 .

[16]  John J. Foxe,et al.  The Anterior Cingulate and Error Avoidance , 2006, The Journal of Neuroscience.

[17]  J. Findlay,et al.  Express saccades: is there a separate population in humans? , 2004, Experimental Brain Research.

[18]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[19]  K. R. Ridderinkhof,et al.  Error-related brain potentials are differentially related to awareness of response errors: evidence from an antisaccade task. , 2001, Psychophysiology.

[20]  H. Critchley Neural mechanisms of autonomic, affective, and cognitive integration , 2005, The Journal of comparative neurology.

[21]  M. Posner,et al.  Localization of a Neural System for Error Detection and Compensation , 1994 .

[22]  Eveline A. Crone,et al.  Cardiac and electro-cortical responses to performance feedback reflect different aspects of feedback processing. , 2004 .

[23]  D. V. Cramon,et al.  Subprocesses of Performance Monitoring: A Dissociation of Error Processing and Response Competition Revealed by Event-Related fMRI and ERPs , 2001, NeuroImage.

[24]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[25]  D. V. von Cramon,et al.  Neural correlates of error detection and error correction: is there a common neuroanatomical substrate? , 2004, The European journal of neuroscience.

[26]  R. Simons,et al.  To err is autonomic: error-related brain potentials, ANS activity, and post-error compensatory behavior. , 2003, Psychophysiology.

[27]  Burkhart Fischer,et al.  Effects of procues on error rate and reaction times of antisaccades in human subjects , 1996, Experimental Brain Research.

[28]  Michael Falkenstein,et al.  Errors, Conflicts, and the Brain , 2004 .

[29]  A. Verberne,et al.  Cortical Modulation of theCardiovascular System , 1998, Progress in Neurobiology.

[30]  Hugo D. Critchley,et al.  Activity in the human brain predicting differential heart rate responses to emotional facial expressions , 2005, NeuroImage.

[31]  G Lohmann,et al.  LIPSIA--a new software system for the evaluation of functional magnetic resonance images of the human brain. , 2001, Computerized medical imaging and graphics : the official journal of the Computerized Medical Imaging Society.

[32]  S. Petersen,et al.  Characterizing the Hemodynamic Response: Effects of Presentation Rate, Sampling Procedure, and the Possibility of Ordering Brain Activity Based on Relative Timing , 2000, NeuroImage.

[33]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[34]  C. Brunia,et al.  Psychophysiological brain research. , 1993 .

[35]  C. Carter,et al.  The Timing of Action-Monitoring Processes in the Anterior Cingulate Cortex , 2002, Journal of Cognitive Neuroscience.

[36]  Thérèse J. M. Overbeek,et al.  Dissociable Components of Error Processing on the Functional Significance of the Pe Vis-à-vis the Ern/ne Performance Monitoring Processes Reflected in the Ne and Pe Review of Studies That Report Both Ne and Pe: Associations and Dissociations Pharmacological Effects , 2022 .

[37]  Hugh Garavan,et al.  Individual differences in error processing: a review and reanalysis of three event-related fMRI studies using the GO/NOGO task. , 2004, Cerebral cortex.

[38]  D. V. von Cramon,et al.  Error Monitoring Using External Feedback: Specific Roles of the Habenular Complex, the Reward System, and the Cingulate Motor Area Revealed by Functional Magnetic Resonance Imaging , 2003, The Journal of Neuroscience.

[39]  J. Tanji,et al.  Role for cingulate motor area cells in voluntary movement selection based on reward. , 1998, Science.

[40]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[41]  T. Endrass,et al.  Error Awareness in a Saccade Countermanding Task , 2005 .

[42]  Eveline A. Crone,et al.  Cardiac concomitants of feedback processing , 2003, Biological Psychology.

[43]  John J. Foxe,et al.  Neural mechanisms involved in error processing: A comparison of errors made with and without awareness , 2005, NeuroImage.