Dorsal Medial Prefrontal Cortex Plays a Necessary Role in Rapid Error Prediction in Humans

Activity in human dorsal anterior cingulate cortex (dACC) is correlated with errors, near-misses, and response conflict. Based on these observations, this region has been cast as playing a central role in models of error processing, conflict monitoring, and cognitive control. However, clear evidence that this region of the brain is necessary for these processes has been elusive. We studied the effects of damage to this region on four different error-related measures in five patients, and 19 healthy participants. Most error-related indices were not affected by such damage: patients had intact post-error slowing, and were able to report and to correct errors after they were made with accuracies comparable with the control group. However, all five patients were notably slow to correct errors, suggesting a deficit in on-line error prediction. This slowing was associated with impairment in the conscious prediction of error likelihood before a response. This finding constitutes important converging evidence for a critical role for human dACC in error monitoring, and sheds light on the selectivity and timing of the error-related process affected by dACC damage.

[1]  P. M. A. RABBITT,et al.  Error Correction Time without External Error Signals , 1966, Nature.

[2]  R. Angel Efference copy in the control of movement , 1976, Neurology.

[3]  M. Raichle,et al.  The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[6]  E. Donchin,et al.  Event-related brain potentials and error-related processing: an analysis of incorrect responses to go and no-go stimuli. , 1996, Psychophysiology.

[7]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[8]  M. Posner,et al.  Executive attention: Conflict, target detection, and cognitive control. , 1998 .

[9]  Jonathan D. Cohen,et al.  Conflict monitoring versus selection-for-action in anterior cingulate cortex , 1999, Nature.

[10]  A. Anderson,et al.  An fMRI study of stroop word-color interference: evidence for cingulate subregions subserving multiple distributed attentional systems , 1999, Biological Psychiatry.

[11]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[12]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

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

[14]  Adrian R. Willoughby,et al.  The Medial Frontal Cortex and the Rapid Processing of Monetary Gains and Losses , 2002, Science.

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

[16]  A. Turken,et al.  Dissociation between conflict detection and error monitoring in the human anterior cingulate cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[18]  E. Awh,et al.  Conflict adaptation effects in the absence of executive control , 2003, Nature Neuroscience.

[19]  Ziv M. Williams,et al.  Human anterior cingulate neurons and the integration of monetary reward with motor responses , 2004, Nature Neuroscience.

[20]  M. Herrmann,et al.  Source localization (LORETA) of the error-related-negativity (ERN/Ne) and positivity (Pe). , 2004, Brain research. Cognitive brain research.

[21]  M. Walton,et al.  Action sets and decisions in the medial frontal cortex , 2004, Trends in Cognitive Sciences.

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

[23]  Xun Liu,et al.  Common and distinct neural substrates of attentional control in an integrated Simon and spatial Stroop task as assessed by event-related fMRI , 2004, NeuroImage.

[24]  Jonathan D. Cohen,et al.  The neural basis of error detection: conflict monitoring and the error-related negativity. , 2004, Psychological review.

[25]  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.

[26]  Clay B. Holroyd,et al.  A mechanism for error detection in speeded response time tasks. , 2005, Journal of experimental psychology. General.

[27]  Joshua W. Brown,et al.  Learned Predictions of Error Likelihood in the Anterior Cingulate Cortex , 2005, Science.

[28]  Lauren M. Bylsma,et al.  The conflict adaptation effect: It’s not just priming , 2005, Cognitive, affective & behavioral neuroscience.

[29]  Stanislas Dehaene,et al.  Effortless control: executive attention and conscious feeling of mental effort are dissociable , 2005, Neuropsychologia.

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

[31]  M. Farah,et al.  Is anterior cingulate cortex necessary for cognitive control? , 2005, Brain : a journal of neurology.

[32]  Donald T. Stuss,et al.  Inhibitory Control is Slowed in Patients with Right Superior Medial Frontal Damage , 2006, Journal of Cognitive Neuroscience.

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

[34]  D. Kumaran,et al.  Frames, Biases, and Rational Decision-Making in the Human Brain , 2006, Science.

[35]  Lawrence R. Frank,et al.  Anterior cingulate activity modulates nonlinear decision weight function of uncertain prospects , 2006, NeuroImage.

[36]  Sam J. Gilbert,et al.  Cognitive functioning after medial frontal lobe damage including the anterior cingulate cortex: A preliminary investigation , 2006, Brain and Cognition.

[37]  C. Carter,et al.  Anterior cingulate cortex and conflict detection: An update of theory and data , 2007, Cognitive, affective & behavioral neuroscience.

[38]  Elisa Ciaramelli,et al.  The Regulation of Cognitive Control following Rostral Anterior Cingulate Cortex Lesion in Humans , 2007, Journal of Cognitive Neuroscience.

[39]  Joshua W. Brown,et al.  Risk prediction and aversion by anterior cingulate cortex , 2007, Cognitive, affective & behavioral neuroscience.

[40]  Timothy E. J. Behrens,et al.  Functional organization of the medial frontal cortex , 2007, Current Opinion in Neurobiology.

[41]  T. Shallice,et al.  Effects of focal frontal lesions on response inhibition. , 2006, Cerebral cortex.

[42]  Joshua W. Brown,et al.  A computational model of risk, conflict, and individual difference effects in the anterior cingulate cortex , 2008, Brain Research.

[43]  E. Procyk,et al.  Behavioral Shifts and Action Valuation in the Anterior Cingulate Cortex , 2008, Neuron.

[44]  Gilles Pourtois,et al.  Unavoidable errors: A spatio-temporal analysis of time-course and neural sources of evoked potentials associated with error processing in a speeded task , 2008, Neuropsychologia.

[45]  W. Notebaert,et al.  Hebbian learning of cognitive control: dealing with specific and nonspecific adaptation. , 2008, Psychological review.

[46]  Lesley K. Fellows,et al.  Medial prefrontal cortex plays a critical and selective role in ‘feeling of knowing’ meta-memory judgments , 2008, Neuropsychologia.

[47]  Kenneth Hugdahl,et al.  Prediction of human errors by maladaptive changes in event-related brain networks , 2008, Proceedings of the National Academy of Sciences.

[48]  Lesley K. Fellows,et al.  Lesion Evidence That Two Distinct Regions within Prefrontal Cortex are Critical for n-Back Performance in Humans , 2009, Journal of Cognitive Neuroscience.