Neural dynamics of error processing in medial frontal cortex

Adaptive behavior requires an organism to evaluate the outcome of its actions, such that future behavior can be adjusted accordingly and the appropriate response selected. During associative learning, the time at which such evaluative information is available changes as learning progresses, from the delivery of performance feedback early in learning to the execution of the response itself during learned performance. Here, we report a learning-dependent shift in the timing of activation in the rostral cingulate zone of the anterior cingulate cortex from external error feedback to internal error detection. This pattern of activity is seen only in the anterior cingulate, not in the pre-supplementary motor area. The dynamics of these reciprocal changes are consistent with the claim that the rostral cingulate zone is involved in response selection on the basis of the expected outcome of an action. Specifically, these data illustrate how the anterior cingulate receives evaluative information, indicating that an action has not produced the desired result.

[1]  K. Zilles,et al.  Differential Involvement of Parietal and Precentral Regions in Movement Preparation and Motor Intention , 2002, The Journal of Neuroscience.

[2]  Karl J. Friston,et al.  Human Brain Function, Second Edition , 2004 .

[3]  Karl J. Friston,et al.  Generalisability, Random Effects & Population Inference , 1998, NeuroImage.

[4]  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.

[5]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[6]  J Tanji,et al.  Role for cells in the presupplementary motor area in updating motor plans. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Karl J. Friston,et al.  Stochastic Designs in Event-Related fMRI , 1999, NeuroImage.

[8]  Parashkev Nachev,et al.  Volition and Conflict in Human Medial Frontal Cortex , 2005, Current Biology.

[9]  R. Passingham,et al.  Learning Arbitrary Visuomotor Associations: Temporal Dynamic of Brain Activity , 2001, NeuroImage.

[10]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[11]  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.

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

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

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

[15]  K. A. Hadland,et al.  The anterior cingulate and reward-guided selection of actions. , 2003, Journal of neurophysiology.

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

[17]  T. Shallice,et al.  Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. , 2003, Brain : a journal of neurology.

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

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

[21]  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.

[22]  Scott E. Maxwell,et al.  Designing Experiments and Analyzing Data , 1992 .

[23]  A. Dickinson Actions and habits: the development of behavioural autonomy , 1985 .

[24]  D Akkal,et al.  Comparison of neuronal activity in the rostral supplementary and cingulate motor areas during a task with cognitive and motor demands , 2002, The European journal of neuroscience.

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

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

[27]  Scott E. Maxwell,et al.  Designing Experiments and Analyzing Data , 1991 .

[28]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[29]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[30]  Jean-Baptiste Poline,et al.  Contrasts and Classical Inference , 2007 .

[31]  M. Posner The Cognitive Neuroscience of Attention , 2020 .

[32]  Clay B. Holroyd,et al.  Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals , 2004, Nature Neuroscience.

[33]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

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

[35]  Clay B. Holroyd,et al.  The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. , 2002, Psychological review.

[36]  A. Holmes Generalisability, random effects and population inference (abstract) , 1998 .

[37]  M. Walton,et al.  Interactions between decision making and performance monitoring within prefrontal cortex , 2004, Nature Neuroscience.

[38]  S. Wise,et al.  Arbitrary associations between antecedents and actions , 2000, Trends in Neurosciences.

[39]  Karl J. Friston,et al.  Human Brain Function , 1997 .

[40]  Michael G. H. Coles,et al.  Anterior cingulate cortex, selection for action, and error processing , 2004 .

[41]  Keiji Tanaka,et al.  The role of the medial prefrontal cortex in achieving goals , 2004, Current Opinion in Neurobiology.

[42]  K Friston,et al.  Signal-, set- and movement-related activity in the human brain: an event-related fMRI study. , 1999, Cerebral cortex.

[43]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.