Remedial action and feedback processing in a time-estimation task: Evidence for a role of the rostral cingulate zone in behavioral adjustments without learning

The present study examined the role of the rostral cingulate zone (RCZ) in feedback processing, and especially focused on effects of modality of the feedback stimulus and remedial action. Participants performed a time-estimation task in which they had to estimate a 1-second interval. After the estimation participants received verbal (correct/false) or facial (fearful face/happy face) feedback. Percentage of positive and negative feedback was kept at 50% by dynamically adjusting the interval in which estimations were labeled correct. Contrary to predictions of the reinforcement learning theory, which predicts more RCZ activation when the outcome of behavior is worse than expected, we found that the RCZ was more active after positive feedback than after negative feedback, independent of the modality of the feedback stimulus. More in line with the suggested role of the RCZ in reinforcement learning was the finding that the RCZ was more active after negative feedback that was followed by a correct adjustment as compared to negative feedback followed by an incorrect adjustment. Both findings can be explained in terms of the RCZ being involved in facilitating remedial action as opposed to the suggested signaling function (outcome is worse than expected) proposed by the reinforcement learning theory.

[1]  Norbert Kathmann,et al.  Neural correlates of error awareness , 2007, NeuroImage.

[2]  John J. Foxe,et al.  Avoiding another mistake: Error and posterror neural activity associated with adaptive posterror behavior change , 2007, Cognitive, affective & behavioral neuroscience.

[3]  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.

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

[5]  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.

[6]  E. Murray The amygdala, reward and emotion , 2007, Trends in Cognitive Sciences.

[7]  M. Botvinick,et al.  Error-likelihood prediction in the medial frontal cortex: a critical evaluation. , 2007, Cerebral cortex.

[8]  Daniel Ansari,et al.  Using developmental trajectories to understand developmental disorders. , 2009, Journal of speech, language, and hearing research : JSLHR.

[9]  Edward E. Smith,et al.  Neuroimaging studies of working memory: , 2003, Cognitive, affective & behavioral neuroscience.

[10]  Clay B. Holroyd,et al.  Knowing good from bad: differential activation of human cortical areas by positive and negative outcomes , 2005, The European journal of neuroscience.

[11]  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.

[12]  William Joseph Gehring The Error-Related Negativity: Evidence for a Neural Mechanism for Error-Related Processing , 1992 .

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

[14]  Michael G. H. Coles,et al.  What if I told you: "You were wrong"? Brain potentials and behavioral adjustments elicited by feedback in a time-estimation task , 2004 .

[15]  G. Pourtois,et al.  Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging , 2007, Neuropsychologia.

[16]  M. W. Molen,et al.  Acute tryptophan depletion in healthy males attenuates phasic cardiac slowing but does not affect electro-cortical response to negative feedback , 2008, Psychopharmacology.

[17]  J. Hohnsbein,et al.  Effects of crossmodal divided attention on late ERP components. II. Error processing in choice reaction tasks. , 1991, Electroencephalography and clinical neurophysiology.

[18]  C. Braun,et al.  Event-Related Brain Potentials Following Incorrect Feedback in a Time-Estimation Task: Evidence for a Generic Neural System for Error Detection , 1997, Journal of Cognitive Neuroscience.

[19]  K. A. Hadland,et al.  Role of the human medial frontal cortex in task switching: a combined fMRI and TMS study. , 2002, Journal of neurophysiology.

[20]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

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

[22]  Carolyn C. Meltzer,et al.  Verbal and spatial working memory in older individuals: A positron emission tomography study , 2006, Brain Research.

[23]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

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

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

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

[27]  Cameron S. Carter,et al.  Errors without conflict: Implications for performance monitoring theories of anterior cingulate cortex , 2004, Brain and Cognition.

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

[29]  Ivan Toni,et al.  Neural dynamics of error processing in medial frontal cortex , 2005, NeuroImage.

[30]  Eveline A. Crone,et al.  Phasic heart rate responses to performance feedback in a time production task: effects of information versus valence , 2004, Biological Psychology.

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

[32]  A. Nobre,et al.  Where and When to Pay Attention: The Neural Systems for Directing Attention to Spatial Locations and to Time Intervals as Revealed by Both PET and fMRI , 1998, The Journal of Neuroscience.

[33]  T. Robbins,et al.  Defining the Neural Mechanisms of Probabilistic Reversal Learning Using Event-Related Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[34]  Clay B. Holroyd,et al.  Reward prediction error signals associated with a modified time estimation task. , 2007, Psychophysiology.

[35]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[36]  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.

[37]  S. Maxwell,et al.  On Using Analysis Of Covariance In Repeated Measures Designs. , 1981, Multivariate behavioral research.