Performance Monitoring in the Anterior Cingulate is Not All Error Related: Expectancy Deviation and the Representation of Action-Outcome Associations

Several converging lines of evidence suggest that the anterior cingulate cortex (ACC) is selectively involved in error detection or evaluation of poor performance. Here we challenge this notion by presenting event-related potential (ERP) evidence that the feedback-elicited error-related negativity, an ERP component attributed to the ACC, can be elicited by positive feedback when a person is expecting negative feedback and vice versa. These results suggest that performance monitoring in the ACC is not limited to error processing. We propose that the ACC acts as part of a more general performance-monitoring system that is activated by violations in expectancy. Further, we propose that the common observation of increased ACC activity elicited by negative events could be explained by an overoptimistic bias in generating expectations of performance. These results could shed light into neurobehavioral disorders, such as depression and mania, associated with alterations in performance monitoring and also in judgments of self-related events.

[1]  J. Bolam,et al.  Uniform Inhibition of Dopamine Neurons in the Ventral Tegmental Area by Aversive Stimuli , 2004, Science.

[2]  Rogier B. Mars,et al.  De Bruijn ERA, Mars RB, & Hulstijn W It wasn't me... or was it? How false feedback affects performance , 2004 .

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

[4]  Clay B. Holroyd,et al.  Errors in reward prediction are re£ected in the event-related brain potential , 2003 .

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

[6]  Aziz M. Ulug,et al.  Differential cingulate and caudate activation following unexpected nonrewarding stimuli , 2004, NeuroImage.

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

[8]  M. Botvinick,et al.  Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[9]  X. Mai,et al.  “Aha!” effects in a guessing riddle task: An event‐related potential study , 2004, Human brain mapping.

[10]  D. Tucker,et al.  Electrophysiological Responses to Errors and Feedback in the Process of Action Regulation , 2003, Psychological science.

[11]  J. Seamans,et al.  Synaptic basis of persistent activity in prefrontal cortex in vivo and in organotypic cultures. , 2003, Cerebral cortex.

[12]  B. Vogt,et al.  Pain Processing in Four Regions of Human Cingulate Cortex Localized with Co‐registered PET and MR Imaging , 1996, The European journal of neuroscience.

[13]  J. Driver,et al.  Control of Cognitive Processes: Attention and Performance XVIII , 2000 .

[14]  Clay B. Holroyd,et al.  ERP correlates of feedback and reward processing in the presence and absence of response choice. , 2005, Cerebral cortex.

[15]  K. Kiehl,et al.  Error processing and the rostral anterior cingulate: an event-related fMRI study. , 2000, Psychophysiology.

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

[17]  Christopher C Lapish,et al.  Mesocortical Dopamine Neurons Operate in Distinct Temporal Domains Using Multimodal Signaling , 2005, The Journal of Neuroscience.

[18]  Daniel G. Dillon,et al.  Individual differences in reinforcement learning: Behavioral, electrophysiological, and neuroimaging correlates , 2008, NeuroImage.

[19]  A. Sanfey,et al.  Independent Coding of Reward Magnitude and Valence in the Human Brain , 2004, The Journal of Neuroscience.

[20]  M Eimer,et al.  Explicit and implicit learning of event sequences: evidence from event-related brain potentials. , 1996, Journal of experimental psychology. Learning, memory, and cognition.

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

[22]  Joshua W. Brown,et al.  Performance Monitoring by the Anterior Cingulate Cortex During Saccade Countermanding , 2003, Science.

[23]  CR Yang,et al.  Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  K. R. Ridderinkhof,et al.  Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning , 2004, Brain and Cognition.

[25]  Michael J. Frank,et al.  Error-Related Negativity Predicts Reinforcement Learning and Conflict Biases , 2005, Neuron.

[26]  Jane Epstein,et al.  Increased anterior cingulate and caudate activity in bipolar mania , 2000, Biological Psychiatry.

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

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

[29]  M. Ungless.  Dopamine: the salient issue , 2004, Trends in Neurosciences.

[30]  Jonathan D. Cohen,et al.  Anterior Cingulate Cortex, Conflict Monitoring, and Levels of Processing , 2001, NeuroImage.

[31]  Dale T. Miller,et al.  Self-serving biases in the attribution of causality: Fact or fiction? , 1975 .

[32]  Markus Kiefer,et al.  Error processing in major depressive disorder: evidence from event-related potentials. , 2006, Journal of psychiatric research.

[33]  M. Kazès,et al.  Initiation and supervisory processes in schizophrenia and depression , 1998, Schizophrenia Research.

[34]  Caroline F. Zink,et al.  Human striatal activation reflects degree of stimulus saliency , 2006, NeuroImage.

[35]  Mark S. Gilzenrat,et al.  A Systems-Level Perspective on Attention and Cognitive Control: Guided Activation, Adaptive Gating, Conflict Monitoring, and Exploitation versus Exploration. , 2004 .

[36]  Clay B. Holroyd,et al.  A note on the oddball N200 and the feedback ERN , 2004 .

[37]  Marjan Jahanshahi,et al.  Basal ganglia, dopamine and temporal processing: Performance on three timing tasks on and off medication in Parkinson’s disease , 2008, Brain and Cognition.

[38]  Jonathan D. Cohen,et al.  On the Control of Control: The Role of Dopamine in Regulating Prefrontal Function and Working Memory , 2007 .

[39]  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.

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

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

[42]  E. Halgren,et al.  Responses of Human Anterior Cingulate Cortex Microdomains to Error Detection, Conflict Monitoring, Stimulus-Response Mapping, Familiarity, and Orienting , 2005, The Journal of Neuroscience.

[43]  P. Fox,et al.  Cingulate function in depression: a potential predictor of treatment response , 1997, Neuroreport.

[44]  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.

[45]  T. Paus.  Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[46]  Scott A. Shappell,et al.  Psychophysiology of N200/N400: A Review and Classification Scheme , 1991 .

[47]  Clay B. Holroyd,et al.  Brain potentials associated with expected and unexpected good and bad outcomes. , 2005, Psychophysiology.

[48]  B. Lewis,et al.  Ventral tegmental area afferents to the prefrontal cortex maintain membrane potential 'up' states in pyramidal neurons via D(1) dopamine receptors. , 2000, Cerebral cortex.

[49]  William J. Tays,et al.  Aging and electrocortical response to error feedback during a spatial learning task. , 2008, Psychophysiology.

[50]  William Perry,et al.  Sensorimotor gating deficits in bipolar disorder patients with acute psychotic mania , 2001, Biological Psychiatry.

[51]  Phan Luu,et al.  The Anterior Cingulate Cortex : Regulating Actions in Context , 2004 .

[52]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

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

[54]  Andrew M. J. Young,et al.  Increased extracellular dopamine in nucleus accumbens in response to unconditioned and conditioned aversive stimuli: studies using 1 min microdialysis in rats , 2004, Journal of Neuroscience Methods.

[55]  Margot J. Taylor,et al.  Guidelines for using human event-related potentials to study cognition: recording standards and publication criteria. , 2000, Psychophysiology.

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

[57]  W Gaebel,et al.  Cingulate function in depression. , 1997, Neuroreport.

[58]  J. Seamans,et al.  The principal features and mechanisms of dopamine modulation in the prefrontal cortex , 2004, Progress in Neurobiology.

[59]  J. Horvitz.  Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events , 2000, Neuroscience.

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

[61]  Sander Nieuwenhuis,et al.  Mediofrontal negativities in the absence of responding. , 2005, Brain research. Cognitive brain research.

[62]  B. Richmond,et al.  Anterior Cingulate: Single Neuronal Signals Related to Degree of Reward Expectancy , 2002, Science.

[63]  Markus Kiefer,et al.  The effect of erroneous responses on response monitoring in patients with major depressive disorder: a study with event-related potentials. , 2004, Psychophysiology.

[64]  Timothy E. J. Behrens,et al.  Choice, uncertainty and value in prefrontal and cingulate cortex , 2008, Nature Neuroscience.

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

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

[67]  Jonathan D. Cohen,et al.  Resting anterior cingulate activity and abnormal responses to errors in subjects with elevated depressive symptoms: A 128‐channel EEG study , 2006, Human brain mapping.

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

[69]  Clay B. Holroyd,et al.  Implementation of error-processing in the human anterior cingulate cortex: a source analysis of the magnetic equivalent of the error-related negativity , 2003, Biological Psychology.

[70]  A. Rodríguez-Fornells,et al.  Brain potentials related to self-generated and external information used for performance monitoring , 2005, Clinical Neurophysiology.

[71]  J D Cohen,et al.  A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior. , 1990, Science.

[72]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

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

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

[75]  H. Bokura,et al.  Electrophysiological correlates for response inhibition in a Go/NoGo task , 2001, Clinical Neurophysiology.

[76]  M. Ullsperger.  Performance monitoring in neurological and psychiatric patients. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[77]  T. Gilovich,et al.  Biased evaluation and persistence in gambling. , 1983, Journal of personality and social psychology.

[78]  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.

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

[80]  Clay B. Holroyd,et al.  Reinforcement-related brain potentials from medial frontal cortex: origins and functional significance , 2004, Neuroscience & Biobehavioral Reviews.

[81]  A. Grace,et al.  Stimulation of D1-type dopamine receptors enhances excitability in prefrontal cortical pyramidal neurons in a state-dependent manner , 2001, Neuroscience.

[82]  E. Procyk,et al.  Anterior cingulate error‐related activity is modulated by predicted reward , 2005, The European journal of neuroscience.

[83]  T. Robbins,et al.  Emotional bias and inhibitory control processes in mania and depression , 1999, Psychological Medicine.

[84]  P. Redgrave,et al.  Is the short-latency dopamine response too short to signal reward error? , 1999, Trends in Neurosciences.

[85]  David A Lewis,et al.  Neural and behavioral substrates of mood and mood regulation , 2002, Biological Psychiatry.

[86]  Martin P Paulus,et al.  Increased sensitivity to error during decision-making in bipolar disorder patients with acute mania. , 2004, Journal of affective disorders.

[87]  Marco Steinhauser,et al.  Is the Error-related Negativity Amplitude Related to Error Detectability? Evidence from Effects of Different Error Types , 2008, Journal of Cognitive Neuroscience.

[88]  Masataka Watanabe,et al.  Prefrontal and cingulate unit activity during timing behavior in the monkey , 1979, Brain Research.

[89]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[90]  G. Pagnoni,et al.  Human Striatal Responses to Monetary Reward Depend On Saliency , 2004, Neuron.

[91]  Keiji Tanaka,et al.  Neuronal Correlates of Goal-Based Motor Selection in the Prefrontal Cortex , 2003, Science.

[92]  Daniel Durstewitz,et al.  Comparing the prefrontal cortex of rats and primates: Insights from electrophysiology , 2008, Neurotoxicity Research.

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