Conflict-related activity in the caudal anterior cingulate cortex in the absence of awareness

The caudal anterior cingulate cortex (cACC) is thought to be involved in performance monitoring, as conflict and error-related activity frequently co-localize in this area. Recent results suggest that these effects may be differentially modulated by awareness. To clarify the role of awareness in performance monitoring by the cACC, we used rapid event-related fMRI to examine the cACC activity while subjects performed a dual task: a delayed recognition task and a serial response task (SRT) with an implicit probabilistic learning rule (i.e. the stimulus location followed a probabilistic sequence of which the subjects were unaware). Task performance confirmed that the location sequence was learned implicitly. Even though we found no evidence of awareness for the presence of the sequence, imaging data revealed increased cACC activity during correct trials which violated the sequence (high-conflict), relative to trials when stimuli followed the sequence (low conflict). Errors made with awareness also activated the same brain region. These results suggest that the performance monitoring function of the cACC extends beyond detection of errors made with or without awareness, and involves detection of multiple responses even when they are outside of awareness.

[1]  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.

[2]  Clay B. Holroyd,et al.  Why is there an ERN/Ne on correct trials? Response representations, stimulus-related components, and the theory of error-processing , 2001, Biological Psychology.

[3]  Matthew Flatt,et al.  PsyScope: An interactive graphic system for designing and controlling experiments in the psychology laboratory using Macintosh computers , 1993 .

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

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

[6]  Jonathan D. Cohen,et al.  Dissociating working memory from task difficulty in human prefrontal cortex , 1997, Neuropsychologia.

[7]  Tim Curran,et al.  Higher-Order Associative Learning in Amnesia: Evidence from the Serial Reaction Time Task , 1997, Journal of Cognitive Neuroscience.

[8]  R. Passingham,et al.  Unconscious Activation of the Cognitive Control System in the Human Prefrontal Cortex , 2007, The Journal of Neuroscience.

[9]  T. Braver,et al.  Anterior cingulate cortex and response conflict: effects of frequency, inhibition and errors. , 2001, Cerebral cortex.

[10]  L. Jiménez,et al.  Implicit Sequence Learning with Competing Explicit Cues , 2001, The Quarterly journal of experimental psychology. A, Human experimental psychology.

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

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

[13]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

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

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

[16]  Scott T. Grafton,et al.  Automated image registration: I. General methods and intrasubject, intramodality validation. , 1998, Journal of computer assisted tomography.

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

[18]  R. Dolan,et al.  How the Brain Translates Money into Force: A Neuroimaging Study of Subliminal Motivation , 2007, Science.

[19]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

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

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

[22]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[23]  James L. McClelland,et al.  Learning the structure of event sequences. , 1991, Journal of experimental psychology. General.

[24]  B. Kopp,et al.  N2, P3 and the lateralized readiness potential in a nogo task involving selective response priming. , 1996, Electroencephalography and clinical neurophysiology.

[25]  S. Rauch,et al.  The counting stroop: An interference task specialized for functional neuroimaging—validation study with functional MRI , 1998, Human brain mapping.

[26]  K. R. Ridderinkhof,et al.  Frontal Cortex Mediates Unconsciously Triggered Inhibitory Control , 2008, The Journal of Neuroscience.

[27]  T. Treasure.  Where did I go wrong? , 1994, The Lancet.

[28]  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.

[29]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[30]  Cheryl L. Dickter,et al.  Strategic control and medial frontal negativity: beyond errors and response conflict. , 2005, Psychophysiology.

[31]  M. Coles,et al.  Performance monitoring in a confusing world: error-related brain activity, judgments of response accuracy, and types of errors. , 2000, Journal of experimental psychology. Human perception and performance.

[32]  M. Milham,et al.  Anterior cingulate cortex: An fMRI analysis of conflict specificity and functional differentiation , 2005, Human brain mapping.

[33]  Michael Friendly,et al.  The Toronto Word Pool: Norms for imagery, concreteness, orthographic variables, and grammatical usage for 1,080 words , 1982 .

[34]  M. Leboyer,et al.  Conscious and subliminal conflicts in normal subjects and patients with schizophrenia: The role of the anterior cingulate , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[35]  T. Woodward,et al.  The Role of the Anterior Cingulate Cortex in Conflict Processing: Evidence from Reverse Stroop Interference , 2001, NeuroImage.

[36]  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.

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

[38]  H. Mayberg,et al.  An ERP study of the temporal course of the Stroop color-word interference effect , 2000, Neuropsychologia.

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

[40]  Jin Fan,et al.  Cognitive and Brain Consequences of Conflict , 2003, NeuroImage.

[41]  S. Dehaene,et al.  Imaging unconscious semantic priming , 1998, Nature.

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

[43]  A M Dale,et al.  Randomized event‐related experimental designs allow for extremely rapid presentation rates using functional MRI , 1998, Neuroreport.

[44]  M. Nissen,et al.  Attentional requirements of learning: Evidence from performance measures , 1987, Cognitive Psychology.

[45]  Terry M. Peters,et al.  3D statistical neuroanatomical models from 305 MRI volumes , 1993, 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference.

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

[47]  Cameron S. Carter,et al.  Overactive Action Monitoring in Obsessive-Compulsive Disorder , 2003, Psychological science.

[48]  H Garavan,et al.  A midline dissociation between error-processing and response-conflict monitoring , 2003, NeuroImage.

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

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

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

[52]  G. Berns,et al.  Brain regions responsive to novelty in the absence of awareness. , 1997, Science.

[53]  M. Coles,et al.  "Where did I go wrong?" A psychophysiological analysis of error detection. , 1995, Journal of experimental psychology. Human perception and performance.

[54]  B. Kopp,et al.  N200 in the flanker task as a neurobehavioral tool for investigating executive control. , 1996, Psychophysiology.

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

[56]  V. Tronnier,et al.  Subthalamic nucleus stimulation affects striato-anterior cingulate cortex circuit in a response conflict task: a PET study. , 2002, Brain : a journal of neurology.

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