Unconscious Errors Enhance Prefrontal-Occipital Oscillatory Synchrony

The medial prefrontal cortex (MFC) is critical for our ability to learn from previous mistakes. Here we provide evidence that neurophysiological oscillatory long-range synchrony is a mechanism of post-error adaptation that occurs even without conscious awareness of the error. During a visually signaled Go/No-Go task in which half of the No-Go cues were masked and thus not consciously perceived, response errors enhanced tonic (i.e., over 1–2 s) oscillatory synchrony between MFC and occipital cortex (OCC) leading up to and during the subsequent trial. Spectral Granger causality analyses demonstrated that MFC → OCC directional synchrony was enhanced during trials following both conscious and unconscious errors, whereas transient stimulus-induced occipital → MFC directional synchrony was independent of errors in the previous trial. Further, the strength of pre-trial MFC-occipital synchrony predicted individual differences in task performance. Together, these findings suggest that synchronous neurophysiological oscillations are a plausible mechanism of MFC-driven cognitive control that is independent of conscious awareness.

[1]  P. Holland,et al.  Robust regression using iteratively reweighted least-squares , 1977 .

[2]  James T. Townsend,et al.  The Stochastic Modeling of Elementary Psychological Processes , 1983 .

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

[4]  Richard L. Abrams,et al.  Three Cognitive Markers of Unconscious Semantic Activation , 1996, Science.

[5]  Yves Rossetti,et al.  Implicit Short-Lived Motor Representations of Space in Brain Damaged and Healthy Subjects , 1998, Consciousness and Cognition.

[6]  R. Elliott,et al.  Neural Response during Preference and Memory Judgments for Subliminally Presented Stimuli: A Functional Neuroimaging Study , 1998, The Journal of Neuroscience.

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

[8]  W. Klimesch.  EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[9]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[10]  V. Lamme,et al.  The distinct modes of vision offered by feedforward and recurrent processing , 2000, Trends in Neurosciences.

[11]  R. Knight,et al.  Prefrontal modulation of visual processing in humans , 2000, Nature Neuroscience.

[12]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[13]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[14]  J. Martinerie,et al.  Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony , 2001, Journal of Neuroscience Methods.

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

[16]  S. Dehaene,et al.  Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework , 2001, Cognition.

[17]  W. Gehring,et al.  Functions of the Medial Frontal Cortex in the Processing of Conflict and Errors , 2001, The Journal of Neuroscience.

[18]  J. Schwarzbach,et al.  Different time courses for visual perception and action priming , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Leslie G. Ungerleider,et al.  Neuroimaging Studies of Attention: From Modulation of Sensory Processing to Top-Down Control , 2003, The Journal of Neuroscience.

[20]  K. R. Ridderinkhof,et al.  Errors are foreshadowed in brain potentials associated with action monitoring in cingulate cortex in humans , 2003, Neuroscience Letters.

[21]  Wilfried Kunde,et al.  Sequential modulations of stimulus-response correspondence effects depend on awareness of response conflict , 2003, Psychonomic bulletin & review.

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

[23]  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.

[24]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

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

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

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

[28]  B. Burle,et al.  The modulation of the Ne-like wave on correct responses foreshadows errors , 2004, Neuroscience Letters.

[29]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[30]  S. Shipp.  The brain circuitry of attention , 2004, Trends in Cognitive Sciences.

[31]  S. Nieuwenhuis,et al.  Neural mechanisms of attention and control: losing our inhibitions? , 2005, Nature Neuroscience.

[32]  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.

[33]  T. Egner,et al.  Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information , 2005, Nature Neuroscience.

[34]  S. Dehaene,et al.  A direct intracranial record of emotions evoked by subliminal words. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Christopher Summerfield,et al.  Functional coupling between frontal and parietal lobes during recognition memory , 2005, Neuroreport.

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

[37]  Jürgen Kayser,et al.  Principal components analysis of Laplacian waveforms as a generic method for identifying ERP generator patterns: I. Evaluation with auditory oddball tasks , 2006, Clinical Neurophysiology.

[38]  E. Kandel,et al.  Resolving Emotional Conflict: A Role for the Rostral Anterior Cingulate Cortex in Modulating Activity in the Amygdala , 2006, Neuron.

[39]  Matthew Davidson,et al.  Context Modulates Early Stimulus Processing when Resolving Stimulus-response Conflict , 2006, Journal of Cognitive Neuroscience.

[40]  Vinod Menon,et al.  Where and When the Anterior Cingulate Cortex Modulates Attentional Response: Combined fMRI and ERP Evidence , 2006, Journal of Cognitive Neuroscience.

[41]  V. Lamme.  Towards a true neural stance on consciousness , 2006, Trends in Cognitive Sciences.

[42]  E. Kandel,et al.  Resolving Emotional Conflict: A Role for the Rostral Anterior Cingulate Cortex in Modulating Activit , 2006 .

[43]  S. Dehaene,et al.  Subliminal words durably affect neuronal activity , 2007, Neuroreport.

[44]  Anna C Nobre,et al.  Subsecond Changes in Top–Down Control Exerted by Human Medial Frontal Cortex during Conflict and Action Selection: A Combined Transcranial Magnetic Stimulation–Electroencephalography Study , 2007, The Journal of Neuroscience.

[45]  W. Singer,et al.  The gamma cycle , 2007, Trends in Neurosciences.

[46]  T. Endrass,et al.  ERP correlates of conscious error recognition: aware and unaware errors in an antisaccade task , 2007, The European journal of neuroscience.

[47]  Michael X. Cohen,et al.  Behavioral / Systems / Cognitive Reinforcement Learning Signals Predict Future Decisions , 2007 .

[48]  P. Nunez,et al.  EEG and MEG coherence: Measures of functional connectivity at distinct spatial scales of neocortical dynamics , 2007, Journal of Neuroscience Methods.

[49]  S. Dehaene,et al.  Levels of processing during non-conscious perception: a critical review of visual masking , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

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

[52]  Michael X. Cohen,et al.  Reward expectation modulates feedback-related negativity and EEG spectra , 2007, NeuroImage.

[53]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[54]  S. Bressler,et al.  Response preparation and inhibition: The role of the cortical sensorimotor beta rhythm , 2008, Neuroscience.

[55]  T. Egner.  Multiple conflict-driven control mechanisms in the human brain , 2008, Trends in Cognitive Sciences.

[56]  Jie Cui,et al.  2008 Special Issue: BSMART: A Matlab/C toolbox for analysis of multichannel neural time series , 2008 .

[57]  Michael X. Cohen,et al.  Neurocomputational mechanisms of reinforcement-guided learning in humans: A review , 2008, Cognitive, affective & behavioral neuroscience.

[58]  Bijan Pesaran,et al.  Free choice activates a decision circuit between frontal and parietal cortex , 2008, Nature.

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

[60]  M. Bar,et al.  The effects of priming on frontal-temporal communication , 2008, Proceedings of the National Academy of Sciences.

[61]  G. Woodman,et al.  The Effect of Visual Search Efficiency on Response Preparation , 2008, Psychological science.

[62]  W. Klimesch,et al.  What does phase information of oscillatory brain activity tell us about cognitive processes? , 2008, Neuroscience & Biobehavioral Reviews.

[63]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[64]  H. Lau.  Volition and the functions of consciousness , 2009, Neuroscience Research.

[65]  H. Lau.  Volition and the Function of Consciousness , 2009 .

[66]  J. Fell,et al.  The specific contribution of neuroimaging versus neurophysiological data to understanding cognition , 2009, Behavioural Brain Research.

[67]  Michael X. Cohen,et al.  Nuclei Accumbens Phase Synchrony Predicts Decision-Making Reversals Following Negative Feedback , 2009, The Journal of Neuroscience.

[68]  Peter Ullsperger,et al.  Dissociable medial frontal negativities from a common monitoring system for self- and externally caused failure of goal achievement , 2009, NeuroImage.

[69]  S. Dehaene,et al.  Converging Intracranial Markers of Conscious Access , 2009, PLoS biology.

[70]  Cameron S. Carter,et al.  Conflict-related activity in the caudal anterior cingulate cortex in the absence of awareness , 2009, Biological Psychology.

[71]  D. Paré,et al.  Coherent gamma oscillations couple the amygdala and striatum during learning , 2009, Nature Neuroscience.

[72]  John J. B. Allen,et al.  Prelude to and Resolution of an Error: EEG Phase Synchrony Reveals Cognitive Control Dynamics during Action Monitoring , 2009, The Journal of Neuroscience.