Conflict awareness dissociates theta-band neural dynamics of the medial frontal and lateral frontal cortex during trial-by-trial cognitive control

Recent findings have refuted the common assumption that executive control functions of the prefrontal cortex exclusively operate consciously, suggesting that many, if not all, cognitive processes could potentially operate unconsciously. However, although many cognitive functions can be launched unconsciously, several theoretical models of consciousness assume that there are crucial qualitative differences between conscious and unconscious processes. We hypothesized that the potential benefit of awareness in cognitive control mechanisms might become apparent when high control has to be maintained across time and requires the interaction between a set of distant frontal brain regions. To test this, we extracted oscillatory power dynamics from electroencephalographic data recorded while participants performed a task in which conflict awareness was manipulated by masking the conflict-inducing stimulus. We observed that instantaneous conflict as well as across trial conflict adaptation mechanisms were associated with medial frontal theta-band power modulations, irrespective of conflict awareness. However, and crucially, across-trial conflict adaptation processes reflected in increased theta-band power over dorsolateral frontal cortex were observed after fully conscious conflict only. This suggests that initial conflict detection and subsequent control adaptation by the medial frontal cortex are automatic and unconscious, whereas the routing of information from the medial frontal cortex to the lateral prefrontal cortex is a unique feature of conscious cognitive control.

[1]  R. Badgaiyan,et al.  Executive control, willed actions, and nonconscious processing , 2000, Human brain mapping.

[2]  M. Frank,et al.  Frontal theta as a mechanism for cognitive control , 2014, Trends in Cognitive Sciences.

[3]  V. Lamme,et al.  Unconscious High-Level Information Processing , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[4]  K. D'ostilio,et al.  Dissociation between unconscious motor response facilitation and conflict in medial frontal areas , 2012, The European journal of neuroscience.

[5]  Johannes J. Fahrenfort,et al.  Pre-SMA Gray-matter Density Predicts Individual Differences in Action Selection in the Face of Conscious and Unconscious Response Conflict , 2011, Journal of Cognitive Neuroscience.

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

[7]  Keiji Tanaka,et al.  Conflict-induced behavioural adjustment: a clue to the executive functions of the prefrontal cortex , 2009, Nature Reviews Neuroscience.

[8]  Simon Hanslmayr,et al.  Neural Communication Patterns Underlying Conflict Detection, Resolution, and Adaptation , 2014, The Journal of Neuroscience.

[9]  E. Awh,et al.  Conflict adaptation effects in the absence of executive control , 2003, Nature Neuroscience.

[10]  K. R. Ridderinkhof,et al.  Medial frontal cortex and response conflict: Evidence from human intracranial EEG and medial frontal cortex lesion , 2008, Brain Research.

[11]  D. Norman,et al.  Attention to Action: Willed and Automatic Control of Behavior Technical Report No. 8006. , 1980 .

[12]  K. R. Ridderinkhof,et al.  Unconscious Errors Enhance Prefrontal-Occipital Oscillatory Synchrony , 2009, Front. Hum. Neurosci..

[13]  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.

[14]  J. Changeux,et al.  Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006 Conscious, preconscious, and subliminal processing: a testable taxonomy , 2022 .

[15]  B. Gold,et al.  Conflict adaptation in prefrontal cortex: Now you see it, now you don't , 2014, Cortex.

[16]  R. Compton,et al.  Is "conflict adaptation" driven by conflict? Behavioral and EEG evidence for the underappreciated role of congruent trials. , 2012, Psychophysiology.

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

[18]  Andrew D. Engell,et al.  The Neural Bases of Cognitive Conflict and Control in Moral Judgment , 2004, Neuron.

[19]  K. R. Ridderinkhof,et al.  Not All Errors Are Alike: Theta and Alpha EEG Dynamics Relate to Differences in Error-Processing Dynamics , 2012, The Journal of Neuroscience.

[20]  John G. Kerns,et al.  Anterior cingulate and prefrontal cortex activity in an FMRI study of trial-to-trial adjustments on the Simon task , 2006, NeuroImage.

[21]  Gili Freedman,et al.  Cognitive control in the intertrial interval: evidence from EEG alpha power. , 2011, Psychophysiology.

[22]  B. Hommel Consciousness and Control Not Identical Twins , 2007 .

[23]  Wilfried Kunde,et al.  No conflict control in the absence of awareness , 2011, Psychological research.

[24]  M. Posner,et al.  Executive attention: Conflict, target detection, and cognitive control. , 1998 .

[25]  Ardi Roelofs,et al.  Anterior cingulate cortex activity can be independent of response conflict in Stroop-like tasks , 2006, Proceedings of the National Academy of Sciences.

[26]  Bernhard Pastötter,et al.  Dynamic Adjustments of Cognitive Control: Oscillatory Correlates of the Conflict Adaptation Effect , 2013, Journal of Cognitive Neuroscience.

[27]  K. R. Ridderinkhof,et al.  Unconsciously Triggered Conflict Adaptation , 2010, PloS one.

[28]  Michael X. Cohen,et al.  Dynamic Interactions between Large-Scale Brain Networks Predict Behavioral Adaptation after Perceptual Errors , 2012, Cerebral cortex.

[29]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[30]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[31]  A. Mognon,et al.  ADJUST: An automatic EEG artifact detector based on the joint use of spatial and temporal features. , 2011, Psychophysiology.

[32]  Michael X. Cohen,et al.  Theta Dynamics Reveal Domain-specific Control over Stimulus and Response Conflict , 2012, Journal of Cognitive Neuroscience.

[33]  James R. Schmidt Questioning conflict adaptation: proportion congruent and Gratton effects reconsidered , 2013, Psychonomic bulletin & review.

[34]  D. Tucker,et al.  Frontal midline theta and the error-related negativity: neurophysiological mechanisms of action regulation , 2004, Clinical Neurophysiology.

[35]  Stanislas Dehaene,et al.  Toward a computational theory of conscious processing , 2014, Current Opinion in Neurobiology.

[36]  Kobe Desender,et al.  Is Consciousness Necessary for Conflict Adaptation? A State of the Art , 2012, Front. Hum. Neurosci..

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

[38]  T. Egner Congruency sequence effects and cognitive control , 2007, Cognitive, affective & behavioral neuroscience.

[39]  T. Wickens Elementary Signal Detection Theory , 2001 .

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

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

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

[43]  B. Peterson,et al.  Adaptation to Conflict via Context-Driven Anticipatory Signals in the Dorsomedial Prefrontal Cortex , 2011, The Journal of Neuroscience.

[44]  Antao Chen,et al.  Electrophysiological correlates of block-wise strategic adaptations to consciously and unconsciously triggered conflict , 2013, Neuropsychologia.

[45]  Keiji Tanaka,et al.  Mnemonic Function of the Dorsolateral Prefrontal Cortex in Conflict-Induced Behavioral Adjustment , 2007, Science.

[46]  W. Notebaert,et al.  The heterogeneous world of congruency sequence effects: an update , 2014, Front. Psychol..

[47]  T. Braver The variable nature of cognitive control: a dual mechanisms framework , 2012, Trends in Cognitive Sciences.

[48]  Lars Bäckman,et al.  A multivariate analysis of age-related differences in functional networks supporting conflict resolution , 2014, NeuroImage.

[49]  Michael X. Cohen,et al.  Subthreshold muscle twitches dissociate oscillatory neural signatures of conflicts from errors , 2014, NeuroImage.

[50]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[51]  Lauren M. Bylsma,et al.  The conflict adaptation effect: It’s not just priming , 2005, Cognitive, affective & behavioral neuroscience.

[52]  Tiago V. Maia,et al.  Conscious and unconscious processes in cognitive control: a theoretical perspective and a novel empirical approach , 2012, Front. Hum. Neurosci..

[53]  Jeounghoon Kim,et al.  Task-dependent response conflict monitoring and cognitive control in anterior cingulate and dorsolateral prefrontal cortices , 2013, Brain Research.

[54]  M. Eimer,et al.  Response facilitation and inhibition in subliminal priming , 2003, Biological Psychology.

[55]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[56]  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.

[57]  E. Donchin,et al.  Optimizing the use of information: strategic control of activation of responses. , 1992, Journal of experimental psychology. General.

[58]  E. Van den Bussche,et al.  Comparing Conscious and Unconscious Conflict Adaptation , 2013, PloS one.

[59]  R. Nigbur,et al.  Theta power as a marker for cognitive interference , 2011, Clinical Neurophysiology.

[60]  Antao Chen,et al.  The neural oscillations of conflict adaptation in the human frontal region , 2013, Biological Psychology.

[61]  B. Hommel,et al.  A feature-integration account of sequential effects in the Simon task , 2004, Psychological research.

[62]  Michael X. Cohen,et al.  Switch-Related and General Preparation Processes in Task-Switching: Evidence from Multivariate Pattern Classification of EEG Data , 2012, Journal of Neuroscience.

[63]  Tim Shallice,et al.  Introspective physicalism as an approach to the science of consciousness , 2001, Cognition.

[64]  John J. B. Allen,et al.  Theta EEG dynamics of the error-related negativity , 2007, Clinical Neurophysiology.

[65]  Simon van Gaal,et al.  Unconscious Activation of the Prefrontal No-Go Network , 2010, The Journal of Neuroscience.

[66]  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.

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