Slow and Fast Responses: Two Mechanisms of Trial Outcome Processing Revealed by EEG Oscillations

Cognitive control includes maintenance of task-specific processes related to attention, and non-specific regulation of motor threshold. Depending upon the nature of the behavioral tasks, these mechanisms may predispose to different kinds of errors, with either increased or decreased response time (RT) of erroneous responses relative to correct responses. Specifically, slow responses are related to attentional lapses and decision uncertainty, these conditions tending to delay RTs of both erroneous and correct responses. Here we studied if RT may be a valid approximation distinguishing trials with high and low levels of sustained attention and decision uncertainty. We analyzed response-related and feedback-related modulations in theta, alpha and beta band activity in the auditory version of the two-choice condensation task, which is highly demanding for sustained attention while involves no inhibition of prepotent responses. Depending upon response speed and accuracy, trials were divided into slow correct, slow erroneous, fast correct and fast erroneous. We found that error-related frontal midline theta (FMT) was present only on fast erroneous trials. The feedback-related FMT was equally strong on slow erroneous and fast erroneous trials. Late post-response posterior alpha suppression was stronger on erroneous slow trials. Feedback-related frontal beta was present only on slow correct trials. The data obtained cumulatively suggests that RT allows distinguishing the two types of trials, with fast trials related to higher levels of attention and low uncertainty, and slow trials related to lower levels of attention and higher uncertainty.

[1]  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.

[2]  B. Chernyshev,et al.  Condensation Task as an Experimental Model for Studying Individual Differences in Cognitive Control , 2015 .

[3]  Tzyy-Ping Jung,et al.  Arousing feedback rectifies lapse in performance and corresponding EEG power spectrum , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[4]  Nikita A. Novikov,et al.  Theta and Alpha Band Modulations Reflect Error-Related Adjustments in the Auditory Condensation Task , 2015, Front. Hum. Neurosci..

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

[6]  M. Posner INFORMATION REDUCTION IN THE ANALYSIS OF SEQUENTIAL TASKS. , 1964, Psychological review.

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

[8]  David Cucurell,et al.  Human oscillatory activity associated to reward processing in a gambling task , 2008, Neuropsychologia.

[9]  G Pfurtscheller,et al.  Event-related desynchronization (ERD) during visual processing. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[10]  Febo Cincotti,et al.  Functional frontoparietal connectivity during short-term memory as revealed by high-resolution EEG coherence analysis. , 2004, Behavioral neuroscience.

[11]  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.

[12]  Chernyshev Boris Vladimirovich,et al.  Spontaneous attentional performance lapses during the auditory condensation task: an ERP study , 2015 .

[13]  Philip T Quinlan,et al.  Feature and conjunction processing in the auditory modality , 2003, Perception & psychophysics.

[14]  Michael X. Cohen,et al.  Oscillatory Activity and Phase–Amplitude Coupling in the Human Medial Frontal Cortex during Decision Making , 2009, Journal of Cognitive Neuroscience.

[15]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

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

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

[18]  James F. Cavanagh,et al.  Frontal theta links prediction errors to behavioral adaptation in reinforcement learning , 2010, NeuroImage.

[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]  Michael X. Cohen,et al.  Error-related medial frontal theta activity predicts cingulate-related structural connectivity , 2011, NeuroImage.

[21]  R. Knight,et al.  Error-Monitoring and Post-Error Compensations: Dissociation between Perceptual Failures and Motor Errors with and without Awareness , 2013, The Journal of Neuroscience.

[22]  Juliana Yordanova,et al.  Error-Related Oscillations , 2009 .

[23]  Michael X. Cohen,et al.  A neural microcircuit for cognitive conflict detection and signaling , 2014, Trends in Neurosciences.

[24]  Ernest Mas-Herrero,et al.  Beta oscillations and reward processing: Coupling oscillatory activity and hemodynamic responses , 2015, NeuroImage.

[25]  A. Engel,et al.  Cortical Network Dynamics of Perceptual Decision-Making in the Human Brain , 2011, Frontiers in Human Neuroscience.

[26]  C. Brunia,et al.  Event-related desynchronization related to the anticipation of a stimulus providing knowledge of results , 1999, Clinical Neurophysiology.

[27]  Roger Ratcliff,et al.  The Diffusion Decision Model: Theory and Data for Two-Choice Decision Tasks , 2008, Neural Computation.

[28]  R. Nusslock,et al.  Willing to wait: Elevated reward-processing EEG activity associated with a greater preference for larger-but-delayed rewards , 2016, Neuropsychologia.

[29]  Matthew S. Tata,et al.  Right frontal cortex generates reward-related theta-band oscillatory activity , 2009, NeuroImage.

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

[31]  Joydeep Bhattacharya,et al.  Processing Graded Feedback: Electrophysiological Correlates of Learning from Small and Large Errors , 2014, Journal of Cognitive Neuroscience.

[32]  W. R. Garner,et al.  Filtering and condensation tasks with integral and separable dimensions , 1975 .

[33]  K. R. Ridderinkhof,et al.  EEG Source Reconstruction Reveals Frontal-Parietal Dynamics of Spatial Conflict Processing , 2013, PloS one.

[34]  John J. Foxe,et al.  Uncovering the Neural Signature of Lapsing Attention: Electrophysiological Signals Predict Errors up to 20 s before They Occur , 2009, The Journal of Neuroscience.

[35]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[36]  Sidney J. Segalowitz,et al.  The effects of uncertainty in error monitoring on associated ERPs , 2004, Brain and Cognition.

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

[38]  Franziska M. Korb,et al.  Post-Error Behavioral Adjustments Are Facilitated by Activation and Suppression of Task-Relevant and Task-Irrelevant Information Processing , 2010, The Journal of Neuroscience.

[39]  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.

[40]  Thomas F Münte,et al.  Coupling electrophysiological and hemodynamic responses to errors , 2012, Human brain mapping.

[41]  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.

[42]  T. Womelsdorf,et al.  Human Neuroscience , 2022 .

[43]  D. Tucker,et al.  Regulating action: alternating activation of midline frontal and motor cortical networks , 2001, Clinical Neurophysiology.

[44]  Ricardo Chavarriaga,et al.  Discriminant brain connectivity patterns of performance monitoring at average and single-trial levels , 2015, NeuroImage.

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

[46]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[47]  Carolin Dudschig,et al.  Speeding before and slowing after errors: Is it all just strategy? , 2009, Brain Research.

[48]  Michael X. Cohen,et al.  Frontal Oscillatory Dynamics Predict Feedback Learning and Action Adjustment , 2011, Journal of Cognitive Neuroscience.

[49]  Koen B E Böcker,et al.  ERD as an index of anticipatory attention? Effects of stimulus degradation. , 2002, Psychophysiology.

[50]  O. Jensen,et al.  Prestimulus alpha and mu activity predicts failure to inhibit motor responses , 2009, Human brain mapping.

[51]  W. R. Garner The Processing of Information and Structure , 1974 .

[52]  M. Ullsperger,et al.  Post-Error Adjustments , 2011, Front. Psychology.

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

[54]  Markus Ullsperger,et al.  Error Awareness Revisited: Accumulation of Multimodal Evidence from Central and Autonomic Nervous Systems , 2011, Journal of Cognitive Neuroscience.

[55]  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.

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

[57]  David Papo,et al.  Modulation of late alpha band oscillations by feedback in a hypothesis testing paradigm. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[58]  C. Tenke,et al.  Principal components analysis of Laplacian waveforms as a generic method for identifying ERP generator patterns: II. Adequacy of low-density estimates , 2006, Clinical Neurophysiology.

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

[60]  J. Wilding The relation between latency and accuracy in the identification of visual stimuli. I. The effects of task difficulty. , 1971, Acta psychologica.

[61]  Antoni Rodríguez-Fornells,et al.  Brain oscillatory activity associated with task switching and feedback processing , 2011, Cognitive, Affective, & Behavioral Neuroscience.

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

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

[64]  Juliana Yordanova,et al.  Parallel systems of error processing in the brain , 2004, NeuroImage.

[65]  R. Duncan Luce,et al.  Response Times: Their Role in Inferring Elementary Mental Organization , 1986 .

[66]  J. Schoffelen,et al.  University of Birmingham Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex , 2014 .

[67]  Richard Ridderinkhof Micro- and macro-adjustments of task set: activation and suppression in conflict tasks , 2002, Psychological research.

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

[69]  R. Compton,et al.  Alpha power is influenced by performance errors. , 2009, Psychophysiology.

[70]  A. Rodríguez-Fornells,et al.  Neuroscience and Biobehavioral Reviews the Role of High-frequency Oscillatory Activity in Reward Processing and Learning , 2022 .