A statistical comparison of EEG time- and time–frequency domain representations of error processing

Successful behavior relies on error detection and subsequent remedial adjustment of behavior. Researchers have identified two electrophysiological signatures of error processing: the time-domain error-related negativity (ERN), and the time-frequency domain increased power in the delta/theta frequency bands (~2-8 Hz). The relationship between these two signatures is not entirely clear: on the one hand they occur after the same type of event and with similar latency, but on the other hand, the time-domain ERP component contains only phase-locked activity whereas the time-frequency response additionally contains non-phase-locked dynamics. Here we examined the ERN and error-related delta/theta activity in relation to each other, focusing on within-subject analyses that utilize single-trial data. Using logistic regression, we constructed three statistical models in which the accuracy of each trial was predicted from the ERN, delta/theta power, or both. We found that both the ERN and delta/theta power worked roughly equally well as predictors of single-trial accuracy (~70% accurate prediction). Furthermore, a model including both measures provided a stronger overall prediction compared to either model alone. Based on these findings two conclusions are drawn: first, the phase-locked part of the EEG signal appears to be roughly as predictive of single-trial response accuracy as the non-phase-locked part; second, the single-trial ERP and delta/theta power contain both overlapping and independent information.

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

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

[3]  M. Ding,et al.  Relation between P300 and event-related theta-band synchronization: A single-trial analysis , 2011, Clinical Neurophysiology.

[4]  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.

[5]  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.

[6]  Aribert Rothenberger,et al.  Increased event-related theta activity as a psychophysiological marker of comorbidity in children with tics and attention-deficit/hyperactivity disorders , 2006, NeuroImage.

[7]  E. Sokhadze,et al.  Single trial time–frequency domain analysis of error processing in post-traumatic stress disorder , 2012, Neuroscience Letters.

[8]  I. Jentzsch,et al.  Weaker error signals do not reduce the effectiveness of post-error adjustments: Comparing error processing in young and middle-aged adults , 2012, Brain Research.

[9]  T. Demiralp,et al.  What if you are not sure? Electroencephalographic correlates of subjective confidence level about a decision , 2012, Clinical Neurophysiology.

[10]  Rafal Bogacz,et al.  Theta phase resetting and the error-related negativity. , 2007, Psychophysiology.

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

[12]  Clay B. Holroyd,et al.  Detection of synchronized oscillations in the electroencephalogram: an evaluation of methods. , 2004, Psychophysiology.

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

[14]  John J. B. Allen,et al.  Theta lingua franca: a common mid-frontal substrate for action monitoring processes. , 2012, Psychophysiology.

[15]  Guillaume A. Rousselet,et al.  Reliability of ERP and single-trial analyses , 2011, NeuroImage.

[16]  Michael X. Cohen,et al.  Midfrontal conflict-related theta-band power reflects neural oscillations that predict behavior. , 2013, Journal of neurophysiology.

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

[18]  S. Luck An Introduction to the Event-Related Potential Technique , 2005 .

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

[20]  W. Gehring,et al.  Neural Systems for Error Monitoring , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

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

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

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

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

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

[26]  Cameron S Carter,et al.  Generalized signaling for control: evidence from postconflict and posterror performance adjustments. , 2009, Journal of experimental psychology. Human perception and performance.

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

[28]  J. Hohnsbein,et al.  Effects of crossmodal divided attention on late ERP components. II. Error processing in choice reaction tasks. , 1991, Electroencephalography and clinical neurophysiology.

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

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

[31]  U. Ansorge,et al.  Exploring trial-by-trial modulations of the Simon effect , 2005, The Quarterly journal of experimental psychology. A, Human experimental psychology.