Error-preceding brain activity reflects (mal-)adaptive adjustments of cognitive control: a modeling study

Errors in choice tasks are preceded by gradual changes in brain activity presumably related to fluctuations in cognitive control that promote the occurrence of errors. In the present paper, we use connectionist modeling to explore the hypothesis that these fluctuations reflect (mal-)adaptive adjustments of cognitive control. We considered ERP data from a study in which the probability of conflict in an Eriksen-flanker task was manipulated in sub-blocks of trials. Errors in these data were preceded by a gradual decline of N2 amplitude. After fitting a connectionist model of conflict adaptation to the data, we analyzed simulated N2 amplitude, simulated response times (RTs), and stimulus history preceding errors in the model, and found that the model produced the same pattern as obtained in the empirical data. Moreover, this pattern is not found in alternative models in which cognitive control varies randomly or in an oscillating manner. Our simulations suggest that the decline of N2 amplitude preceding errors reflects an increasing adaptation of cognitive control to specific task demands, which leads to an error when these task demands change. Taken together, these results provide evidence that error-preceding brain activity can reflect adaptive adjustments rather than unsystematic fluctuations of cognitive control, and therefore, that these errors are actually a consequence of the adaptiveness of human cognition.

[1]  Bryan Rodgers,et al.  What does a Man do after he Makes an Error? An Analysis of Response Programming , 1977 .

[2]  Robert T. Knight,et al.  Lapses in a Prefrontal-Extrastriate Preparatory Attention Network Predict Mistakes , 2006, Journal of Cognitive Neuroscience.

[3]  Jan R. Wessel,et al.  Modulation of the error-related negativity by response conflict. , 2009, Psychophysiology.

[4]  Rafal Bogacz,et al.  Parameterization of connectionist models , 2004, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[5]  W. Notebaert,et al.  Dissociating conflict adaptation from feature integration: a multiple regression approach. , 2007, Journal of experimental psychology. Human perception and performance.

[6]  Tom Eichele,et al.  Posterior Medial Frontal Cortex Activity Predicts Post-Error Adaptations in Task-Related Visual and Motor Areas , 2011, The Journal of Neuroscience.

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

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

[9]  K. R. Ridderinkhof,et al.  Error-preceding brain activity: Robustness, temporal dynamics, and boundary conditions , 2005, Biological Psychology.

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

[11]  Jonathan R. Folstein,et al.  Influence of cognitive control and mismatch on the N2 component of the ERP: a review. , 2007, Psychophysiology.

[12]  Marco Steinhauser,et al.  Performance monitoring and the causal attribution of errors , 2011, Cognitive, affective & behavioral neuroscience.

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

[14]  C. Eriksen,et al.  Effects of noise letters upon the identification of a target letter in a nonsearch task , 1974 .

[15]  Marco Steinhauser,et al.  Error-related brain activity and adjustments of selective attention following errors , 2011, NeuroImage.

[16]  K. R. Ridderinkhof,et al.  Electrophysiological correlates of anterior cingulate function in a go/no-go task: Effects of response conflict and trial type frequency , 2003, Cognitive, affective & behavioral neuroscience.

[17]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[18]  Jonathan D. Cohen,et al.  The Impact of Cognitive Deficits on Conflict Monitoring , 2006, Psychological science.

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

[20]  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.

[21]  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.

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

[23]  Christo Pantev,et al.  Multimodal imaging of functional networks and event-related potentials in performance monitoring , 2011, NeuroImage.

[24]  Tom Eichele,et al.  Semi-automatic identification of independent components representing EEG artifact , 2009, Clinical Neurophysiology.

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

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

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

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

[29]  Rajita Sinha,et al.  Greater activation of the “default” brain regions predicts stop signal errors , 2007, NeuroImage.

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

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

[32]  Wim Fias,et al.  Post-error slowing: An orienting account , 2009, Cognition.

[33]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[34]  Jonathan D. Cohen,et al.  Parametric Manipulation of the Conflict Signal and Control-state Adaptation , 2011, Journal of Cognitive Neuroscience.

[35]  Kenneth Hugdahl,et al.  Prediction of human errors by maladaptive changes in event-related brain networks , 2008, Proceedings of the National Academy of Sciences.

[36]  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.

[37]  Hilde T. Juvodden,et al.  Mal-Adaptation of Event-Related EEG Responses Preceding Performance Errors , 2010, Front. Hum. Neurosci..

[38]  D. Laming.  Choice reaction performance following an error , 1979 .

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

[40]  Brian Mingus,et al.  The Emergent neural modeling system , 2008, Neural Networks.