Errors can be related to pre-stimulus differences in ERP topography and their concomitant sources

Much of the variation in both neuronal and behavioral responses to stimuli can be explained by pre-stimulus fluctuations in brain activity. We hypothesized that also errors are the result of stochastic fluctuations in pre-stimulus activity and investigated the temporal dynamics of the scalp topography and their concomitant intracranial generators of stimulus- and response-locked high-density event-related potentials (ERPs) to errors and correct trials in a Stroop task. We found significant differences in ERP map topography and intracranial sources before the onset of the stimulus and after the initiation of the response but not as a function of stimulus-induced conflict. Before the stimulus, topographic differences were accompanied by differential activity in lateral frontal, parietal and temporal areas known to be involved in voluntary reorientation of attention and cognitive control. Differential post-response activity propagated both medially and laterally on a rostral-caudal axis of a network typically involved in performance monitoring. Analysis of the statistical properties of error occurrences revealed their stochasticity.

[1]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[2]  Christoph M. Michel,et al.  Segregated Processing of Auditory Motion and Auditory Location: An ERP Mapping Study , 2002, NeuroImage.

[3]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[4]  Christoph M. Michel,et al.  Duration and not strength of activation in temporo-parietal cortex positively correlates with schizotypy , 2007, NeuroImage.

[5]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[6]  Robert Tibshirani,et al.  Cluster Validation by Prediction Strength , 2005 .

[7]  Christoph M. Michel,et al.  Combination of EEG–fMRI and EEG source analysis improves interpretation of spike-associated activation networks in paediatric pharmacoresistant focal epilepsies , 2009, NeuroImage.

[8]  Theodor Landis,et al.  Brain state-dependent functional hemispheric specialization in men but not in women. , 2005, Cerebral cortex.

[9]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

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

[11]  Á. Pascual-Leone,et al.  α-Band Electroencephalographic Activity over Occipital Cortex Indexes Visuospatial Attention Bias and Predicts Visual Target Detection , 2006, The Journal of Neuroscience.

[12]  Alon Friedman,et al.  Propagation of interictal discharges in temporal lobe epilepsy: Correlation of spatiotemporal mapping with intracranial foramen ovale electrode recordings , 2006, Clinical Neurophysiology.

[13]  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.

[14]  W. Klimesch,et al.  Visual discrimination performance is related to decreased alpha amplitude but increased phase locking , 2005, Neuroscience Letters.

[15]  C M Michel,et al.  Spatiotemporal EEG analysis and distributed source estimation in presurgical epilepsy evaluation. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[16]  C. Carter,et al.  The Timing of Action-Monitoring Processes in the Anterior Cingulate Cortex , 2002, Journal of Cognitive Neuroscience.

[17]  Á. Pascual-Leone,et al.  Spontaneous fluctuations in posterior alpha-band EEG activity reflect variability in excitability of human visual areas. , 2008, Cerebral cortex.

[18]  Denis Brunet,et al.  Topographic ERP Analyses: A Step-by-Step Tutorial Review , 2008, Brain Topography.

[19]  C. Carter,et al.  The anterior cingulate as a conflict monitor: fMRI and ERP studies , 2002, Physiology & Behavior.

[20]  W. Krzanowski,et al.  A Criterion for Determining the Number of Groups in a Data Set Using Sum-of-Squares Clustering , 1988 .

[21]  Christoph M. Michel,et al.  The spatio-temporal mapping of epileptic networks: Combination of EEG–fMRI and EEG source imaging , 2009, NeuroImage.

[22]  C M Michel,et al.  Event-related potential maps depend on prestimulus brain electric microstate map. , 1994, The International journal of neuroscience.

[23]  Gregor Thut,et al.  Prediction of response speed by anticipatory high‐frequency (gamma band) oscillations in the human brain , 2005, Human brain mapping.

[24]  Thomas R. Knösche,et al.  Who Comes First? The Role of the Prefrontal and Parietal Cortex in Cognitive Control , 2005, Journal of Cognitive Neuroscience.

[25]  Alexander Maye,et al.  Temporal dynamics of access to consciousness in the attentional blink , 2007, NeuroImage.

[26]  Clara D. Martin,et al.  Controlling for interstimulus perceptual variance abolishes N170 face selectivity , 2007, Nature Neuroscience.

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

[28]  C M Michel,et al.  Event-related potential map differences depend on the prestimulus microstates. , 1995, Journal of medical engineering & technology.

[29]  C. Michel,et al.  Electromagnetic Inverse Solutions in Anatomically Constrained Spherical Head Models , 2004, Brain Topography.

[30]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[31]  Christoph M. Michel,et al.  Spatiotemporal Dynamics of Human Cognition. , 1999, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[32]  M. Brass,et al.  The role of the inferior frontal junction area in cognitive control , 2005, Trends in Cognitive Sciences.

[33]  R. VanRullen,et al.  The phase of ongoing EEG oscillations predicts visual perception , 2010 .

[34]  D. Lehmann,et al.  Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[35]  C. Michel,et al.  EEG Source Imaging in Pediatric Epilepsy Surgery: A New Perspective in Presurgical Workup , 2006, Epilepsia.

[36]  Theodor Landis,et al.  Right parietal brain activity precedes perceptual alternation of bistable stimuli. , 2009, Cerebral cortex.

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

[38]  G. Thut,et al.  Mechanisms of selective inhibition in visual spatial attention are indexed by α‐band EEG synchronization , 2007, The European journal of neuroscience.

[39]  C. M. Michel,et al.  Prestimulus EEG microstates influence visual event-related potential microstates in field maps with 47 channels , 2005, Journal of Neural Transmission.

[40]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[41]  M. Fuchs,et al.  Linear and nonlinear current density reconstructions. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[42]  S. Morand,et al.  Electric source imaging of human brain functions , 2001, Brain Research Reviews.

[43]  A. Grinvald,et al.  Dynamics of Ongoing Activity: Explanation of the Large Variability in Evoked Cortical Responses , 1996, Science.

[44]  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.

[45]  C. Gray,et al.  Cellular Mechanisms Contributing to Response Variability of Cortical Neurons In Vivo , 1999, The Journal of Neuroscience.

[46]  Christoph M. Michel,et al.  A bias for posterior α-band power suppression versus enhancement during shifting versus maintenance of spatial attention , 2009, NeuroImage.

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

[48]  M. Herrmann,et al.  Source localization (LORETA) of the error-related-negativity (ERN/Ne) and positivity (Pe). , 2004, Brain research. Cognitive brain research.

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

[50]  Colin M. Macleod.  Half a century of research on the Stroop effect: an integrative review. , 1991, Psychological bulletin.

[51]  Tonia A. Rihs,et al.  Resting EEG alpha-power over posterior sites indexes baseline visual cortex excitability , 2008 .

[52]  G Lantz,et al.  Simultaneous intracranial and extracranial recording of interictal epileptiform activity in patients with drug resistant partial epilepsy: patterns of conduction and results from dipole reconstructions. , 1996, Electroencephalography and clinical neurophysiology.

[53]  S. Thorpe,et al.  Seeking Categories in the Brain , 2001, Science.

[54]  M Corbetta,et al.  Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Daniel Brandeis,et al.  Impaired semantic processing during sentence reading in children with dyslexia: Combined fMRI and ERP evidence , 2008, NeuroImage.

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

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

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

[59]  Simon Hanslmayr,et al.  Prestimulus oscillations predict visual perception performance between and within subjects , 2007, NeuroImage.