Event-Related Potentials Elicited by Errors during the Stop-Signal Task. I. Macaque Monkeys

The error-related negativity (ERN) and positivity (Pe) are components of event-related potential (ERP) waveforms recorded from humans and are thought to reflect performance monitoring. Error-related signals have also been found in single-neuron responses and local-field potentials recorded in supplementary eye field and anterior cingulate cortex of macaque monkeys. However, the homology of these neural signals across species remains controversial. Here, we show that monkeys exhibit ERN and Pe components when they commit errors during a saccadic stop-signal task. The voltage distributions and current densities of these components were similar to those found in humans performing the same task. Subsequent analyses show that neither stimulus- nor response-related artifacts accounted for the error-ERPs. This demonstration of macaque homologues of the ERN and Pe forms a keystone in the bridge linking human and nonhuman primate studies on the neural basis of performance monitoring.

[1]  E. Procyk,et al.  Behavioral Shifts and Action Valuation in the Anterior Cingulate Cortex , 2008, Neuron.

[2]  Clay B. Holroyd,et al.  Error-related scalp potentials elicited by hand and foot movements: evidence for an output-independent error-processing system in humans , 1998, Neuroscience Letters.

[3]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

[4]  Joshua W. Brown,et al.  Learned Predictions of Error Likelihood in the Anterior Cingulate Cortex , 2005, Science.

[5]  E Halgren,et al.  Rapid distributed fronto-parieto-occipital processing stages during working memory in humans. , 2002, Cerebral cortex.

[6]  H. Helmholtz Ueber einige Gesetze der Vertheilung elektrischer Ströme in körperlichen Leitern mit Anwendung auf die thierisch‐elektrischen Versuche , 1853 .

[7]  Jörn Kastner,et al.  SWARM: sLORETA-weighted accurate minimum norm inverse solutions , 2007 .

[8]  K. Johnston,et al.  Top-Down Control-Signal Dynamics in Anterior Cingulate and Prefrontal Cortex Neurons following Task Switching , 2007, Neuron.

[9]  Michael W. Cole,et al.  Cingulate cortex: Diverging data from humans and monkeys , 2009, Trends in Neurosciences.

[10]  T. Endrass,et al.  Error Awareness in a Saccade Countermanding Task , 2005 .

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

[12]  Thomas F Münte,et al.  Time Course of Error Detection and Correction in Humans: Neurophysiological Evidence , 2002, The Journal of Neuroscience.

[13]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[14]  R. West,et al.  Tracking the temporal dynamics of updating cognitive control: an examination of error processing. , 2008, Cerebral cortex.

[15]  Wim Fias,et al.  Outcome expectancy and not accuracy determines posterror slowing: ERP support , 2010, Cognitive, affective & behavioral neuroscience.

[16]  J. Schall,et al.  Role of frontal eye fields in countermanding saccades: visual, movement, and fixation activity. , 1998, Journal of neurophysiology.

[17]  Ole Jensen,et al.  Oxford handbook of event-related potential components. , 2011 .

[18]  Ann-Christine Ehlis,et al.  Allelic Variation of Serotonin Transporter Function Modulates the Brain Electrical Response for Error Processing , 2004, Neuropsychopharmacology.

[19]  R. Wurtz,et al.  Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. , 1993, Journal of neurophysiology.

[20]  O. Hikosaka,et al.  Perceptual Learning, Motor Learning and Automaticity Switching from Automatic to Controlled Behavior: Cortico-basal Ganglia Mechanisms , 2022 .

[21]  K. Kiehl,et al.  Error processing and the rostral anterior cingulate: an event-related fMRI study. , 2000, Psychophysiology.

[22]  Markus Ullsperger,et al.  Neuropharmacology of performance monitoring , 2009, Neuroscience & Biobehavioral Reviews.

[23]  P. Redgrave,et al.  Is the short-latency dopamine response too short to signal reward error? , 1999, Trends in Neurosciences.

[24]  D. Tucker,et al.  Electrophysiological Responses to Errors and Feedback in the Process of Action Regulation , 2003, Psychological science.

[25]  Clay B. Holroyd,et al.  Why is there an ERN/Ne on correct trials? Response representations, stimulus-related components, and the theory of error-processing , 2001, Biological Psychology.

[26]  Veit Stuphorn,et al.  Role of supplementary eye field in saccade initiation: executive, not direct, control. , 2010, Journal of neurophysiology.

[27]  Michael W. Cole,et al.  Conflict over Cingulate Cortex: Between-Species Differences in Cingulate May Support Enhanced Cognitive Flexibility in Humans , 2010, Brain, Behavior and Evolution.

[28]  W. Hulstijn,et al.  Drug-induced stimulation and suppression of action monitoring in healthy volunteers , 2004, Psychopharmacology.

[29]  David C. Godlove Eye Movement Artifact May Account for Putative Frontal Feedback-Related Potentials in Nonhuman Primates , 2010, The Journal of Neuroscience.

[30]  D. P. Hanes,et al.  Controlled Movement Processing: Superior Colliculus Activity Associated with Countermanded Saccades , 2003, The Journal of Neuroscience.

[31]  C. Bruce,et al.  Primate frontal eye fields. I. Single neurons discharging before saccades. , 1985, Journal of neurophysiology.

[32]  W. Gehring,et al.  Functions of the Medial Frontal Cortex in the Processing of Conflict and Errors , 2001, The Journal of Neuroscience.

[33]  Aditya Murthy,et al.  Frontal eye field contributions to rapid corrective saccades. , 2007, Journal of neurophysiology.

[34]  T. Paus Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[35]  Joshua W. Brown,et al.  Performance monitoring local field potentials in the medial frontal cortex of primates: supplementary eye field. , 2010, Journal of neurophysiology.

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

[37]  Clay B. Holroyd,et al.  A mechanism for error detection in speeded response time tasks. , 2005, Journal of experimental psychology. General.

[38]  Josep Marco-Pallarés,et al.  The Impact of Catechol-O-Methyltransferase and Dopamine D4 Receptor Genotypes on Neurophysiological Markers of Performance Monitoring , 2007, The Journal of Neuroscience.

[39]  P. Redgrave,et al.  The basal ganglia: a vertebrate solution to the selection problem? , 1999, Neuroscience.

[40]  Clay B. Holroyd,et al.  The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. , 2002, Psychological review.

[41]  G. Woodman,et al.  Measurement of the extraocular spike potential during saccade countermanding. , 2011, Journal of neurophysiology.

[42]  Joshua W. Brown,et al.  Performance Monitoring by the Anterior Cingulate Cortex During Saccade Countermanding , 2003, Science.

[43]  M. W. van der Molen,et al.  Differential involvement of the aterior cingulated cortex in performance monitoring during a stop-signal task , 2005 .

[44]  Jeffrey D Schall,et al.  Nonhuman primate event-related potentials indexing covert shifts of attention , 2007, Proceedings of the National Academy of Sciences.

[45]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[46]  O. Hikosaka,et al.  Visual and Anticipatory Bias in Three Cortical Eye Fields of the Monkey during an Adaptive Decision-Making Task , 2002, The Journal of Neuroscience.

[47]  Patrick G. Bissett,et al.  Balancing Cognitive Demands: Control Adjustments in the Stop-signal Paradigm Stop-signal Paradigm Post-stop-signal Slowing , 2011 .

[48]  A. Dale,et al.  Improved Localizadon of Cortical Activity by Combining EEG and MEG with MRI Cortical Surface Reconstruction: A Linear Approach , 1993, Journal of Cognitive Neuroscience.

[49]  Gilles Pourtois,et al.  Unavoidable errors: A spatio-temporal analysis of time-course and neural sources of evoked potentials associated with error processing in a speeded task , 2008, Neuropsychologia.

[50]  William J. Gehring,et al.  The Error-Related Negativity (ERN/Ne) , 2011 .

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

[52]  J. Schall,et al.  Countermanding saccades in macaque , 1995, Visual Neuroscience.

[53]  Leanne Boucher,et al.  Nonindependent and nonstationary response times in stopping and stepping saccade tasks , 2010, Attention, perception & psychophysics.

[54]  J. Schall,et al.  Performance monitoring by the supplementary eye ® eld , 2000 .

[55]  J. Hohnsbein,et al.  ERP components on reaction errors and their functional significance: a tutorial , 2000, Biological Psychology.

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

[57]  Leanne Boucher,et al.  Influence of history on saccade countermanding performance in humans and macaque monkeys , 2007, Vision Research.

[58]  R. Simons,et al.  To err is autonomic: error-related brain potentials, ANS activity, and post-error compensatory behavior. , 2003, Psychophysiology.

[59]  P. Jurák,et al.  Error processing – evidence from intracerebral ERP recordings , 2002, Experimental Brain Research.

[60]  Marty G. Woldorff,et al.  Abnormal Brain Activity Related to Performance Monitoring and Error Detection in Children with ADHD , 2005, Cortex.

[61]  Ziad M. Hafed,et al.  A Neural Mechanism for Microsaccade Generation in the Primate Superior Colliculus , 2009, Science.

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

[63]  J. Tanji,et al.  Role for cingulate motor area cells in voluntary movement selection based on reward. , 1998, Science.

[64]  Jeffrey D Schall,et al.  Performance monitoring local field potentials in the medial frontal cortex of primates: supplementary eye field. , 2010, Journal of neurophysiology.

[65]  G. Logan On the ability to inhibit thought and action , 1984 .

[66]  J. Schall,et al.  Executive control of countermanding saccades by the supplementary eye field , 2006, Nature Neuroscience.

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

[68]  R. Passingham,et al.  Medial frontal cortex: from self-generated action to reflection on one's own performance , 2010, Trends in Cognitive Sciences.

[69]  R D Pascual-Marqui,et al.  Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. , 2002, Methods and findings in experimental and clinical pharmacology.

[70]  Cameron S Carter,et al.  Development of action monitoring through adolescence into adulthood: ERP and source localization. , 2007, Developmental science.

[71]  E. Procyk,et al.  Anterior cingulate error‐related activity is modulated by predicted reward , 2005, The European journal of neuroscience.

[72]  A. Rodríguez-Fornells,et al.  A neurophysiological study of the detrimental effects of alprazolam on human action monitoring. , 2005, Brain research. Cognitive brain research.

[73]  A. Cooper,et al.  Predictive Reward Signal of Dopamine Neurons , 2011 .

[74]  Aditya Murthy,et al.  Neural control of visual search by frontal eye field: effects of unexpected target displacement on visual selection and saccade preparation. , 2009, Journal of neurophysiology.

[75]  Norbert Kathmann,et al.  Neural correlates of error awareness , 2007, NeuroImage.

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

[77]  Leanne Boucher,et al.  Executive control of gaze by the frontal lobes , 2007, Cognitive, affective & behavioral neuroscience.

[78]  Jutta Stahl,et al.  Dynamics of response-conflict monitoring and individual differences in response control and behavioral control: An electrophysiological investigation using a stop-signal task , 2007, Clinical Neurophysiology.

[79]  Jeffrey D. Schall,et al.  Conflict in Cingulate Cortex Function between Humans and Macaque Monkeys: More Apparent than Real , 2010, Brain, Behavior and Evolution.

[80]  E. Donchin,et al.  P300 and tracking difficulty: evidence for multiple resources in dual-task performance. , 1980, Psychophysiology.

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

[82]  K. R. Ridderinkhof,et al.  Error-related brain potentials are differentially related to awareness of response errors: evidence from an antisaccade task. , 2001, Psychophysiology.

[83]  J. Fermaglich Electric Fields of the Brain: The Neurophysics of EEG , 1982 .

[84]  Antoni Rodríguez-Fornells,et al.  Noradrenergic Stimulation Enhances Human Action Monitoring , 2005, The Journal of Neuroscience.

[85]  Andreas K. Engel,et al.  Monitoring error processing by means of simultaneous EEG/fMRI recordings II: single-trial independent component analysis of the error-related negativity (ERN) , 2005 .