Spatiotemporal characterization of response inhibition

Despite an extensive literature on the neural substrates of response inhibition, when and where this process occurs in the brain remain unclear. The present study aimed to shed light on this issue by exploiting the high temporal resolution of the event-related potentials (ERPs) and recent advances in source localization. Temporo-spatial principal component analysis was employed to define more precisely the two ERP components most often associated with response inhibition (i.e., frontocentral N2 and frontocentral P3), as well as to improve the accuracy of source localization. In addition, participants (N=40) performed a modified Go/Nogo task composed of three types of stimuli (frequent-Go, infrequent-Go, and infrequent-Nogo), which allowed us to dissociate neural activity associated with response inhibition from that related to novelty processing by directly contrasting nogo and go trials matched with respect to frequency of occurrence. Scalp ERP data indicated that the frontocentral P3, but not the frontocentral N2, showed larger amplitudes for infrequent-Nogo than for infrequent-Go trials. Source localization data parallel the results obtained at the scalp level: only P3-related activity showed differences between infrequent-Nogo and infrequent-Go trials. This increased activation was observed predominantly in the presupplementary motor area (preSMA). Present results suggest that the frontocentral P3 and the preSMA play a core role in response inhibition. The findings of this study substantiate and complement previous results obtained by hemodynamic procedures.

[1]  R. Chapman,et al.  EP Component Identification and Measurement by Principal Components-Analysis , 1995, Brain and Cognition.

[2]  Rolando J. Biscay-Lirio,et al.  Assessing interactions in the brain with exact low-resolution electromagnetic tomography , 2011, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[3]  R. Barry,et al.  Movement-related potentials in the Go/NoGo task: The P3 reflects both cognitive and motor inhibition , 2008, Clinical Neurophysiology.

[4]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[5]  Andreas Mueller,et al.  Dissociating action inhibition, conflict monitoring and sensory mismatch into independent components of event related potentials in GO/NOGO task , 2011, NeuroImage.

[6]  Bettina Sorger,et al.  Novelty and target processing during an auditory novelty oddball: A simultaneous event-related potential and functional magnetic resonance imaging study , 2008, NeuroImage.

[7]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[8]  R. Constable,et al.  Imaging Response Inhibition in a Stop-Signal Task: Neural Correlates Independent of Signal Monitoring and Post-Response Processing , 2006, The Journal of Neuroscience.

[9]  K Richard Ridderinkhof,et al.  ERP components associated with successful and unsuccessful stopping in a stop-signal task. , 2004, Psychophysiology.

[10]  Robert J. Barry,et al.  The auditory-evoked N2 and P3 components in the stop-signal task: Indices of inhibition, response-conflict or error-detection? , 2006, Brain and Cognition.

[11]  Jaime S. Ide,et al.  A cerebellar thalamic cortical circuit for error-related cognitive control , 2011, NeuroImage.

[12]  Rajita Sinha,et al.  Subcortical processes of motor response inhibition during a stop signal task , 2008, NeuroImage.

[13]  Blake W. Johnson,et al.  “Shut up!” An electrophysiological study investigating the neural correlates of vocal inhibition , 2012, Neuropsychologia.

[14]  Todd C. Handy,et al.  Event-related potentials : a methods handbook , 2005 .

[15]  Shane M. O’Mara,et al.  Individual differences discriminate event-related potentials but not performance during response inhibition , 2004, Experimental Brain Research.

[16]  C. C. Duncan,et al.  Event-related potentials in clinical research: Guidelines for eliciting, recording, and quantifying mismatch negativity, P300, and N400 , 2009, Clinical Neurophysiology.

[17]  Cong Huang,et al.  Neural Correlates of Post-error Slowing during a Stop Signal Task: A Functional Magnetic Resonance Imaging Study , 2008, Journal of Cognitive Neuroscience.

[18]  R. Poldrack,et al.  Common neural substrates for inhibition of spoken and manual responses. , 2008, Cerebral cortex.

[19]  E. Donchin,et al.  Spatiotemporal analysis of the late ERP responses to deviant stimuli. , 2001, Psychophysiology.

[20]  Sara López-Martín,et al.  Emotional context modulates response inhibition: Neural and behavioral data , 2010, NeuroImage.

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

[22]  H. Bokura,et al.  Electrophysiological correlates for response inhibition in a Go/NoGo task , 2001, Clinical Neurophysiology.

[23]  Christina F. Lavallee,et al.  Electroencephalography of response inhibition tasks: functional networks and cognitive contributions. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[24]  F. Karayanidis,et al.  ERPs and behavioral inhibition in a Go/No-go task in children with attention-deficit hyperactivity disorder. , 2000, Brain and cognition.

[25]  E. Donchin,et al.  Localization of the event-related potential novelty response as defined by principal components analysis. , 2003, Brain research. Cognitive brain research.

[26]  Cyril Poupon,et al.  Microstructure of a three-way anatomical network predicts individual differences in response inhibition: A tractography study , 2012, NeuroImage.

[27]  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.

[28]  C. Kennard,et al.  Functional role of the supplementary and pre-supplementary motor areas , 2008, Nature Reviews Neuroscience.

[29]  Donald T. Stuss,et al.  Inhibitory Control is Slowed in Patients with Right Superior Medial Frontal Damage , 2006, Journal of Cognitive Neuroscience.

[30]  Koji Jimura,et al.  Activation of Right Inferior Frontal Gyrus during Response Inhibition across Response Modalities , 2007, Journal of Cognitive Neuroscience.

[31]  J. Pekar,et al.  fMRI evidence that the neural basis of response inhibition is task-dependent. , 2003, Brain research. Cognitive brain research.

[32]  Vinod Menon,et al.  Event-related FMRI evidence of frontotemporal involvement in aberrant response inhibition and task switching in attention-deficit/hyperactivity disorder. , 2004, Journal of the American Academy of Child and Adolescent Psychiatry.

[33]  Godfrey Pearlson,et al.  An adaptive reflexive processing model of neurocognitive function: supporting evidence from a large scale (n = 100) fMRI study of an auditory oddball task , 2005, NeuroImage.

[34]  K. J. Bruin,et al.  Response priming in a go/nogo task: do we have to explain the go/nogo N2 effect in terms of response activation instead of inhibition? , 2001, Clinical Neurophysiology.

[35]  Shenmin Zhang,et al.  Resting-state functional connectivity of the medial superior frontal cortex. , 2012, Cerebral cortex.

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

[37]  R. Poldrack,et al.  Cortical and Subcortical Contributions to Stop Signal Response Inhibition: Role of the Subthalamic Nucleus , 2006, The Journal of Neuroscience.

[38]  R. Cattell.  The Scree Test For The Number Of Factors. , 1966, Multivariate behavioral research.

[39]  Robert Schmitt,et al.  Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection , 2004, NeuroImage.

[40]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

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

[42]  Y. Miyashita,et al.  Preparation to Inhibit a Response Complements Response Inhibition during Performance of a Stop-Signal Task , 2009, The Journal of Neuroscience.

[43]  H. Walter,et al.  Response inhibition in borderline personality disorder: event-related potentials in a Go/Nogo task , 2007, Journal of Neural Transmission.

[44]  K. Kiehl,et al.  An event-related fMRI study of visual and auditory oddball tasks , 2001 .

[45]  C. Li,et al.  Behavioral/systems/cognitive Functional Connectivity Delineates Distinct Roles of the Inferior Frontal Cortex and Presupplementary Motor Area in Stop Signal Inhibition , 2022 .

[46]  Phillip J Holcomb,et al.  Surprise? Early visual novelty processing is not modulated by attention. , 2011, Psychophysiology.

[47]  T. Shallice,et al.  Effects of focal frontal lesions on response inhibition. , 2006, Cerebral cortex.

[48]  M. Falkenstein,et al.  Response inhibition in Huntington's disease—A study using ERPs and sLORETA , 2008, Neuropsychologia.

[49]  Roberto D. Pascual-Marqui,et al.  Discrete, 3D distributed, linear imaging methods of electric neuronal activity. Part 1: exact, zero error localization , 2007, 0710.3341.

[50]  E. Bullmore,et al.  Mapping Motor Inhibition: Conjunctive Brain Activations across Different Versions of Go/No-Go and Stop Tasks , 2001, NeuroImage.

[51]  R. Elliott,et al.  Response inhibition and impulsivity: an fMRI study , 2003, Neuropsychologia.

[52]  Thomas Dierks,et al.  Spatial pattern of cerebral glucose metabolism (PET) correlates with localization of intracerebral EEG-generators in Alzheimer's disease , 2000, Clinical Neurophysiology.

[53]  Christo Pantev,et al.  Conflict and inhibition differentially affect the N200/P300 complex in a combined go/nogo and stop-signal task , 2010, NeuroImage.

[54]  Neil G. Muggleton,et al.  Control of prepotent responses by the superior medial frontal cortex , 2009, NeuroImage.

[55]  Joseph Dien,et al.  Evaluating two-step PCA of ERP data with Geomin, Infomax, Oblimin, Promax, and Varimax rotations. , 2010, Psychophysiology.

[56]  C. Li,et al.  Activation of the pre-supplementary motor area but not inferior prefrontal cortex in association with short stop signal reaction time – an intra-subject analysis , 2009, BMC Neuroscience.

[57]  G. Logan,et al.  Impulsivity and Inhibitory Control , 1997 .

[58]  Diane Swick,et al.  Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks , 2011, NeuroImage.

[59]  R. Simons,et al.  On the relationship of P3a and the Novelty-P3 , 2001, Biological Psychology.

[60]  M M Mesulam,et al.  An electrophysiological index of stimulus unfamiliarity. , 2000, Psychophysiology.

[61]  R. T. Constable,et al.  Error-specific medial cortical and subcortical activity during the stop signal task: A functional magnetic resonance imaging study , 2008, Neuroscience.

[62]  Hiroki M. Morimoto,et al.  Functional dissociation in right inferior frontal cortex during performance of go/no-go task. , 2009, Cerebral cortex.

[63]  Robert J. Barry,et al.  Response priming in the Go/NoGo task: The N2 reflects neither inhibition nor conflict , 2007, Clinical Neurophysiology.

[64]  D. Pizzagalli,et al.  Functional but not structural subgenual prefrontal cortex abnormalities in melancholia , 2004 .

[65]  Young Youn Kim,et al.  Electrophysiological correlates of behavioral response inhibition in patients with obsessive–compulsive disorder , 2007, Depression and anxiety.

[66]  J. Pekar,et al.  Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent , 2008, Neuropsychologia.

[67]  K. Kiehl,et al.  Event‐related fMRI study of response inhibition , 2001, Human brain mapping.

[68]  E. Donchin,et al.  On quantifying surprise: the variation of event-related potentials with subjective probability. , 1977, Psychophysiology.

[69]  A. A. Wijers,et al.  Inhibition, response mode, and stimulus probability: a comparative event-related potential study , 2002, Clinical Neurophysiology.

[70]  Sara López-Martín,et al.  Voltage-Based Versus Factor Score-Based Source Localization Analyses of Electrophysiological Brain Activity: A Comparison , 2004, Brain Topography.

[71]  M Spitzer,et al.  The time course of brain activations during response inhibition: evidence from event‐related potentials in a go/no go task , 1998, Neuroreport.

[72]  T. Sejnowski,et al.  Removing electroencephalographic artifacts by blind source separation. , 2000, Psychophysiology.

[73]  Joseph Dien,et al.  Evaluation of PCA and ICA of simulated ERPs: Promax vs. infomax rotations , 2007, Human brain mapping.

[74]  H. Garavan,et al.  Dissociable Executive Functions in the Dynamic Control of Behavior: Inhibition, Error Detection, and Correction , 2002, NeuroImage.

[75]  J. Hohnsbein,et al.  ERP components in Go/Nogo tasks and their relation to inhibition. , 1999, Acta psychologica.

[76]  Avram J. Holmes,et al.  Dissociable recruitment of rostral anterior cingulate and inferior frontal cortex in emotional response inhibition , 2008, NeuroImage.

[77]  B. Kopp,et al.  N2, P3 and the lateralized readiness potential in a nogo task involving selective response priming. , 1996, Electroencephalography and clinical neurophysiology.

[78]  Laura Hokkanen,et al.  Neural correlates of late positivities associated with infrequent visual events and response errors , 2010, NeuroImage.

[79]  Maneesh C. Patel,et al.  Distinct frontal systems for response inhibition, attentional capture, and error processing , 2010, Proceedings of the National Academy of Sciences.

[80]  Stuart J. Johnstone,et al.  Neural mechanisms underlying trait impulsivity in non-clinical adults: Stop-signal performance and event-related potentials , 2007, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[81]  C. Gonsalvez,et al.  Response inhibition deficits in obsessive–compulsive disorder , 2002, Psychiatry Research.

[82]  J. Cohen,et al.  On the number of trials needed for P300. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[83]  G. Logan,et al.  Response inhibition in the stop-signal paradigm , 2008, Trends in Cognitive Sciences.

[84]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[85]  Juri D. Kropotov,et al.  Decomposing N2 NOGO wave of event-related potentials into independent components , 2009, Neuroreport.

[86]  Mike Wendt,et al.  Disentangling Sequential Effects of Stimulus- and Response-related Conflict and Stimulus-Response Repetition using Brain Potentials , 2007, Journal of Cognitive Neuroscience.

[87]  D. Friedman,et al.  The novelty P3: an event-related brain potential (ERP) sign of the brain's evaluation of novelty , 2001, Neuroscience & Biobehavioral Reviews.

[88]  Geert J. M. van Boxtel,et al.  The N2 in go/no-go tasks reflects conflict monitoring not response inhibition , 2004, Brain and Cognition.

[89]  E. Jodo,et al.  Relation of a negative ERP component to response inhibition in a Go/No-go task. , 1992, Electroencephalography and clinical neurophysiology.