Cognitive control in the eye of the beholder: Electrocortical theta and alpha modulation during response preparation in a cued saccade task

Abstract The oscillatory dynamics of medial frontal EEG theta and posterior alpha are implicated in the modulation of attention and cognitive control. We used a novel saccade cueing paradigm to examine whether theta and alpha are modulated by task difficulty during response preparation. After isolating and functionally classifying medial frontal and posterior alpha independent components, the EEG spectral power in these components was calculated on pro‐ and anti‐saccade trials prior to response probes. The results of bootstrap re‐sampling show that, compared to pro‐saccade trials, correct anti‐saccades are characterized by an increase in medial frontal theta and suppression of posterior alpha during the response preparation period. Furthermore, an absence of increased medial frontal theta prior to anti‐saccades probes occurs on error trials, that is, a failure to control pre‐potent eye movements. For these error trials, a burst in medial frontal theta is instead observed following error feedback. Our findings show that enhanced medial frontal theta is linked not only to dynamic cognitive control that is reactive (such as, after error commission), but is also an important prerequisite for success when behavioral control is challenged. HighlightsSaccade cueing paradigm to examine oscillatory dynamics of response preparation.Theta enhanced during response preparation on anti‐saccade correct trials.Alpha reduced during response preparation on anti‐saccade correct trials.Theta also increases following anti‐saccade errors.Medial frontal theta is important prerequisite for response control.

[1]  John J. Foxe,et al.  Uncovering the Neural Signature of Lapsing Attention: Electrophysiological Signals Predict Errors up to 20 s before They Occur , 2009, The Journal of Neuroscience.

[2]  W. Klimesch.  EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[3]  Anna Christina Nobre,et al.  Anticipating Conflict Facilitates Controlled Stimulus-response Selection , 2009, Journal of Cognitive Neuroscience.

[4]  J. Mazer.  Spatial Attention, Feature-Based Attention, and Saccades: Three Sides of One Coin? , 2011, Biological Psychiatry.

[5]  Jorge Bosch,et al.  Do specific EEG frequencies indicate different processes during mental calculation? , 1999, Neuroscience Letters.

[6]  K. R. Ridderinkhof,et al.  Not All Errors Are Alike: Theta and Alpha EEG Dynamics Relate to Differences in Error-Processing Dynamics , 2012, The Journal of Neuroscience.

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

[8]  Christian Beste,et al.  Crosslinking EEG time–frequency decomposition and fMRI in error monitoring , 2013, Brain Structure and Function.

[9]  Guillaume A. Rousselet,et al.  Quantifying the Time Course of Visual Object Processing Using ERPs: It's Time to Up the Game , 2011, Front. Psychology.

[10]  Y. Isomura,et al.  Direct recording of theta oscillations in primate prefrontal and anterior cingulate cortices. , 2006, Journal of neurophysiology.

[11]  Andrew C. N. Chen,et al.  EEG default mode network in the human brain: Spectral regional field powers , 2008 .

[12]  E D Adrian,et al.  The interpretation of potential waves in the cortex , 1934, The Journal of physiology.

[13]  Rand R. Wilcox,et al.  How many discoveries have been lost by ignoring modern statistical methods , 1998 .

[14]  Jia Wu,et al.  Social exclusion modulates event-related frontal theta and tracks ostracism distress in children , 2015, NeuroImage.

[15]  Markus Ullsperger,et al.  Continuous theta-burst stimulation (cTBS) over the lateral prefrontal cortex alters reinforcement learning bias , 2011, NeuroImage.

[16]  Clay B. Holroyd,et al.  Frontal midline theta and N200 amplitude reflect complementary information about expectancy and outcome evaluation. , 2013, Psychophysiology.

[17]  Theodore H. Poister,et al.  Performance monitoring , 1996 .

[18]  C. Buss,et al.  Children's Brain Development Benefits from Longer Gestation , 2011, Front. Psychology.

[19]  S. Micheloyannis,et al.  What does delta band tell us about cognitive processes: A mental calculation study , 2010, Neuroscience Letters.

[20]  O. Jensen,et al.  University of Birmingham Attention Modulates TMS-Locked Alpha Oscillations in the Visual Cortex , 2015 .

[21]  Anthony T. Herdman,et al.  Spatio-temporal Brain Dynamics Underlying Saccade Execution, Suppression, and Error-related Feedback , 2007, Journal of Cognitive Neuroscience.

[22]  James A Desjardins,et al.  Deconstructing the early visual electrocortical responses to face and house stimuli. , 2013, Journal of vision.

[23]  David Goodman,et al.  Performance Monitoring in the Anterior Cingulate is Not All Error Related: Expectancy Deviation and the Representation of Action-Outcome Associations , 2007, Journal of Cognitive Neuroscience.

[24]  E. Ziegel.  Introduction to Robust Estimation and Hypothesis Testing (2nd ed.) , 2005 .

[25]  Haifeng Li,et al.  Brain oscillations mechanism for cognitive control process , 2015 .

[26]  J. Lisman,et al.  Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. , 2002, Cerebral cortex.

[27]  Y. Isomura,et al.  Theta oscillations in primate prefrontal and anterior cingulate cortices in forewarned reaction time tasks. , 2010, Journal of neurophysiology.

[28]  Yanling Yin,et al.  EEG default mode network in the human brain: Spectral regional field powers , 2008, NeuroImage.

[29]  Kathy A. Low,et al.  Different slopes for different folks: alpha and delta EEG power predict subsequent video game learning rate and improvements in cognitive control tasks. , 2012, Psychophysiology.

[30]  G. V. Simpson,et al.  Parieto‐occipital ∼1 0Hz activity reflects anticipatory state of visual attention mechanisms , 1998 .

[31]  Felix A Wichmann,et al.  When luminance increment thresholds depend on apparent lightness. , 2012, Journal of vision.

[32]  John J. Foxe,et al.  The Role of Alpha-Band Brain Oscillations as a Sensory Suppression Mechanism during Selective Attention , 2011, Front. Psychology.

[33]  Carles Escera,et al.  EEG delta oscillations index inhibitory control of contextual novelty to both irrelevant distracters and relevant task-switch cues. , 2014, Psychophysiology.

[34]  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.

[35]  H. Keselman,et al.  Modern robust data analysis methods: measures of central tendency. , 2003, Psychological methods.

[36]  Markus Ullsperger,et al.  Surprise and Error: Common Neuronal Architecture for the Processing of Errors and Novelty , 2012, The Journal of Neuroscience.

[37]  J. Schoffelen,et al.  Prestimulus Oscillatory Activity in the Alpha Band Predicts Visual Discrimination Ability , 2008, The Journal of Neuroscience.

[38]  Ryan K. Jessup,et al.  Error Effects in Anterior Cingulate Cortex Reverse when Error Likelihood Is High , 2010, The Journal of Neuroscience.

[39]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[40]  T. Fernández,et al.  EEG delta activity: an indicator of attention to internal processing during performance of mental tasks. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[41]  Mark D'Esposito,et al.  Alpha-Band Phase Synchrony Is Related to Activity in the Fronto-Parietal Adaptive Control Network , 2012, The Journal of Neuroscience.

[42]  T. Harmony.  The functional significance of delta oscillations in cognitive processing , 2013, Front. Integr. Neurosci..

[43]  N. Yeung,et al.  The roles of cortical oscillations in sustained attention , 2015, Trends in Cognitive Sciences.

[44]  Kara A. Dyckman,et al.  Pre-Cue Fronto-Occipital Alpha Phase and Distributed Cortical Oscillations Predict Failures of Cognitive Control , 2012, The Journal of Neuroscience.

[45]  Yoshikazu Isomura,et al.  Neural Coding of “Attention for Action” and “Response Selection” in Primate Anterior Cingulate Cortex , 2003, The Journal of Neuroscience.

[46]  L. M. Ward,et al.  Long-distance alpha-band MEG synchronization maintains selective visual attention , 2007 .

[47]  A. Fiore,et al.  Different roles of alpha- and beta-branch xanthophylls in photosystem assembly and photoprotection. , 2007, The Journal of biological chemistry.

[48]  S. Makeig,et al.  Mining event-related brain dynamics , 2004, Trends in Cognitive Sciences.

[49]  Michael X. Cohen,et al.  Single-Trial Regression Elucidates the Role of Prefrontal Theta Oscillations in Response Conflict , 2011, Front. Psychology.

[50]  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.

[51]  Markus Ullsperger,et al.  Selection of independent components representing event-related brain potentials: A data-driven approach for greater objectivity , 2011, NeuroImage.

[52]  James F. Cavanagh,et al.  Frontal theta links prediction errors to behavioral adaptation in reinforcement learning , 2010, NeuroImage.

[53]  M. Frank,et al.  Frontal theta as a mechanism for cognitive control , 2014, Trends in Cognitive Sciences.

[54]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[55]  Tzyy-Ping Jung,et al.  Imaging brain dynamics using independent component analysis , 2001, Proc. IEEE.

[56]  R. Folmer.  rTMS for Tinnitus , 2012, Front. Hum. Neurosci..

[57]  K. R. Ridderinkhof,et al.  Medial frontal cortex and response conflict: Evidence from human intracranial EEG and medial frontal cortex lesion , 2008, Brain Research.

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

[59]  Clayton E. Curtis,et al.  Maintenance of Spatial and Motor Codes during Oculomotor Delayed Response Tasks , 2004, The Journal of Neuroscience.

[60]  石井 良平.  Medial prefrontal cortex generates frontal midline theta rhythm , 1999 .

[61]  Jesse S. Husk,et al.  Time course and robustness of ERP object and face differences. , 2008, Journal of vision.

[62]  M. Corbetta,et al.  Frontoparietal Cortex Controls Spatial Attention through Modulation of Anticipatory Alpha Rhythms , 2009, The Journal of Neuroscience.

[63]  Hermann Wagner,et al.  Disparity sensitivity in man and owl: Psychophysical evidence for equivalent perception of shape-from-stereo. , 2011, Journal of vision.

[64]  John J. Foxe,et al.  Oscillatory alpha-band suppression mechanisms during the rapid attentional shifts required to perform an anti-saccade task , 2013, NeuroImage.

[65]  Jordan P. Hamm,et al.  Alpha oscillations and the control of voluntary saccadic behavior , 2012, Experimental Brain Research.

[66]  W Pieter Medendorp,et al.  Parietofrontal circuits in goal‐oriented behaviour , 2011, The European journal of neuroscience.

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

[68]  Julia Kastner,et al.  Introduction to Robust Estimation and Hypothesis Testing , 2005 .

[69]  J. Cavanagh,et al.  Frontal midline theta reflects anxiety and cognitive control: Meta-analytic evidence , 2015, Journal of Physiology-Paris.

[70]  Laura Moretti,et al.  Theta signal as the neural signature of social exclusion. , 2013, Cerebral cortex.

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

[72]  A. Anastasi.  Individual differences. , 2020, Annual review of psychology.

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

[74]  G. Knyazev,et al.  The default mode network and EEG alpha oscillations: An independent component analysis , 2011, Brain Research.

[75]  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.

[76]  W. Guo,et al.  Design of dual mode radix4 SRT divider , 2015 .

[77]  Stefan Everling,et al.  Theta-activity in anterior cingulate cortex predicts task rules and their adjustments following errors , 2010, Proceedings of the National Academy of Sciences.

[78]  Sidney J. Segalowitz,et al.  Performance monitoring and the medial prefrontal cortex: a review of individual differences and context effects as a window on self-regulation , 2012, Front. Hum. Neurosci..

[79]  John J. Foxe,et al.  Increases in alpha oscillatory power reflect an active retinotopic mechanism for distracter suppression during sustained visuospatial attention. , 2006, Journal of neurophysiology.

[80]  Bita Moghaddam,et al.  Preparatory attention relies on dynamic interactions between prelimbic cortex and anterior cingulate cortex. , 2013, Cerebral cortex.

[81]  Borís Burle,et al.  Rostral Cingulate Zone and correct response monitoring: ICA and source localization evidences for the unicity of correct- and error-negativities , 2010, NeuroImage.

[82]  Michael Falkenstein,et al.  Independent component analysis of erroneous and correct responses suggests online response control , 2010, Human brain mapping.

[83]  R. Oostenveld,et al.  Frontal theta EEG activity correlates negatively with the default mode network in resting state. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[84]  Jeroen J. A. van Boxtel,et al.  Retinotopic and non-retinotopic stimulus encoding in binocular rivalry and the involvement of feedback. , 2008, Journal of vision.

[85]  Ole Jensen,et al.  Different roles of alpha and beta band oscillations in anticipatory sensorimotor gating , 2014, Front. Hum. Neurosci..

[86]  James F. Cavanagh,et al.  Common medial frontal mechanisms of adaptive control in humans and rodents , 2013, Nature Neuroscience.

[87]  Joshua W. Brown,et al.  Medial prefrontal cortex predicts and evaluates the timing of action outcomes , 2011, NeuroImage.

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

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

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

[91]  John J. Foxe,et al.  Attention-dependent suppression of distracter visual input can be cross-modally cued as indexed by anticipatory parieto-occipital alpha-band oscillations. , 2001, Brain research. Cognitive brain research.

[92]  Gregor Thut,et al.  Resting electroencephalogram alpha-power over posterior sites indexes baseline visual cortex excitability , 2008, Neuroreport.

[93]  Denis Schluppeck,et al.  Differential roles for frontal eye fields (FEFs) and intraparietal sulcus (IPS) in visual working memory and visual attention. , 2010, Journal of vision.

[94]  Jed A. Meltzer,et al.  Individual differences in EEG theta and alpha dynamics during working memory correlate with fMRI responses across subjects , 2007, Clinical Neurophysiology.

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

[96]  Brandon G. King,et al.  A computational approach to understanding the longitudinal changes in cortical activity associated with intensive meditation training , 2010, BMC Neuroscience.

[97]  Thomas Dierks,et al.  BOLD correlates of EEG alpha phase-locking and the fMRI default mode network , 2009, NeuroImage.

[98]  Byoung-Kyong Min,et al.  Task-related modulation of anterior theta and posterior alpha EEG reflects top-down preparation , 2010, BMC Neuroscience.

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

[100]  Sidney J. Segalowitz,et al.  Watch out! Medial frontal cortex is activated by cues signaling potential changes in response demands , 2015, NeuroImage.