University of Dundee Trial-by-trial covariation of pre-stimulus EEG alpha power and visuospatial bias reflects a mixture of stochastic and deterministic effects

Human perception of perithreshold stimuli critically depends on oscillatory EEG activity prior to stimulus onset. However, it remains unclear exactly which aspects of perception are shaped by this pre-stimulus activity and what role stochastic (trial-bytrial) variability plays in driving these relationships. We employed a novel jackknife approach to link single-trial variability in oscillatory activity to psychometric measures from a task that requires judgement of the relative length of two line segments (the landmark task). The results provide evidence that pre-stimulus alpha fluctuations influence perceptual bias. Importantly, a mediation analysis showed that this relationship is partially driven by long-term (deterministic) alpha changes over time, highlighting the need to account for sources of trial-by-trial variability when interpreting EEG predictors of perception. These results provide fundamental insight into the nature of the effects of ongoing oscillatory activity on perception. The jackknife approach we implemented may serve to identify and investigate neural signatures of perceptual relevance in more detail.

[1]  M. H. Quenouille Approximate Tests of Correlation in Time‐Series , 1949 .

[2]  K. Heilman,et al.  Pseudoneglect: Effects of hemispace on a tactile line bisection task , 1980, Neuropsychologia.

[3]  W. Parr Jackknifing Differentiable Statistical Functionals , 1985 .

[4]  D. A. Kenny,et al.  The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. , 1986, Journal of personality and social psychology.

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

[6]  A. Milner,et al.  To halve and to halve not: An analysis of line bisection judgements in normal subjects , 1992, Neuropsychologia.

[7]  A. Milner,et al.  An Investigation of Hemispatial Neglect Using the Landmark Task , 1995, Brain and Cognition.

[8]  A. Wirz-Justice,et al.  Power density in theta/alpha frequencies of the waking EEG progressively increases during sustained wakefulness. , 1995, Sleep.

[9]  T. Jung,et al.  Changes in alertness are a principal component of variance in the EEG spectrum , 1995, Neuroreport.

[10]  M. McCourt,et al.  Cognitive and perceptual influences on visual line bisection: Psychophysical and chronometric analyses of pseudoneglect , 1997, Neuropsychologia.

[11]  K. Zilles,et al.  Line bisection judgments implicate right parietal cortex and cerebellum as assessed by fMRI , 2000, Neurology.

[12]  M. McCourt,et al.  Pseudoneglect: a review and meta-analysis of performance factors in line bisection tasks , 2000, Neuropsychologia.

[13]  G. V. Simpson,et al.  Anticipatory Biasing of Visuospatial Attention Indexed by Retinotopically Specific α-Bank Electroencephalography Increases over Occipital Cortex , 2000, The Journal of Neuroscience.

[14]  Y. Benjamini,et al.  THE CONTROL OF THE FALSE DISCOVERY RATE IN MULTIPLE TESTING UNDER DEPENDENCY , 2001 .

[15]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[16]  K. Willmes,et al.  On the Functional Neuroanatomy of Intrinsic and Phasic Alertness , 2001, NeuroImage.

[17]  I. THE ATTENTION SYSTEM OF THE HUMAN BRAIN , 2002 .

[18]  Daniel C. Javitt,et al.  Right hemisphere control of visuospatial attention: line-bisection judgments evaluated with high-density electrical mapping and source analysis☆ , 2003, NeuroImage.

[19]  D. A. Kenny,et al.  Lower Level Mediation in Multilevel Models , 2022 .

[20]  Andreas Kleinschmidt,et al.  EEG-correlated fMRI of human alpha activity , 2003, NeuroImage.

[21]  A. Milner,et al.  A Revised Method for Analysing Neglect using the Landmark Task , 2004, Cortex.

[22]  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.

[23]  T. Ergenoğlu,et al.  Alpha rhythm of the EEG modulates visual detection performance in humans. , 2004, Brain research. Cognitive brain research.

[24]  H. Gibbons,et al.  The application of jackknife-based onset detection of lateralized readiness potential in correlative approaches. , 2004, Psychophysiology.

[25]  K. Linkenkaer-Hansen,et al.  Prestimulus Oscillations Enhance Psychophysical Performance in Humans , 2004, The Journal of Neuroscience.

[26]  Manuel Schabus,et al.  A shift of visual spatial attention is selectively associated with human EEG alpha activity , 2005, The European journal of neuroscience.

[27]  C. Dodds,et al.  Rightward shift in spatial awareness with declining alertness , 2005, Neuropsychologia.

[28]  Denis Cousineau,et al.  Confidence intervals in within-subject designs: A simpler solution to Loftus and Masson's method , 2005 .

[29]  V. Candas,et al.  Time-on-task effect in pseudoneglect , 2006, Experimental Brain Research.

[30]  K. Willmes,et al.  The effect of low arousal on visuo-spatial attention , 2006, Neuropsychologia.

[31]  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.

[32]  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.

[33]  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.

[34]  J. Palva,et al.  New vistas for alpha-frequency band oscillations. , 2007, Trends in neurosciences.

[35]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

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

[37]  J. Palva,et al.  Very Slow EEG Fluctuations Predict the Dynamics of Stimulus Detection and Oscillation Amplitudes in Humans , 2008, The Journal of Neuroscience.

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

[39]  John J. Foxe,et al.  The strength of anticipatory spatial biasing predicts target discrimination at attended locations: a high‐density EEG study , 2009, The European journal of neuroscience.

[40]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[41]  C. Tallon-Baudry,et al.  How Ongoing Fluctuations in Human Visual Cortex Predict Perceptual Awareness: Baseline Shift versus Decision Bias , 2009, The Journal of Neuroscience.

[42]  Diane M. Beck,et al.  To See or Not to See: Prestimulus α Phase Predicts Visual Awareness , 2009, The Journal of Neuroscience.

[43]  R. VanRullen,et al.  The Phase of Ongoing EEG Oscillations Predicts Visual Perception , 2009, The Journal of Neuroscience.

[44]  Paul Sajda,et al.  Quality of evidence for perceptual decision making is indexed by trial-to-trial variability of the EEG , 2009, Proceedings of the National Academy of Sciences.

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

[46]  Brent L. Hughes,et al.  Neural mechanisms of emotion regulation: Evidence for two independent prefrontal-subcortical pathways , 2009 .

[47]  Yan Zhang,et al.  Detection of a Weak Somatosensory Stimulus: Role of the Prestimulus Mu Rhythm and Its Top–Down Modulation , 2010, Journal of Cognitive Neuroscience.

[48]  A. Kleinschmidt,et al.  Intrinsic Connectivity Networks, Alpha Oscillations, and Tonic Alertness: A Simultaneous Electroencephalography/Functional Magnetic Resonance Imaging Study , 2010, The Journal of Neuroscience.

[49]  J. Gross,et al.  On the Role of Prestimulus Alpha Rhythms over Occipito-Parietal Areas in Visual Input Regulation: Correlation or Causation? , 2010, The Journal of Neuroscience.

[50]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[51]  R. VanRullen,et al.  Spontaneous EEG oscillations reveal periodic sampling of visual attention , 2010, Proceedings of the National Academy of Sciences.

[52]  Ingo Fründ,et al.  Inference for psychometric functions in the presence of nonstationary behavior. , 2011, Journal of vision.

[53]  R. VanRullen,et al.  Ongoing EEG Phase as a Trial-by-Trial Predictor of Perceptual and Attentional Variability , 2011, Front. Psychology.

[54]  Diane M. Beck,et al.  Pulsed Out of Awareness: EEG Alpha Oscillations Represent a Pulsed-Inhibition of Ongoing Cortical Processing , 2011, Front. Psychology.

[55]  A. Nobre,et al.  Indexing the graded allocation of visuospatial attention using anticipatory alpha oscillations , 2011, Journal of neurophysiology.

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

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

[58]  M. Corbetta,et al.  Spatial neglect and attention networks. , 2011, Annual review of neuroscience.

[59]  Mingzhou Ding,et al.  From Prestimulus Alpha Oscillation to Visual-evoked Response: An Inverted-U Function and Its Attentional Modulation , 2011, Journal of Cognitive Neuroscience.

[60]  P. Schyns,et al.  Cracking the Code of Oscillatory Activity , 2011, PLoS biology.

[61]  R. Romo,et al.  α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking , 2011, Proceedings of the National Academy of Sciences.

[62]  John J. Foxe,et al.  Ready, Set, Reset: Stimulus-Locked Periodicity in Behavioral Performance Demonstrates the Consequences of Cross-Sensory Phase Reset , 2011, The Journal of Neuroscience.

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

[64]  M. Catani,et al.  A lateralized brain network for visuospatial attention , 2011, Nature Neuroscience.

[65]  G. Rousselet,et al.  Single-Trial Analyses: Why Bother? , 2011, Front. Psychology.

[66]  G. Thut,et al.  Stimulus- and state-dependence of systematic bias in spatial attention: Additive effects of stimulus-size and time-on-task , 2012 .

[67]  C. Miniussi,et al.  The Functional Importance of Rhythmic Activity in the Brain , 2012, Current Biology.

[68]  Geraint Rees,et al.  Better Ways to Improve Standards in Brain-Behavior Correlation Analysis , 2012, Front. Hum. Neurosci..

[69]  M. Posner,et al.  The attention system of the human brain: 20 years after. , 2012, Annual review of neuroscience.

[70]  W. Klimesch Alpha-band oscillations, attention, and controlled access to stored information , 2012, Trends in Cognitive Sciences.

[71]  A. Craig,et al.  Regional brain wave activity changes associated with fatigue. , 2012, Psychophysiology.

[72]  J. Lange,et al.  Fluctuations of prestimulus oscillatory power predict subjective perception of tactile simultaneity. , 2012, Cerebral cortex.

[73]  Michael X. Cohen,et al.  Midfrontal conflict-related theta-band power reflects neural oscillations that predict behavior. , 2013, Journal of neurophysiology.

[74]  H. Lau,et al.  Prestimulus Oscillatory Activity over Motor Cortex Reflects Perceptual Expectations , 2013, The Journal of Neuroscience.

[75]  Manuel R. Mercier,et al.  Cortical cross-frequency coupling predicts perceptual outcomes , 2013, NeuroImage.

[76]  S. Kastner,et al.  Shifting Attentional Priorities: Control of Spatial Attention through Hemispheric Competition , 2013, The Journal of Neuroscience.

[77]  R. Oostenveld,et al.  Reduced Occipital Alpha Power Indexes Enhanced Excitability Rather than Improved Visual Perception , 2013, The Journal of Neuroscience.

[78]  Daniel P. Newman,et al.  Linking time-on-task, spatial bias and hemispheric activation asymmetry: A neural correlate of rightward attention drift , 2013, Neuropsychologia.

[79]  S. Kelly,et al.  Internal and External Influences on the Rate of Sensory Evidence Accumulation in the Human Brain , 2013, The Journal of Neuroscience.

[80]  Xiao Liu,et al.  EEG correlates of time-varying BOLD functional connectivity , 2013, NeuroImage.

[81]  G. Thut,et al.  Spatial attention: Differential shifts in pseudoneglect direction with time-on-task and initial bias support the idea of observer subtypes , 2013, Neuropsychologia.

[82]  Matthias M. Müller,et al.  Early visual and auditory processing rely on modality-specific attentional resources , 2013, NeuroImage.

[83]  G. Fink,et al.  Dorsal and Ventral Attention Systems: Distinct Neural Circuits but Collaborative Roles , 2013 .

[84]  G. Thut,et al.  A rightward shift in the visuospatial attention vector with healthy aging , 2014, Front. Aging Neurosci..

[85]  J. Schoffelen,et al.  Dissociated α-band modulations in the dorsal and ventral visual pathways in visuospatial attention and perception. , 2014, Cerebral cortex.

[86]  J. Schoffelen,et al.  University of Birmingham Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex , 2014 .

[87]  Gregor Thut,et al.  On the neural origin of pseudoneglect: EEG-correlates of shifts in line bisection performance with manipulation of line length☆ , 2014, NeuroImage.

[88]  Lei Ai,et al.  The phase of prestimulus alpha oscillations affects tactile perception. , 2014, Journal of neurophysiology.

[89]  J. Gross Analytical methods and experimental approaches for electrophysiological studies of brain oscillations , 2014, Journal of Neuroscience Methods.

[90]  Maximilien Chaumon,et al.  Prestimulus Neural Oscillations Inhibit Visual Perception via Modulation of Response Gain , 2014, Journal of Cognitive Neuroscience.

[91]  Michael X. Cohen,et al.  Attention and Temporal Expectations Modulate Power, Not Phase, of Ongoing Alpha Oscillations , 2015, Journal of Cognitive Neuroscience.

[92]  Iain D. Gilchrist,et al.  The contribution of pre-stimulus neural oscillatory activity to spontaneous response time variability , 2015, NeuroImage.

[93]  C. Tenke,et al.  Surface Laplacians (SL) and phase properties of EEG rhythms: Simulated generators in a volume-conduction model. , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[94]  Michael J. Morais,et al.  Global network influences on local functional connectivity , 2015, Nature Neuroscience.

[95]  Stella F. Lourenco,et al.  Right hemisphere control of visuospatial attention in near space , 2015, Neuropsychologia.

[96]  C. Miniussi,et al.  Non-linear effects of transcranial direct current stimulation as a function of individual baseline performance: Evidence from biparietal tDCS influence on lateralized attention bias , 2015, Cortex.

[97]  P. Veltink,et al.  Observation of time-dependent psychophysical functions and accounting for threshold drifts , 2015, Attention, perception & psychophysics.

[98]  Jürgen Kayser,et al.  On the benefits of using surface Laplacian (current source density) methodology in electrophysiology. , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[99]  Gerard M. Loughnane,et al.  Behavioral and electrophysiological evidence of opposing lateral visuospatial asymmetries in the upper and lower visual fields , 2015, Cortex.

[100]  T. Wager,et al.  Distinct Brain Systems Mediate the Effects of Nociceptive Input and Self-Regulation on Pain , 2015, PLoS biology.

[101]  Conrado A. Bosman,et al.  A jackknife approach to quantifying single-trial correlation between covariance-based metrics undefined on a single-trial basis , 2015, NeuroImage.

[102]  Christopher W. Pleydell-Pearce,et al.  The phase of pre-stimulus alpha oscillations influences the visual perception of stimulus timing , 2016, NeuroImage.

[103]  Daniel P. Newman,et al.  Ocular exposure to blue-enriched light has an asymmetric influence on neural activity and spatial attention , 2016, Scientific Reports.

[104]  Caspar M. Schwiedrzik,et al.  Expecting to See a Letter: Alpha Oscillations as Carriers of Top-Down Sensory Predictions. , 2016, Cerebral cortex.

[105]  J. Gross,et al.  Individual Human Brain Areas Can Be Identified from Their Characteristic Spectral Activation Fingerprints , 2016, PLoS biology.

[106]  Lee M. Miller,et al.  The Role of Alpha Activity in Spatial and Feature-Based Attention , 2016, eNeuro.

[107]  H.A. Slagter,et al.  Facilitation and inhibition in attention: Functional dissociation of pre-stimulus alpha activity, P1, and N1 components , 2016, NeuroImage.

[108]  T. Nef,et al.  The asymmetrical influence of increasing time-on-task on attentional disengagement , 2016, Neuropsychologia.

[109]  P. Corballis,et al.  Prestimulus alpha power influences response criterion in a detection task. , 2016, Psychophysiology.

[110]  R. VanRullen How to evaluate phase differences between trial groups in ongoing electrophysiological signals , 2016, bioRxiv.

[111]  W. El-Deredy,et al.  Pre-stimulus alpha oscillations over somatosensory cortex predict tactile misperceptions , 2017, Neuropsychologia.

[112]  Daniel P. Newman,et al.  Visuospatial Asymmetries Arise from Differences in the Onset Time of Perceptual Evidence Accumulation , 2017, The Journal of Neuroscience.

[113]  B. Postle,et al.  Prestimulus alpha-band power biases visual discrimination confidence, but not accuracy , 2016, Consciousness and Cognition.

[114]  F. Mast,et al.  The Influence of Alertness on the Spatial Deployment of Visual Attention is Mediated by the Excitability of the Posterior Parietal Cortices , 2016, Cerebral cortex.

[115]  G. Lupyan,et al.  How prior knowledge prepares perception: Prestimulus oscillations carry perceptual expectations and influence early visual responses , 2016, bioRxiv.

[116]  Gregor Thut,et al.  Visual cortex responses reflect temporal structure of continuous quasi-rhythmic sensory stimulation , 2017, NeuroImage.

[117]  G. Thut,et al.  Inconsistent Effects of Parietal α-tACS on Pseudoneglect across Two Experiments: A Failed Internal Replication , 2017, Front. Psychol..

[118]  Sébastien M. Crouzet,et al.  Spontaneous Neural Oscillations Bias Perception by Modulating Baseline Excitability. , 2017, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[119]  Gregor Thut,et al.  Age-related reduction of hemispheric lateralisation for spatial attention: An EEG study , 2017, NeuroImage.