Self-reported Mind Wandering and Response Time Variability Differentiate Prestimulus Electroencephalogram Microstate Dynamics during a Sustained Attention Task

Brain activity continuously and spontaneously fluctuates during tasks of sustained attention. This spontaneous activity reflects the intrinsic dynamics of neurocognitive networks, which have been suggested to differentiate moments of externally directed task focus from episodes of mind wandering. However, the contribution of specific electrophysiological brain states and their millisecond dynamics to the experience of mind wandering is still unclear. In this study, we investigated the association between electroencephalogram microstate temporal dynamics and self-reported mind wandering. Thirty-six participants completed a sustained attention to response task in which they were asked to respond to frequently occurring upright faces (nontargets) and withhold responses to rare inverted faces (targets). Intermittently, experience sampling probes assessed whether participants were focused on the task or whether they were mind wandering (i.e., off-task). Broadband electroencephalography was recorded and segmented into a time series of brain electric microstates based on data-driven clustering of topographic voltage patterns. The strength, prevalence, and rate of occurrence of specific microstates differentiated on- versus off-task moments in the prestimulus epochs of trials preceding probes. Similar associations were also evident between microstates and variability in response times. Together, these findings demonstrate that distinct microstates and their millisecond dynamics are sensitive to the experience of mind wandering.

[1]  Jonathan Smallwood,et al.  Subjective experience and the attentional lapse: Task engagement and disengagement during sustained attention , 2004, Consciousness and Cognition.

[2]  Christoph M. Michel,et al.  EEG microstates of wakefulness and NREM sleep , 2012, NeuroImage.

[3]  M. Raichle The brain's default mode network. , 2015, Annual review of neuroscience.

[4]  James S. P. Macdonald,et al.  Trial-by-Trial Variations in Subjective Attentional State are Reflected in Ongoing Prestimulus EEG Alpha Oscillations , 2011, Front. Psychology.

[5]  R. Compton,et al.  The wandering mind oscillates: EEG alpha power is enhanced during moments of mind-wandering , 2019, Cognitive, Affective, & Behavioral Neuroscience.

[6]  Jonathan W. Schooler,et al.  Early event-related brain potentials and hemispheric asymmetries reveal mind-wandering while reading and predict comprehension , 2015, Biological Psychology.

[7]  Han Yuan,et al.  Spatiotemporal dynamics of the brain at rest — Exploring EEG microstates as electrophysiological signatures of BOLD resting state networks , 2012, NeuroImage.

[8]  Aaron Kucyi,et al.  Just a thought: How mind-wandering is represented in dynamic brain connectivity , 2017, NeuroImage.

[9]  Christoph M. Michel,et al.  Spatiotemporal Analysis of Multichannel EEG: CARTOOL , 2011, Comput. Intell. Neurosci..

[10]  Thomas Koenig,et al.  15 Years of Microstate Research in Schizophrenia – Where Are We? A Meta-Analysis , 2016, Front. Psychiatry.

[11]  Jonathan Smallwood,et al.  The Decoupled Mind: Mind-wandering Disrupts Cortical Phase-locking to Perceptual Events , 2014, Journal of Cognitive Neuroscience.

[12]  Thomas Koenig,et al.  Electrical Neuroimaging in the time domain , 2009 .

[13]  Kevin Fitzpatrick,et al.  Slow Fluctuations in Attentional Control of Sensory Cortex , 2011, Journal of Cognitive Neuroscience.

[14]  Jonathan Smallwood,et al.  Going AWOL in the Brain: Mind Wandering Reduces Cortical Analysis of External Events , 2008, Journal of Cognitive Neuroscience.

[15]  Todd C. Handy,et al.  The neurocognitive consequences of the wandering mind: a mechanistic account of sensory-motor decoupling , 2013, Front. Psychol..

[16]  Jason S. Nomi,et al.  Dynamic brain network configurations during rest and an attention task with frequent occurrence of mind wandering , 2019, Human brain mapping.

[17]  Hao-Ting Wang,et al.  Dimensions of Experience: Exploring the Heterogeneity of the Wandering Mind , 2018, Psychological science.

[18]  E. Rosch,et al.  The Embodied Mind: Cognitive Science and Human Experience , 1993 .

[19]  M. D’Esposito,et al.  Functional Characterization of the Cingulo-Opercular Network in the Maintenance of Tonic Alertness. , 2015, Cerebral cortex.

[20]  Jonathan P. McNulty,et al.  The salience network is responsible for switching between the default mode network and the central executive network: Replication from DCM , 2014, NeuroImage.

[21]  Wolfgang Skrandies,et al.  Global field power and topographic similarity , 2005, Brain Topography.

[22]  Michael A. Pitts,et al.  Right parietal brain activity precedes perceptual alternation during binocular rivalry , 2011, Human brain mapping.

[23]  T. Handy,et al.  Visual asymmetry revisited: Mind wandering preferentially disrupts processing in the left visual field , 2014, Brain and Cognition.

[24]  Francisco J. Varela,et al.  The Embodied Mind , 2018 .

[25]  Christoph M. Michel,et al.  EEG Source Imaging: A Practical Review of the Analysis Steps , 2019, Front. Neurol..

[26]  E. Wascher,et al.  Inter-trial alpha power indicates mind wandering. , 2020, Psychophysiology.

[27]  I. Kirsch,et al.  Questions and Controversies. , 2006 .

[28]  L. Yao,et al.  Top-Down Regulation of Default Mode Activity in Spatial Visual Attention , 2013, The Journal of Neuroscience.

[29]  D. Schacter,et al.  Mind-Wandering as a Natural Kind: A Family-Resemblances View , 2018, Trends in Cognitive Sciences.

[30]  D. Margulies,et al.  Reductions in task positive neural systems occur with the passage of time and are associated with changes in ongoing thought , 2020, Scientific Reports.

[31]  A. Zanesco EEG Electric Field Topography is Stable During Moments of High Field Strength , 2020, Brain Topography.

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

[33]  Dimitri Van De Ville,et al.  BOLD correlates of EEG topography reveal rapid resting-state network dynamics , 2010, NeuroImage.

[34]  Dietrich Lehmann,et al.  The functional significance of EEG microstates—Associations with modalities of thinking , 2016, NeuroImage.

[35]  Claire Braboszcz,et al.  Lost in thoughts: Neural markers of low alertness during mind wandering , 2011, NeuroImage.

[36]  J. Smallwood,et al.  The science of mind wandering: empirically navigating the stream of consciousness. , 2015, Annual review of psychology.

[37]  T. Koenig,et al.  Brain electric microstates and momentary conscious mind states as building blocks of spontaneous thinking: I. Visual imagery and abstract thoughts. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[38]  R. Cotterill CyberChild - A simulation test-bed for consciousness studies , 2003 .

[39]  M. Albert,et al.  The Science of the Mind , 1997, Science.

[40]  J. Smallwood,et al.  The restless mind. , 2006, Psychological bulletin.

[41]  Christoph M. Michel,et al.  EEG-microstate dependent emergence of perceptual awareness , 2014, Front. Behav. Neurosci..

[42]  Dimitri Van De Ville,et al.  Electroencephalographic Resting-State Networks: Source Localization of Microstates , 2017, Brain Connect..

[43]  J. Schooler,et al.  Disentangling decoupling: comment on Smallwood (2013). , 2013, Psychological bulletin.

[44]  Erin J. Wamsley,et al.  Spontaneous Entry into an “Offline” State during Wakefulness: A Mechanism of Memory Consolidation? , 2020, Journal of Cognitive Neuroscience.

[45]  J. Smallwood Distinguishing how from why the mind wanders: a process-occurrence framework for self-generated mental activity. , 2013, Psychological bulletin.

[46]  F. D. Silva Neural mechanisms underlying brain waves: from neural membranes to networks. , 1991 .

[47]  Vince D. Calhoun,et al.  Questions and controversies in the study of time-varying functional connectivity in resting fMRI , 2020, Network Neuroscience.

[48]  Jonathan S. A. Carriere,et al.  How few and far between? Examining the effects of probe rate on self-reported mind wandering , 2013, Front. Psychol..

[49]  Jeffrey D. Wammes,et al.  On the Clock: Evidence for the Rapid and Strategic Modulation of Mind Wandering , 2018, Psychological science.

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

[51]  Mikaël Bastian,et al.  Mind wandering at the fingertips: automatic parsing of subjective states based on response time variability , 2013, Front. Psychol..

[52]  R. D. Pascual-Marqui,et al.  The EEG microstate topography is predominantly determined by intracortical sources in the alpha band , 2017, NeuroImage.

[53]  Jelmer P. Borst,et al.  Predicting task-general mind-wandering with EEG , 2019, Cognitive, Affective, & Behavioral Neuroscience.

[54]  B T Thomas Yeo,et al.  Towards a Universal Taxonomy of Macro-scale Functional Human Brain Networks , 2019, Brain Topography.

[55]  R. Nathan Spreng,et al.  The wandering brain: Meta-analysis of functional neuroimaging studies of mind-wandering and related spontaneous thought processes , 2015, NeuroImage.

[56]  D. Lehmann Multichannel topography of human alpha EEG fields. , 1971, Electroencephalography and clinical neurophysiology.

[57]  Daniel L. Schacter,et al.  Large-scale network interactions involved in dividing attention between the external environment and internal thoughts to pursue two distinct goals , 2019, NeuroImage.

[58]  Deepti R. Bathula,et al.  Investigating the temporal dynamics of electroencephalogram (EEG) microstates using recurrent neural networks , 2020, Human brain mapping.

[59]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[60]  Carryl L. Baldwin,et al.  Detecting and Quantifying Mind Wandering during Simulated Driving , 2017, Front. Hum. Neurosci..

[61]  Brandon G. King,et al.  Within and between-person correlates of the temporal dynamics of resting EEG microstates , 2019, NeuroImage.

[62]  Amishi P. Jha,et al.  Attenuated Face Processing during Mind Wandering , 2018, Journal of Cognitive Neuroscience.

[63]  D Lehmann,et al.  EEG alpha map series: brain micro-states by space-oriented adaptive segmentation. , 1987, Electroencephalography and clinical neurophysiology.

[64]  M. Ding,et al.  Neural mechanisms of internal distraction suppression in visual attention , 2019, Cortex.

[65]  Thomas Koenig,et al.  EEG microstates as a tool for studying the temporal dynamics of whole-brain neuronal networks: A review , 2017, NeuroImage.

[66]  Á. Pascual-Leone,et al.  Microstates in resting-state EEG: Current status and future directions , 2015, Neuroscience & Biobehavioral Reviews.

[67]  Christoph M. Michel,et al.  Capturing the spatiotemporal dynamics of self-generated, task-initiated thoughts with EEG and fMRI , 2019, NeuroImage.

[68]  Tracy Brown,et al.  The Embodied Mind: Cognitive Science and Human Experience , 2002, Cybern. Hum. Knowing.

[69]  I. Robertson,et al.  `Oops!': Performance correlates of everyday attentional failures in traumatic brain injured and normal subjects , 1997, Neuropsychologia.

[70]  Amishi P. Jha,et al.  Experience sampling of the degree of mind wandering distinguishes hidden attentional states , 2020, Cognition.

[71]  Elizabeth Jefferies,et al.  Situating the default-mode network along a principal gradient of macroscale cortical organization , 2016, Proceedings of the National Academy of Sciences.

[72]  M. Smith,et al.  The Core System , 2017 .

[73]  Hao-Ting Wang,et al.  The ebb and flow of attention: Between-subject variation in intrinsic connectivity and cognition associated with the dynamics of ongoing experience , 2019, NeuroImage.

[74]  F. Varela,et al.  NEUROPHENOMENOLOGY A Methodological Remedy for the Hard Problem , 1996 .

[75]  Enzo Tagliazucchi,et al.  Information-theoretical analysis of resting state EEG microstate sequences - non-Markovianity, non-stationarity and periodicities , 2017, NeuroImage.

[76]  Zachary C. Irving,et al.  The Neuroscience of Spontaneous Thought: An Evolving, Interdisciplinary Field , 2017, 1704.02533.

[77]  Zachary C. Irving,et al.  Mind-wandering as spontaneous thought: a dynamic framework , 2016, Nature Reviews Neuroscience.

[78]  Jonathan W. Schooler,et al.  States of Mind: Characterizing the Neural Bases of Focus and Mind-wandering through Dynamic Functional Connectivity , 2017, Journal of Cognitive Neuroscience.

[79]  Daniel Smilek,et al.  Wandering minds and wavering rhythms: linking mind wandering and behavioral variability. , 2013, Journal of experimental psychology. Human perception and performance.

[80]  M. Kane,et al.  What Mind Wandering Reveals About Executive-Control Abilities and Failures , 2012 .

[81]  Aaron Kucyi,et al.  Dynamic functional connectivity of the default mode network tracks daydreaming , 2014, NeuroImage.

[82]  E. Thompson,et al.  Neurophenomenology Integrating Subjective Experience and Brain Dynamics in the Neuroscience of Consciousness , 2003 .

[83]  Benjamin A. Seitzman,et al.  Cognitive manipulation of brain electric microstates , 2017, NeuroImage.

[84]  R. N. Spreng,et al.  The default network and self‐generated thought: component processes, dynamic control, and clinical relevance , 2014, Annals of the New York Academy of Sciences.

[85]  H G Vaughan,et al.  THE NEURAL ORIGINS OF HUMAN EVENT‐RELATED POTENTIALS * , 1980, Annals of the New York Academy of Sciences.