The neurocognitive consequences of the wandering mind: a mechanistic account of sensory-motor decoupling

A unique human characteristic is our ability to mind wander – a state in which we are free to engage in thoughts that are not directly tied to sensations and perceptions from our immediate physical environment. From a neurocognitive perspective, it has been proposed that during mind wandering, our executive resources are decoupled from the external environment and directed to these internal thoughts. In this review, we examine an underappreciated aspect of this phenomenon – attenuation of sensory-motor processing – from two perspectives. First, we describe the range of widespread sensory, cognitive and motor processes attenuated during mind wandering states, and how this impacts our neurocognitive processing of external events. We then consider sensory-motor attenuation in a class of clinical neurocognitive disorders that have ties to pathological patterns of decoupling, reviews suggesting that mind wandering and these clinical states may share a common mechanism of sensory-motor attenuation. Taken together, these observations suggest the sensory-motor consequences of decoupled thinking are integral to normal and pathological neurocognitive states.

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

[2]  M. Kane,et al.  Does mind wandering reflect executive function or executive failure? Comment on Smallwood and Schooler (2006) and Watkins (2008). , 2010, Psychological bulletin.

[3]  Marty G. Woldorff,et al.  Momentary reductions of attention permit greater processing of irrelevant stimuli , 2009, NeuroImage.

[4]  A. Kingstone,et al.  The eyes have it! Reflexive orienting is triggered by nonpredictive gaze , 1998 .

[5]  David J. Turk,et al.  Self-reflection and the temporal focus of the wandering mind , 2011, Consciousness and Cognition.

[6]  Jonathan S. A. Carriere,et al.  Everyday attention lapses and memory failures: The affective consequences of mindlessness , 2008, Consciousness and Cognition.

[7]  Erik D. Reichle,et al.  Meta-awareness, perceptual decoupling and the wandering mind , 2011, Trends in Cognitive Sciences.

[8]  Steve Majerus,et al.  Neural Correlates of Ongoing Conscious Experience: Both Task-Unrelatedness and Stimulus-Independence Are Related to Default Network Activity , 2011, PloS one.

[9]  David W. Frank,et al.  Stimulus-driven reorienting in the ventral frontoparietal attention network: the role of emotional content , 2012, Front. Hum. Neurosci..

[10]  H J Keselman,et al.  A generally robust approach to hypothesis testing in independent and correlated groups designs. , 2003, Psychophysiology.

[11]  R. Schmidt,et al.  VARIABILITY OF PRACTICE AND IMPLICIT MOTOR LEARNING , 1997 .

[12]  R. Kaplan,et al.  The Experience of Nature: A Psychological Perspective , 1989 .

[13]  Tianzi Jiang,et al.  Altered resting-state functional connectivity patterns of anterior cingulate cortex in adolescents with attention deficit hyperactivity disorder , 2006, Neuroscience Letters.

[14]  M. Kane,et al.  Conducting the train of thought: working memory capacity, goal neglect, and mind wandering in an executive-control task. , 2009, Journal of experimental psychology. Learning, memory, and cognition.

[15]  E. Klinger,et al.  Daydreaming and Fantasizing: Thought Flow and Motivation , 2008 .

[16]  G. Hajcak,et al.  Differentiating neural responses to emotional pictures: evidence from temporal-spatial PCA. , 2009, Psychophysiology.

[17]  L. Boyd,et al.  Excitatory repetitive transcranial magnetic stimulation to left dorsal premotor cortex enhances motor consolidation of new skills , 2009, BMC Neuroscience.

[18]  R. Knight,et al.  Neural Mechanisms of Involuntary Attention to Acoustic Novelty and Change , 1998, Journal of Cognitive Neuroscience.

[19]  L. Giambra,et al.  A Laboratory Method for Investigating Influences on Switching Attention to Task-Unrelated Imagery and Thought , 1995, Consciousness and Cognition.

[20]  J. Smallwood,et al.  Inspired by Distraction : Mind Wandering Facilitates Creative Incubation , 2012 .

[21]  Kevin S. Brown,et al.  Cooperation between the default mode network and the frontal–parietal network in the production of an internal train of thought , 2012, Brain Research.

[22]  B. Baars.  A cognitive theory of consciousness , 1988 .

[23]  Evelyn Barron,et al.  Absorbed in Thought , 2011, Psychological science.

[24]  D. Kahneman,et al.  Attention and Effort , 1973 .

[25]  Clay B. Holroyd,et al.  Reward prediction error signals associated with a modified time estimation task. , 2007, Psychophysiology.

[26]  R. Barkley.  Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. , 1997, Psychological bulletin.

[27]  James W. Tanaka,et al.  Learning to Become an Expert: Reinforcement Learning and the Acquisition of Perceptual Expertise , 2009, Journal of Cognitive Neuroscience.

[28]  Charles Dobson,et al.  Evaluative and generative modes of thought during the creative process , 2012, NeuroImage.

[29]  C. Vázquez,et al.  Automatic and effortful processing in depression. , 1993, Psychological bulletin.

[30]  C. Braun,et al.  Event-Related Brain Potentials Following Incorrect Feedback in a Time-Estimation Task: Evidence for a Generic Neural System for Error Detection , 1997, Journal of Cognitive Neuroscience.

[31]  Carolee J Winstein,et al.  Providing explicit information disrupts implicit motor learning after basal ganglia stroke. , 2004, Learning & memory.

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

[33]  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.

[34]  C. Escera,et al.  Role of Mismatch Negativity and Novelty-P3 in Involuntary Auditory Attention , 2007 .

[35]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[36]  Yvonne Freeh,et al.  An R and S–PLUS Companion to Applied Regression , 2004 .

[37]  Shihui Han,et al.  Temporal dynamic of neural mechanisms involved in empathy for pain: An event-related brain potential study , 2008, Neuropsychologia.

[38]  Michelle G. Craske,et al.  Worry and Rumination: Repetitive Thought as a Concomitant and Predictor of Negative Mood , 2000, Cognitive Therapy and Research.

[39]  B. Pennington,et al.  Validity of the Executive Function Theory of Attention-Deficit/Hyperactivity Disorder: A Meta-Analytic Review , 2005, Biological Psychiatry.

[40]  S. Delplanque,et al.  Modulation of cognitive processing by emotional valence studied through event-related potentials in humans , 2004, Neuroscience Letters.

[41]  J. Andrews-Hanna,et al.  Not all minds that wander are lost: the importance of a balanced perspective on the mind-wandering state , 2013, Front. Psychol..

[42]  William S Helton,et al.  Impulsive responding and the sustained attention to response task , 2009, Journal of clinical and experimental neuropsychology.

[43]  Hongkeun Kim,et al.  A dual-subsystem model of the brain's default network: Self-referential processing, memory retrieval processes, and autobiographical memory retrieval , 2012, NeuroImage.

[44]  Viviana Betti,et al.  Synchronous with Your Feelings: Sensorimotor γ Band and Empathy for Pain , 2009, The Journal of Neuroscience.

[45]  Todd C. Handy,et al.  Mind Wandering and the Adaptive Control of Attentional Resources , 2013, Journal of Cognitive Neuroscience.

[46]  Todd C. Handy,et al.  Neural systems mediating field and observer memories , 2009, Neuropsychologia.

[47]  J. Gabrieli,et al.  Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia , 2009, Proceedings of the National Academy of Sciences.

[48]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  M. Carrasco,et al.  PSYCHOLOGICAL SCIENCE Research Article Emotion Facilitates Perception and Potentiates the Perceptual Benefits of Attention , 2022 .

[50]  J. Polich.  Updating P 300 : An Integrative Theory of P 3 a and P 3 b , 2009 .

[51]  R. McCarley,et al.  Reductions in the N1 and P2 auditory event-related potentials in first-hospitalized and chronic schizophrenia. , 2010, Schizophrenia bulletin.

[52]  E. Fox,et al.  Do threatening stimuli draw or hold visual attention in subclinical anxiety? , 2001, Journal of experimental psychology. General.

[53]  B. Levine,et al.  The functional neuroanatomy of autobiographical memory: A meta-analysis , 2006, Neuropsychologia.

[54]  Xiaosi Gu,et al.  Attention and reality constraints on the neural processes of empathy for pain , 2007, NeuroImage.

[55]  K. Craig,et al.  Facing others in pain: the effects of empathy , 2005, Pain.

[56]  Daniel L Schacter,et al.  Amygdala Activity Is Associated with the Successful Encoding of Item, But Not Source, Information for Positive and Negative Stimuli , 2006, The Journal of Neuroscience.

[57]  Romina Moavero,et al.  The neurobiology of attention deficit/hyperactivity disorder. , 2009, European journal of paediatric neurology : EJPN : official journal of the European Paediatric Neurology Society.

[58]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[59]  R. Näätänen,et al.  Attention and mismatch negativity. , 1993, Psychophysiology.

[60]  D. Gilbert,et al.  A Wandering Mind Is an Unhappy Mind , 2010, Science.

[61]  Jesse Rosenthal,et al.  Excessive daydreaming: A case history and discussion of mind wandering and high fantasy proneness , 2009, Consciousness and Cognition.

[62]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[63]  J. Smallwood,et al.  Encoding during the attentional lapse: Accuracy of encoding during the semantic sustained attention to response task , 2006, Consciousness and Cognition.

[64]  David J. Turk,et al.  Placing a tool in the spotlight: spatial attention modulates visuomotor responses in cortex , 2005, NeuroImage.

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

[66]  Ralf Engbert,et al.  Your mind wanders weakly, your mind wanders deeply: Objective measures reveal mindless reading at different levels , 2012, Cognition.

[67]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[68]  Michael J Kane,et al.  Drifting from slow to "D'oh!": working memory capacity and mind wandering predict extreme reaction times and executive control errors. , 2012, Journal of experimental psychology. Learning, memory, and cognition.

[69]  Amishi P. Jha,et al.  Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain , 2005, NeuroImage.

[70]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[71]  Ann K. Shinn,et al.  Abnormal Medial Prefrontal Cortex Resting-State Connectivity in Bipolar Disorder and Schizophrenia , 2011, Neuropsychopharmacology.

[72]  Alan D. Baddeley,et al.  Working memory and stimulus-independent thought: Effects of memory load and presentation rate , 1993 .

[73]  E. Klinger,et al.  Consequences of commitment to and disengagement from incentives. , 1975 .

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

[75]  C. Beevers,et al.  Neural mechanisms of the cognitive model of depression , 2011, Nature Reviews Neuroscience.

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

[77]  Gutti J. Babu,et al.  Fundamentals of Modern Statistical Methods , 2002, Technometrics.

[78]  F. Castellanos,et al.  Spontaneous attentional fluctuations in impaired states and pathological conditions: A neurobiological hypothesis , 2007, Neuroscience & Biobehavioral Reviews.

[79]  Jayne Bigelsen,et al.  Compulsive fantasy: Proposed evidence of an under-reported syndrome through a systematic study of 90 self-identified non-normative fantasizers , 2011, Consciousness and Cognition.

[80]  S. Hillyard,et al.  Modulations of sensory-evoked brain potentials indicate changes in perceptual processing during visual-spatial priming. , 1991, Journal of experimental psychology. Human perception and performance.

[81]  Wei Li,et al.  Perspective taking modulates event-related potentials to perceived pain , 2010, Neuroscience Letters.

[82]  R. Näätänen,et al.  Auditory frequency discrimination and event-related potentials. , 1985, Electroencephalography and clinical neurophysiology.

[83]  A. Fingelkurts,et al.  Persistent operational synchrony within brain default-mode network and self-processing operations in healthy subjects , 2011, Brain and Cognition.

[84]  F. Castellanos,et al.  Characterizing cognition in ADHD: beyond executive dysfunction , 2006, Trends in Cognitive Sciences.

[85]  S. Luck,et al.  Electrocortical substrates of visual selective attention , 1993 .

[86]  J. Decety,et al.  Human Empathy Through the Lens of Social Neuroscience , 2006, TheScientificWorldJournal.

[87]  Jonathan Smallwood,et al.  Pupillometric Evidence for the Decoupling of Attention from Perceptual Input during Offline Thought , 2011, PloS one.

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

[89]  Danielle Mizuiri,et al.  A lack of default network suppression is linked to increased distractibility in ADHD , 2009, Brain Research.

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

[91]  Robert J. Zatorre,et al.  Mental Concerts: Musical Imagery and Auditory Cortex , 2005, Neuron.

[92]  S. Hillyard,et al.  Modulation of early auditory processing during selective listening to rapidly presented tones. , 1991, Electroencephalography and clinical neurophysiology.

[93]  M. Gazzaniga,et al.  Combined spatial and temporal imaging of brain activity during visual selective attention in humans , 1994, Nature.

[94]  Alan Kingstone,et al.  Brain Responses to Biological Relevance , 2008, Journal of Cognitive Neuroscience.

[95]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[96]  R. Näätänen.  The role of attention in auditory information processing as revealed by event-related potentials and other brain measures of cognitive function , 1990, Behavioral and Brain Sciences.

[97]  S. Preston,et al.  Empathy: Its ultimate and proximate bases. , 2001, The Behavioral and brain sciences.

[98]  L M Giambra,et al.  Daydreaming as a Function of Cueing and Task Difficulty , 1973, Perceptual and motor skills.

[99]  R. McCarley,et al.  Auditory ERPs to non-target stimuli in schizophrenia: relationship to probability, task-demands, and target ERPs. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[100]  M. Scherg,et al.  A Source Analysis of the Late Human Auditory Evoked Potentials , 1989, Journal of Cognitive Neuroscience.

[101]  Todd C. Handy,et al.  Mind wandering and motor control: off-task thinking disrupts the online adjustment of behavior , 2012, Front. Hum. Neurosci..

[102]  Lawrence M. Ward,et al.  Human Neuroscience Original Research Article Differential Synchronization in Default and Task-specific Networks of the Human Brain , 2022 .

[103]  Viviana Betti,et al.  Seeing the pain of others while being in pain: A laser-evoked potentials study , 2008, NeuroImage.

[104]  岸田弥奈.  自閉症患者におけるresting state functional MRIの検討 , 2014 .

[105]  L. Phillips,et al.  Shifting moods, wandering minds: negative moods lead the mind to wander. , 2009, Emotion.

[106]  W. Krieg.  Functional Neuroanatomy , 1953, Springer Series in Experimental Entomology.

[107]  R. Kaplan,et al.  The Experience of Nature , 2022, Why Conserve Nature?.

[108]  M. Mintun,et al.  Resting-state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus , 2010, Proceedings of the National Academy of Sciences.

[109]  J. Smallwood,et al.  Inspired by Distraction , 2012, Psychological science.

[110]  P. Fox,et al.  Retinotopic organization of early visual spatial attention effects as revealed by PET and ERPs , 1997, Human brain mapping.

[111]  Erich Schröger,et al.  Auditory distraction: event-related potential and behavioral indices , 2000, Clinical Neurophysiology.

[112]  P. Schwartzkroin,et al.  Neural mechanisms. , 1994, Science.

[113]  A. Arnsten,et al.  Fundamentals of attention-deficit/hyperactivity disorder: circuits and pathways. , 2006, The Journal of clinical psychiatry.

[114]  M. Posner,et al.  Short-term meditation training improves attention and self-regulation , 2007, Proceedings of the National Academy of Sciences.

[115]  R. Dolan,et al.  Modulation of spatial attention by fear-conditioned stimuli: an event-related fMRI study , 2002, Neuropsychologia.

[116]  K. Christoff,et al.  Experience sampling during fMRI reveals default network and executive system contributions to mind wandering , 2009, Proceedings of the National Academy of Sciences.

[117]  Georg Northoff,et al.  Self-referential processing in our brain—A meta-analysis of imaging studies on the self , 2006, NeuroImage.

[118]  Scott T. Grafton,et al.  Wandering Minds: The Default Network and Stimulus-Independent Thought , 2007, Science.

[119]  Gaspare Galati,et al.  Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain , 2005, Nature Neuroscience.

[120]  Claire Braboszcz,et al.  Meditation and neuroscience: From basic research to clinical practice. , 2010 .

[121]  A. Baddeley,et al.  Stimulus-independent thought depends on central executive resources , 1995, Memory & cognition.

[122]  Scott T. Grafton,et al.  Graspable objects grab attention when the potential for action is recognized , 2003, Nature Neuroscience.

[123]  W. M. Cox,et al.  Dimensions of Thought Flow in Everyday Life , 1987 .

[124]  J. Polich.  Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[125]  J. Duncan,et al.  Competitive brain activity in visual attention , 1997, Current Opinion in Neurobiology.

[126]  C. Frith,et al.  The Role of Working Memory in Visual Selective Attention , 2001, Science.

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

[128]  Christoph Klein,et al.  Intra-Subject Variability in Attention-Deficit Hyperactivity Disorder , 2006, Biological Psychiatry.

[129]  D. Schacter,et al.  Remembering the past to imagine the future: the prospective brain , 2007, Nature Reviews Neuroscience.

[130]  L. Kvavilashvili,et al.  From mind-pops to hallucinations? A study of involuntary semantic memories in schizophrenia , 2012, Psychiatry Research.

[131]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[132]  M. Rosenberg,et al.  In the zone or zoning out? Tracking behavioral and neural fluctuations during sustained attention. , 2013, Cerebral cortex.

[133]  F. Castellanos,et al.  Varieties of Attention-Deficit/Hyperactivity Disorder-Related Intra-Individual Variability , 2005, Biological Psychiatry.

[134]  T. Handy,et al.  I don’t feel your pain (as much): The desensitizing effect of mind wandering on the perception of others’ discomfort , 2013, Cognitive, Affective, & Behavioral Neuroscience.

[135]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[136]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

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

[138]  R. Näätänen,et al.  Early selective-attention effect on evoked potential reinterpreted. , 1978, Acta psychologica.

[139]  R. Brown,et al.  Rumination and executive function in depression: an experimental study , 2002, Journal of neurology, neurosurgery, and psychiatry.

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

[141]  Ann K. Shinn,et al.  Default mode network abnormalities in bipolar disorder and schizophrenia , 2010, Psychiatry Research: Neuroimaging.

[142]  G. Glover,et al.  Resting-State Functional Connectivity in Major Depression: Abnormally Increased Contributions from Subgenual Cingulate Cortex and Thalamus , 2007, Biological Psychiatry.

[143]  Jonathan S. A. Carriere,et al.  Absent-mindedness: Lapses of conscious awareness and everyday cognitive failures , 2006, Consciousness and Cognition.

[144]  K. Christoff,et al.  Undirected thought: Neural determinants and correlates , 2012, Brain Research.

[145]  L. Alloy,et al.  Rumination as a common mechanism relating depressive risk factors to depression. , 2001, Emotion.

[146]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[147]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[148]  J. Teasdale,et al.  Rumination and overgeneral memory in depression: effects of self-focus and analytic thinking. , 2001, Journal of abnormal psychology.

[149]  R. Buckner,et al.  Evidence for the Default Network's Role in Spontaneous Cognition , 2010 .

[150]  T. Hendler,et al.  Towards a Neuroscience of Mind-Wandering , 2011, Front. Hum. Neurosci..

[151]  Alan Kingstone,et al.  Attentional effects of counterpredictive gaze and arrow cues. , 2004, Journal of experimental psychology. Human perception and performance.

[152]  L. Giambra,et al.  Task-unrelated-thought frequency as a function of age: a laboratory study. , 1989, Psychology and aging.

[153]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]／Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[154]  J. Jonides,et al.  The Cognitive Benefits of Interacting With Nature , 2008, Psychological science.

[155]  J. Smallwood,et al.  When attention matters: The curious incident of the wandering mind , 2008, Memory & cognition.

[156]  S. Kosslyn,et al.  Neural Systems Shared by Visual Imagery and Visual Perception: A Positron Emission Tomography Study , 1997, NeuroImage.

[157]  Erik D. Reichle,et al.  Eye Movements During Mindless Reading , 2010, Psychological science.

[158]  Jonathan Smallwood,et al.  Task unrelated thought: The role of distributed processing , 2003, Consciousness and Cognition.

[159]  Jonathan Smallwood,et al.  Catching the mind in flight: Using behavioral indices to detect mindless reading in real time , 2011, Psychonomic bulletin & review.

[160]  T. R. Herzog,et al.  Reflection and attentional recovery as distinctive benefits of restorative environments , 1997 .

[161]  A. Jha,et al.  Mindfulness training modifies subsystems of attention , 2007, Cognitive, affective & behavioral neuroscience.

[162]  M. Kane,et al.  Tracking the train of thought from the laboratory into everyday life: An experience-sampling study of mind wandering across controlled and ecological contexts , 2009, Psychonomic bulletin & review.