Mindfulness-induced selflessness: a MEG neurophenomenological study

Contemporary philosophical and neurocognitive studies of the self have dissociated two distinct types of self-awareness: a “narrative” self-awareness (NS) weaving together episodic memory, future planning and self-evaluation into a coherent self-narrative and identity, and a “minimal” self-awareness (MS) focused on present momentary experience and closely tied to the sense of agency and ownership. Long-term Buddhist meditation practice aims at realization of a “selfless” mode of awareness (SL), where identification with a static sense of self is replaced by identification with the phenomenon of experiencing itself. NS-mediating mechanisms have been explored by neuroimaging, mainly fMRI, implicating prefrontal midline structures, but MS processes are not well characterized and SL even less so. To this end we tested 12 long-term mindfulness meditators using a neurophenomenological study design, incorporating both magnetoencephalogram (MEG) recordings and first person descriptions. We found that (1) NS attenuation involves extensive frontal, and medial prefrontal gamma band (60–80 Hz) power decreases, consistent with fMRI and intracranial EEG findings; (2) MS attenuation is related to beta-band (13–25 Hz) power decreases in a network that includes ventral medial prefrontal, medial posterior and lateral parietal regions; and (3) the experience of selflessness is linked to attenuation of beta-band activity in the right inferior parietal lobule. These results highlight the role of dissociable frequency-dependent networks in supporting different modes of self-processing, and the utility of combining phenomenology, mindfulness training and electrophysiological neuroimaging for characterizing self-awareness.

[1]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[2]  Lutz Jäncke,et al.  Pre-reflective and reflective self-reference: A spatiotemporal EEG analysis , 2008, NeuroImage.

[3]  Georg Northoff,et al.  How is our self related to midline regions and the default-mode network? , 2011, NeuroImage.

[4]  D. Spalding The Principles of Psychology , 1873, Nature.

[5]  Hans-Jochen Heinze,et al.  Differential parametric modulation of self‐relatedness and emotions in different brain regions , 2009, Human brain mapping.

[6]  Britta K. Hölzel,et al.  Mindfulness practice leads to increases in regional brain gray matter density , 2011, Psychiatry Research: Neuroimaging.

[7]  M. Hallett,et al.  The neural processes underlying self-agency. , 2011, Cerebral cortex.

[8]  K. Vogeley,et al.  The “sense of agency” and its underlying cognitive and neural mechanisms , 2008, Consciousness and Cognition.

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

[10]  Jonathan W. Schooler,et al.  Re-representing consciousness: dissociations between experience and meta-consciousness , 2002, Trends in Cognitive Sciences.

[11]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[12]  G. Rizzolatti,et al.  Through the looking glass: Self and others , 2011, Consciousness and Cognition.

[13]  T. Metzinger Being No One: The Self-Model Theory of Subjectivity , 2004 .

[14]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[15]  P. Ruby,et al.  What is self-specific? Theoretical investigation and critical review of neuroimaging results. , 2009, Psychological review.

[16]  P. Fossati,et al.  Medial prefrontal cortex and the self in major depression. , 2011, Journal of affective disorders.

[17]  C. Phillips,et al.  Impaired Effective Cortical Connectivity in Vegetative State: Preliminary Investigation Using PET , 1999, NeuroImage.

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

[19]  C. Hansel,et al.  Mind wandering. , 1956, British journal of psychology.

[20]  I. Fried,et al.  Coupling between Neuronal Firing Rate, Gamma LFP, and BOLD fMRI Is Related to Interneuronal Correlations , 2007, Current Biology.

[21]  David A. Silbersweig,et al.  Self-awareness, self-regulation, and self-transcendence (S-ART): a framework for understanding the neurobiological mechanisms of mindfulness , 2012, Front. Hum. Neurosci..

[22]  Philippe Kahane,et al.  Exploring the electrophysiological correlates of the default ‐ mode network with intracerebral EEG , 2022 .

[23]  Gareth R. Barnes,et al.  Group imaging of task-related changes in cortical synchronisation using nonparametric permutation testing , 2003, NeuroImage.

[24]  M. Iacoboni,et al.  The self and social cognition: the role of cortical midline structures and mirror neurons , 2007, Trends in Cognitive Sciences.

[25]  Habib Benali,et al.  Impact of meditation training on the default mode network during a restful state. , 2013, Social cognitive and affective neuroscience.

[26]  Antonio R. Damasio,et al.  Self comes to mind , 2008 .

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

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

[29]  A. Damasio,et al.  Persistence of feelings and sentience after bilateral damage of the insula. , 2013, Cerebral cortex.

[30]  D. Goleman,et al.  The Attention Revolution: Unlocking the Power of the Focused Mind , 2006 .

[31]  C. Frith,et al.  Experiencing Oneself vs Another Person as Being the Cause of an Action: The Neural Correlates of the Experience of Agency , 2002, NeuroImage.

[32]  R. Davidson Well-being and affective style: neural substrates and biobehavioural correlates. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[33]  Experimenting with introspection Comment from Shaun Gallagher , 2002, Trends in Cognitive Sciences.

[34]  S. Muthukumaraswamy,et al.  Modulation of the human mirror neuron system during cognitive activity. , 2008, Psychophysiology.

[35]  P. Fossati,et al.  Different brain structures related to self- and external-agency attribution: a brief review and meta-analysis , 2011, Brain Structure and Function.

[36]  S. Lisanby,et al.  Self-enhancement processing in the default network: a single-pulse TMS study , 2012, Experimental Brain Research.

[37]  Antonino Raffone,et al.  The ‘I’ and the ‘Me’ in self-referential awareness: a neurocognitive hypothesis , 2010, Cognitive Processing.

[38]  Dietrich Lehmann,et al.  Reduced functional connectivity between cortical sources in five meditation traditions detected with lagged coherence using EEG tomography , 2012, NeuroImage.

[39]  J. Gray,et al.  Meditation experience is associated with differences in default mode network activity and connectivity , 2011, Proceedings of the National Academy of Sciences.

[40]  Antoine Lutz,et al.  Buddha's Brain: Neuroplasticity and Meditation [In the Spotlight] , 2008, IEEE Signal Processing Magazine.

[41]  S. Goenka,et al.  The art of living : Vipassana meditation as taught by S.N. Goenka , 1990 .

[42]  Dieter Vaitl,et al.  Investigation of mindfulness meditation practitioners with voxel-based morphometry. , 2008, Social cognitive and affective neuroscience.

[43]  R. Gunderman,et al.  Emotional intelligence. , 2011, Journal of the American College of Radiology : JACR.

[44]  H. Heinze,et al.  The resting brain and our self: Self-relatedness modulates resting state neural activity in cortical midline structures , 2008, Neuroscience.

[45]  P. Haggard,et al.  Sense of agency , 2012, Current Biology.

[46]  A. Roepstorff Brains in Scanners: An Umwelt of Cognitive Neuroscience , 2001 .

[47]  Martial Van der Linden,et al.  Self-referential reflective activity and its relationship with rest: a PET study , 2005, NeuroImage.

[48]  J. Panksepp,et al.  The trans-species concept of self and the subcortical–cortical midline system , 2008, Trends in Cognitive Sciences.

[49]  O. Blanke,et al.  Multisensory Mechanisms in Temporo-Parietal Cortex Support Self-Location and First-Person Perspective , 2011, Neuron.

[50]  J. McGrath,et al.  The cognitive neuropsychology of schizophrenia. , 1997 .

[51]  A. Lutz,et al.  Attention regulation and monitoring in meditation , 2008, Trends in Cognitive Sciences.

[52]  A. Goldstein,et al.  Mindfulness-induced changes in gamma band activity – Implications for the default mode network, self-reference and attention , 2012, Clinical Neurophysiology.

[53]  R I Grossman,et al.  Brain imaging , 1999, Current Biology.

[54]  David J. Turk,et al.  The angular gyrus computes action awareness representations. , 2008, Cerebral cortex.

[55]  Evelyn C. Ferstl,et al.  Functional specialization within the anterior medial prefrontal cortex: a functional magnetic resonance imaging study with human subjects , 2003, Neuroscience Letters.

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

[57]  Britta K. Hölzel,et al.  How Does Mindfulness Meditation Work? Proposing Mechanisms of Action From a Conceptual and Neural Perspective , 2011, Perspectives on psychological science : a journal of the Association for Psychological Science.

[58]  A. Lutz,et al.  Meditation and the neuroscience of consciousness , 2007 .

[59]  Shaun Gallagher,et al.  Neurocognitive Models of Schizophrenia: A Neurophenomenological Critique , 2004, Psychopathology.

[60]  J. Gardiner Episodic memory and autonoetic consciousness: a first-person approach. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[61]  S. Rauch,et al.  Meditation experience is associated with increased cortical thickness , 2005, Neuroreport.

[62]  A. Damasio The Feeling of What Happens: Body and Emotion in the Making of Consciousness , 1999 .

[63]  J. Kabat-Zinn,et al.  Full catastrophe living : using the wisdom of your body and mind to face stress, pain, and illness , 1990 .

[64]  E. Meintjes,et al.  The neural substrates of mindfulness: An fMRI investigation , 2011, Social neuroscience.

[65]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[66]  A. Serretti,et al.  Does mindfulness training improve cognitive abilities? A systematic review of neuropsychological findings. , 2011, Clinical psychology review.

[67]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

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

[69]  G. Pagnoni,et al.  “Thinking about Not-Thinking”: Neural Correlates of Conceptual Processing during Zen Meditation , 2008, PloS one.

[70]  L. Barsalou,et al.  Effects of Meditation Experience on Functional Connectivity of Distributed Brain Networks , 2012, Front. Hum. Neurosci..

[71]  Peter C. Hansen,et al.  MEG. An introduction to methods , 2010 .

[72]  Jon Kabat-Zinn,et al.  Mindfulness: diverse perspectives on its meaning, origins, and multiple applications at the intersection of science and dharma , 2011 .

[73]  R. Zimmermann,et al.  MEG and EEG show different sensitivity to myogenic artifacts. , 2004, Neurology & clinical neurophysiology : NCN.

[74]  J. Decety,et al.  Effect of subjective perspective taking during simulation of action: a PET investigation of agency , 2001, Nature Neuroscience.

[75]  L. Pbert,et al.  Effectiveness of a meditation-based stress reduction program in the treatment of anxiety disorders. , 1992, The American journal of psychiatry.

[76]  A. Newen,et al.  Beyond the comparator model: A multifactorial two-step account of agency , 2008, Consciousness and Cognition.

[77]  Max A. Viergever,et al.  High frequency spectral components after Secobarbital: The contribution of muscular origin—A study with MEG/EEG , 2012, Epilepsy Research.

[78]  Juan R. Vidal,et al.  Transient Suppression of Broadband Gamma Power in the Default-Mode Network Is Correlated with Task Complexity and Subject Performance , 2011, The Journal of Neuroscience.

[79]  T. Sejnowski,et al.  Removal of eye activity artifacts from visual event-related potentials in normal and clinical subjects , 2000, Clinical Neurophysiology.

[80]  Rebecca Saxe,et al.  Associations and dissociations between default and self-reference networks in the human brain , 2011, NeuroImage.

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

[82]  Istvan Molnar-Szakacs,et al.  rTMS to the right inferior parietal lobule disrupts self-other discrimination. , 2006, Social cognitive and affective neuroscience.

[83]  Lama Ole Nydahl The Way Things Are: A Living Approach to Buddhism for Today's World , 1996 .

[84]  E. Thompson,et al.  Specifying the self for cognitive neuroscience , 2011, Trends in Cognitive Sciences.

[85]  C. Kerr,et al.  Developing an observing attitude: an analysis of meditation diaries in an MBSR clinical trial. , 2011, Clinical psychology & psychotherapy.

[86]  Bruce Luber,et al.  Self-specific processing in the default network: a single-pulse TMS study , 2010, Experimental Brain Research.

[87]  S. Gallagher Philosophical conceptions of the self: implications for cognitive science , 2000, Trends in Cognitive Sciences.

[88]  S. Gallagher,et al.  Experimenting with phenomenology , 2006, Consciousness and Cognition.

[89]  Justin S. Feinstein,et al.  Preserved Self-Awareness following Extensive Bilateral Brain Damage to the Insula, Anterior Cingulate, and Medial Prefrontal Cortices , 2012, PloS one.

[90]  A. Roepstorff,et al.  Introspection and cognitive brain mapping: from stimulus–response to script–report , 2002, Trends in Cognitive Sciences.

[91]  Steven Laureys,et al.  Brain function in coma, vegetative state, and related disorders , 2004, The Lancet Neurology.

[92]  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.

[93]  Scott T. Grafton,et al.  Response to Comment on "Wandering Minds: The Default Network and Stimulus-Independent Thought" , 2007, Science.

[94]  S. Muthukumaraswamy High-frequency brain activity and muscle artifacts in MEG/EEG: a review and recommendations , 2013, Front. Hum. Neurosci..

[95]  R. Buckner,et al.  Functional-Anatomic Fractionation of the Brain's Default Network , 2010, Neuron.

[96]  N. Allen,et al.  Mindful emotion regulation: An integrative review. , 2009, Clinical psychology review.

[97]  Virginia S. Y. Kwan,et al.  Assessing the neural correlates of self-enhancement bias: a transcranial magnetic stimulation study , 2007, Experimental Brain Research.

[98]  A. Engel,et al.  Spectral fingerprints of large-scale neuronal interactions , 2012, Nature Reviews Neuroscience.

[99]  K. Ressler,et al.  Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic , 2007, Nature Neuroscience.

[100]  K. Zilles,et al.  Neural Correlates of First-Person Perspective as One Constituent of Human Self-Consciousness , 2004, Journal of Cognitive Neuroscience.

[101]  Lawrence W. Barsalou,et al.  Mind wandering and attention during focused meditation: A fine-grained temporal analysis of fluctuating cognitive states , 2012, NeuroImage.

[102]  Claus Tempelmann,et al.  Are emotions associated with activity during rest or interoception? An exploratory fMRI study in healthy subjects , 2011, Neuroscience Letters.

[103]  J. Kabat-Zinn,et al.  An outpatient program in behavioral medicine for chronic pain patients based on the practice of mindfulness meditation: theoretical considerations and preliminary results. , 1982, General hospital psychiatry.

[104]  Se Robinson,et al.  Functional neuroimaging by Synthetic Aperture Magnetometry (SAM) , 1999 .

[105]  Matthew J. Brookes,et al.  Optimising experimental design for MEG beamformer imaging , 2008, NeuroImage.

[106]  G. Fink,et al.  Neural correlates of the first-person-perspective , 2003, Trends in Cognitive Sciences.

[107]  I. Fried,et al.  A Widely Distributed Spectral Signature of Task-Negative Electrocorticography Responses Revealed during a Visuomotor Task in the Human Cortex , 2012, The Journal of Neuroscience.

[108]  N. Farb,et al.  Attending to the present: mindfulness meditation reveals distinct neural modes of self-reference. , 2007, Social cognitive and affective neuroscience.

[109]  O. Blanke Multisensory brain mechanisms of bodily self-consciousness , 2012, Nature Reviews Neuroscience.

[110]  Evan Thompson,et al.  Asian perspectives: Indian theories of mind , 2007 .

[111]  Joachim Gross,et al.  Coherence in consciousness: Paralimbic gamma synchrony of self‐reference links conscious experiences , 2009, Human brain mapping.

[112]  J. Polich,et al.  Meditation states and traits: EEG, ERP, and neuroimaging studies. , 2006, Psychological bulletin.

[113]  H. Aach The art of living. , 1949, Journal - Michigan State Medical Society.

[114]  Stefan Thurner,et al.  Self-awareness and the subconscious effect of personal pronouns on word encoding: A magnetoencephalography (MEG) study , 2007, Neuropsychologia.

[115]  Krish D. Singh,et al.  Which “neural activity” do you mean? fMRI, MEG, oscillations and neurotransmitters , 2012, NeuroImage.

[116]  Hillary S. Schaefer,et al.  Neural correlates of attentional expertise in long-term meditation practitioners , 2007, Proceedings of the National Academy of Sciences.

[117]  U. Neisser Five kinds of self‐knowledge , 1988 .

[118]  A. Serretti,et al.  A systematic review of neurobiological and clinical features of mindfulness meditations , 2009, Psychological Medicine.

[119]  Kensuke Sekihara,et al.  A novel adaptive beamformer for MEG source reconstruction effective when large background brain activities exist , 2006, IEEE Transactions on Biomedical Engineering.

[120]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[121]  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.

[122]  Georg Northoff,et al.  Brain imaging of the self – Conceptual, anatomical and methodological issues , 2011, Consciousness and Cognition.

[123]  Matthew J. Brookes,et al.  Measuring functional connectivity using MEG: Methodology and comparison with fcMRI , 2011, NeuroImage.

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

[125]  R. Cabeza,et al.  Frontiers in Human Neuroscience , 2009 .

[126]  Nan-Kuei Chen,et al.  Meditation-State Functional Connectivity (msFC): Strengthening of the Dorsal Attention Network and Beyond , 2012, Evidence-based complementary and alternative medicine : eCAM.

[127]  P. Ekman,et al.  Buddhist and Psychological Perspectives on Emotions and Well-Being , 2005 .

[128]  Marc Jeannerod,et al.  Modulating the experience of agency: a positron emission tomography study , 2003, NeuroImage.