Mindfulness meditation training alters cortical representations of interoceptive attention.

One component of mindfulness training (MT) is the development of interoceptive attention (IA) to visceral bodily sensations, facilitated through daily practices such as breath monitoring. Using functional magnetic resonance imaging (fMRI), we examined experience-dependent functional plasticity in accessing interoceptive representations by comparing graduates of a Mindfulness-Based Stress Reduction course to a waitlisted control group. IA to respiratory sensations was contrasted against two visual tasks, controlling for attentional requirements non-specific to IA such as maintaining sensation and suppressing distraction. In anatomically partitioned analyses of insula activity, MT predicted greater IA-related activity in anterior dysgranular insula regions, consistent with greater integration of interoceptive sensation with external context. MT also predicted decreased recruitment of the dorsomedial prefrontal cortex (DMPFC) during IA, and altered functional connectivity between the DMPFC and the posterior insula, putative primary interoceptive cortex. Furthermore, meditation practice compliance predicted greater posterior insula and reduced visual pathway recruitment during IA. These findings suggest that interoceptive training modulates task-specific cortical recruitment, analogous to training-related plasticity observed in the external senses. Further, DMPFC modulation of IA networks may be an important mechanism by which MT alters information processing in the brain, increasing the contribution of interoception to perceptual experience.

[1]  HighWire Press Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

[2]  E. Gibson,et al.  Improvement in perceptual judgments as a function of controlled practice or training. , 1953, Psychological bulletin.

[3]  N. Anderson Likableness ratings of 555 personality-trait words. , 1968, Journal of personality and social psychology.

[4]  J. Brener,et al.  Interoceptive discrimination in intact humans: detection of cardiac activity. , 1974, Physiology & behavior.

[5]  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.

[6]  M. Mesulam,et al.  Insula of the old world monkey. Architectonics in the insulo‐orbito‐temporal component of the paralimbic brain , 1982, The Journal of comparative neurology.

[7]  J. Kaas The organization of neocortex in mammals: implications for theories of brain function. , 1987, Annual review of psychology.

[8]  E. Gibson Exploratory behavior in the development of perceiving, acting, and the acquiring of knowledge. , 1988 .

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

[10]  J. Mazziotta,et al.  Caudate glucose metabolic rate changes with both drug and behavior therapy for obsessive-compulsive disorder. , 1992, Archives of general psychiatry.

[11]  R. K. Wallace,et al.  The physiology of meditation: A review. A wakeful hypometabolic integrated response , 1992, Neuroscience & Biobehavioral Reviews.

[12]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[13]  J. Price,et al.  Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys , 1995, The Journal of comparative neurology.

[14]  R. Hari,et al.  Visual awareness of objects correlates with activity of right occipital cortex , 1996, Neuroreport.

[15]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[16]  Suzanne N. Haber,et al.  Insular Cortical Projections to Functional Regions of the Striatum Correlate with Cortical Cytoarchitectonic Organization in the Primate , 1997, The Journal of Neuroscience.

[17]  D. Le Bihan,et al.  fMRI Study of Taste Cortical Areas in Humans , 1998, Annals of the New York Academy of Sciences.

[18]  Alvaro Pascual-Leone,et al.  Cortical plasticity associated with Braille learning , 1998, Trends in Cognitive Sciences.

[19]  M Corbetta,et al.  Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[20]  F. Flynn,et al.  Anatomy of the insula functional and clinical correlates , 1999 .

[21]  E. Deci,et al.  Self-determination theory and the facilitation of intrinsic motivation, social development, and well-being. , 2000, The American psychologist.

[22]  A. Damasio,et al.  Subcortical and cortical brain activity during the feeling of self-generated emotions , 2000, Nature Neuroscience.

[23]  M Liotti,et al.  Brain responses associated with consciousness of breathlessness (air hunger). , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[24]  T Wüstenberg,et al.  Short-term functional plasticity in the human auditory cortex: an fMRI study. , 2001, Brain research. Cognitive brain research.

[25]  J. Desmond,et al.  Prefrontal regions involved in keeping information in and out of mind. , 2001, Brain : a journal of neurology.

[26]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

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

[28]  J. O'Doherty,et al.  Appetitive and Aversive Olfactory Learning in Humans Studied Using Event-Related Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[29]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[30]  Christoph Braun,et al.  Behavioral significance of input-dependent plasticity of human somatosensory cortex , 2003, Neuroreport.

[31]  F. Bermpohl,et al.  Cortical midline structures and the self , 2004, Trends in Cognitive Sciences.

[32]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[33]  Marc A Heiser,et al.  Associative learning shapes the neural code for stimulus magnitude in primary auditory cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Rajesh Kumar,et al.  A method for removal of global effects from fMRI time series , 2004, NeuroImage.

[35]  H. Critchley Neural mechanisms of autonomic, affective, and cognitive integration , 2005, The Journal of comparative neurology.

[36]  Lisa R. Betts,et al.  Distributed Neural Plasticity for Shape Learning in the Human Visual Cortex , 2005, PLoS biology.

[37]  J. Nagode,et al.  Double Dissociation of Exteroceptive and Interoceptive Feedback Systems in the Orbital and Ventromedial Prefrontal Cortex of Humans , 2005, The Journal of Neuroscience.

[38]  Karl J. Friston,et al.  Voxel-based morphometry of the human brain: Methods and applications , 2005 .

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

[40]  M. Paulus,et al.  An Insular View of Anxiety , 2006, Biological Psychiatry.

[41]  Michael M Merzenich,et al.  Perceptual Learning Directs Auditory Cortical Map Reorganization through Top-Down Influences , 2006, The Journal of Neuroscience.

[42]  Peter A. Bandettini,et al.  Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI , 2006, NeuroImage.

[43]  Gregory T. Smith,et al.  Using Self-Report Assessment Methods to Explore Facets of Mindfulness , 2006, Assessment.

[44]  R. Ryan,et al.  Mindfulness: Theoretical Foundations and Evidence for its Salutary Effects , 2007 .

[45]  Biyu J. He,et al.  Breakdown of Functional Connectivity in Frontoparietal Networks Underlies Behavioral Deficits in Spatial Neglect , 2007, Neuron.

[46]  Paul A. Frewen,et al.  Letting Go: Mindfulness and Negative Automatic Thinking , 2008, Cognitive Therapy and Research.

[47]  N. Allen,et al.  The Impact of Intensive Mindfulness Training on Attentional Control, Cognitive Style, and Affect , 2008, Cognitive Therapy and Research.

[48]  Z. Segal,et al.  Relationship of posttreatment decentering and cognitive reactivity to relapse in major depression. , 2007, Journal of consulting and clinical psychology.

[49]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

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

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

[52]  Gin S Malhi,et al.  The psychological and neurophysiological concomitants of mindfulness forms of meditation , 2007, Acta Neuropsychiatrica.

[53]  J. Gallant,et al.  Attention to Stimulus Features Shifts Spectral Tuning of V4 Neurons during Natural Vision , 2008, Neuron.

[54]  T. Klingberg,et al.  Prefrontal cortex and basal ganglia control access to working memory , 2008, Nature Neuroscience.

[55]  Yuko Yotsumoto,et al.  Defining a Link between Perceptual Learning and Attention , 2008, PLoS biology.

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

[57]  Justin L. Vincent,et al.  Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[58]  M. Carrasco,et al.  How spatial and feature-based attention affect the gain and tuning of population responses , 2009, Vision Research.

[59]  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.

[60]  Antoine Bechara,et al.  The hidden island of addiction: the insula , 2009, Trends in Neurosciences.

[61]  A. Schulze-Bonhage,et al.  Functional organization of the human anterior insular cortex , 2009, Neuroscience Letters.

[62]  Scott A. Huettel,et al.  Neural Substrates of Contingency Learning and Executive Control: Dissociating Physical, Valuative, and Behavioral Changes , 2009, Front. Hum. Neurosci..

[63]  H. Critchley,et al.  A common role of insula in feelings, empathy and uncertainty , 2009, Trends in Cognitive Sciences.

[64]  P Dupont,et al.  Cortical deactivations during gastric fundus distension in health: visceral pain‐specific response or attenuation of ‘default mode’ brain function? A H215O‐PET study , 2009, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[65]  A. Craig,et al.  Emotional moments across time: a possible neural basis for time perception in the anterior insula , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[66]  J. Carmody,et al.  An empirical study of the mechanisms of mindfulness in a mindfulness-based stress reduction program. , 2009, Journal of clinical psychology.

[67]  N. Farb,et al.  Minding one's emotions: mindfulness training alters the neural expression of sadness. , 2010, Emotion.

[68]  Takeo Watanabe,et al.  Advances in visual perceptual learning and plasticity , 2010, Nature Reviews Neuroscience.

[69]  N. Farb,et al.  "Minding one's emotions: Mindfulness training alters the neural expression of sadness": Correction to Farb et al (2010). , 2010 .

[70]  E. Watkins,et al.  Negative affect and ruminative self-focus during everyday goal pursuit , 2009, Cognition & emotion.

[71]  G. Finnerty,et al.  Sensory Experience and Cortical Rewiring , 2010, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[72]  B. Fredrickson,et al.  Positive Reappraisal Mediates the Stress-Reductive Effects of Mindfulness: An Upward Spiral Process , 2011 .

[73]  J. Joormann,et al.  Affective Processing and Emotion Regulation in Dysphoria and Depression: Cognitive Biases and Deficits in Cognitive Control , 2011 .

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

[75]  A. Maslow A Theory of Human Motivation , 1943 .

[76]  N. Farb,et al.  Attentional modulation of primary interoceptive and exteroceptive cortices. , 2013, Cerebral cortex.