Experienced Mindfulness Meditators Exhibit Higher Parietal-Occipital EEG Gamma Activity during NREM Sleep

Over the past several years meditation practice has gained increasing attention as a non-pharmacological intervention to provide health related benefits, from promoting general wellness to alleviating the symptoms of a variety of medical conditions. However, the effects of meditation training on brain activity still need to be fully characterized. Sleep provides a unique approach to explore the meditation-related plastic changes in brain function. In this study we performed sleep high-density electroencephalographic (hdEEG) recordings in long-term meditators (LTM) of Buddhist meditation practices (approximately 8700 mean hours of life practice) and meditation naive individuals. We found that LTM had increased parietal-occipital EEG gamma power during NREM sleep. This increase was specific for the gamma range (25–40 Hz), was not related to the level of spontaneous arousal during NREM and was positively correlated with the length of lifetime daily meditation practice. Altogether, these findings indicate that meditation practice produces measurable changes in spontaneous brain activity, and suggest that EEG gamma activity during sleep represents a sensitive measure of the long-lasting, plastic effects of meditative training on brain function.

[1]  G. Tononi,et al.  Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity , 2006, Nature Neuroscience.

[2]  C. Morin,et al.  Validation of the Insomnia Severity Index as an outcome measure for insomnia research. , 2001, Sleep medicine.

[3]  Erol Başar,et al.  Brain oscillations are highly influenced by gender differences. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[4]  Ulrike Held,et al.  Validation of the fatigue severity scale in a Swiss cohort. , 2008, Sleep.

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

[6]  Peter Achermann,et al.  Individual ‘Fingerprints’ in Human Sleep EEG Topography , 2001, Neuropsychopharmacology.

[7]  G. Tononi,et al.  Source modeling sleep slow waves , 2009, Proceedings of the National Academy of Sciences.

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

[9]  G. Saayman,et al.  Meditation and archetypal content of nocturnal dreams. , 1978, The Journal of analytical psychology.

[10]  G Tononi,et al.  Cortical reactivity and effective connectivity during REM sleep in humans , 2010, Cognitive neuroscience.

[11]  A. Lutz,et al.  Mental Training Enhances Attentional Stability: Neural and Behavioral Evidence , 2009, The Journal of Neuroscience.

[12]  Christoph S. Herrmann,et al.  Early gamma-band responses reflect anticipatory top-down modulation in the auditory cortex , 2009, NeuroImage.

[13]  R. Chervin Epworth sleepiness scale? , 2003, Sleep medicine.

[14]  P. König,et al.  A Functional Gamma-Band Defined by Stimulus-Dependent Synchronization in Area 18 of Awake Behaving Cats , 2003, The Journal of Neuroscience.

[15]  S J Anderson,et al.  The role of oscillatory brain activity in object processing and figure-ground segmentation in human vision. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[16]  Marcello Massimini,et al.  Sleep homeostasis and cortical synchronization: III. A high-density EEG study of sleep slow waves in humans. , 2007, Sleep.

[17]  G. Tononi,et al.  Local sleep and learning , 2004, Nature.

[18]  J. Born,et al.  Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[19]  O. Bertrand,et al.  Neural correlates of consolidation in working memory , 2007, Human brain mapping.

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

[21]  Giulio Tononi,et al.  Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles. , 2010, The American journal of psychiatry.

[22]  B. Feige,et al.  Sleep electroencephalographic spectral power after withdrawal from alcohol in alcohol-dependent patients. , 2007, Alcoholism, clinical and experimental research.

[23]  Bruce F O'Hara,et al.  Meditation acutely improves psychomotor vigilance, and may decrease sleep need , 2010, Behavioral and Brain Functions.

[24]  H. Nittono,et al.  Comparison of the event‐related potentials between tonic and phasic periods of rapid eye movement sleep , 2002, Psychiatry and clinical neurosciences.

[25]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

[26]  Florian Holsboer,et al.  Acoustic Oddball during NREM Sleep: A Combined EEG/fMRI Study , 2009, PloS one.

[27]  M. Johns,et al.  A new method for measuring daytime sleepiness: the Epworth sleepiness scale. , 1991, Sleep.

[28]  B. Stigsby,et al.  Electroencephalographic findings during mantra meditation (transcendental meditation). A controlled, quantitative study of experienced meditators. , 1981, Electroencephalography and clinical neurophysiology.

[29]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[30]  M. Steriade The corticothalamic system in sleep. , 2003, Frontiers in bioscience : a journal and virtual library.

[31]  I Feinberg,et al.  Systematic trends across the night in human sleep cycles. , 1979, Psychophysiology.

[32]  D. Martinez,et al.  Light sleep and sleep time misperception – Relationship to alpha–delta sleep , 2010, Clinical Neurophysiology.

[33]  O. Jensen,et al.  Modulation of Gamma and Alpha Activity during a Working Memory Task Engaging the Dorsal or Ventral Stream , 2007, The Journal of Neuroscience.

[34]  Arnaud Delorme,et al.  Occipital gamma activation during Vipassana meditation , 2009, Cognitive Processing.

[35]  A. Maclean,et al.  Psychometric evaluation of the Stanford Sleepiness Scale , 1992, Journal of sleep research.

[36]  D. Giles,et al.  Beta EEG activity and insomnia. , 2001, Sleep medicine reviews.

[37]  K. Krakow,et al.  Arousal thresholds during human tonic and phasic REM sleep , 2010, Journal of sleep research.

[38]  A. Borbély,et al.  All‐night dynamics of the human sleep EEG , 1993, Journal of sleep research.

[39]  Egill Rostrup,et al.  Cortical Deactivation Induced by Visual Stimulation in Human Slow-Wave Sleep , 2002, NeuroImage.

[40]  August B. Hollingshead,et al.  Two Factor Index of Social Position , 1957 .

[41]  Andrew D. Engell,et al.  Selective Attention Modulates Face-Specific Induced Gamma Oscillations Recorded from Ventral Occipitotemporal Cortex , 2010, The Journal of Neuroscience.

[42]  B. Kutty,et al.  Meditation and Its Regulatory Role on Sleep , 2012, Front. Neur..

[43]  M. Corsi-Cabrera,et al.  Brain activity and temporal coupling related to eye movements during REM sleep: EEG and MEG results , 2008, Brain Research.

[44]  S. Nieuwenhuis,et al.  Mental Training Affects Distribution of Limited Brain Resources , 2007, PLoS biology.

[45]  M. Gold,et al.  The symptoms and signs of upper airway resistance syndrome: a link to the functional somatic syndromes. , 2003, Chest.

[46]  H. Moldofsky,et al.  Periodic movements in sleep and sleep-wake complaint. , 1985, Sleep.

[47]  G. Tononi,et al.  Reduced sleep spindle activity in schizophrenia patients. , 2007, The American journal of psychiatry.

[48]  A John Rush,et al.  High Frequency EEG Activity during Sleep: Characteristics in Schizophrenia and Depression , 2005, Clinical EEG and neuroscience.

[49]  G. Marsh,et al.  Electrophysiological correlates of higher states of consciousness during sleep in long-term practitioners of the Transcendental Meditation program. , 1997, Sleep.

[50]  J. Markowitz,et al.  The 16-Item quick inventory of depressive symptomatology (QIDS), clinician rating (QIDS-C), and self-report (QIDS-SR): a psychometric evaluation in patients with chronic major depression , 2003, Biological Psychiatry.

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

[52]  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.

[53]  G. Tononi,et al.  Non-fluent aphasia and neural reorganization after speech therapy: insights from human sleep electrophysiology and functional magnetic resonance imaging. , 2010, Archives italiennes de biologie.

[54]  R. Oostenveld,et al.  Theta and Gamma Oscillations Predict Encoding and Retrieval of Declarative Memory , 2006, The Journal of Neuroscience.

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

[56]  D. Leopold,et al.  Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: Implications for functional connectivity at rest , 2008, Human brain mapping.

[57]  G. Tononi,et al.  Electrophysiological correlates of behavioural changes in vigilance in vegetative state and minimally conscious state. , 2011, Brain : a journal of neurology.

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

[59]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[60]  Emil C. Toescu,et al.  Effect of ageing on CA3 interneuron sAHP and gamma oscillations is activity-dependent , 2011, Neurobiology of Aging.

[61]  L. Derogatis,et al.  Factorial invariance across gender for the primary symptom dimensions of the SCL-90. , 1977, The British journal of social and clinical psychology.

[62]  B. Kutty,et al.  Practitioners of vipassana meditation exhibit enhanced slow wave sleep and REM sleep states across different age groups , 2010 .

[63]  Per B Sederberg,et al.  The temporal contiguity effect predicts episodic memory performance. , 2010, Memory & cognition.

[64]  A. Lutz,et al.  Long-term meditators self-induce high-amplitude gamma synchrony during mental practice. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[65]  S. Chokroverty,et al.  The visual scoring of sleep in adults. , 2007, Journal of clinical sleep medicine : JCSM : official publication of the American Academy of Sleep Medicine.

[66]  Dominique Hasboun,et al.  Human Gamma Oscillations during Slow Wave Sleep , 2012, PloS one.

[67]  F. Travis Mindfulness and psychologic well-being: are they related to type of meditation technique practiced? , 2011, Journal of alternative and complementary medicine.

[68]  K. Miller,et al.  Direct electrophysiological measurement of human default network areas , 2009, Proceedings of the National Academy of Sciences.

[69]  Y. Dauvilliers,et al.  Response to "Idiopathic hypersomnia: a diagnostic dilemma" (J. Montplaisir and L. Fantini). , 2001, Sleep medicine reviews.

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

[71]  G. Tononi,et al.  *Both authors contributed equally to this manuscript. , 2022 .

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

[73]  G. Tononi,et al.  TMS-Induced Cortical Potentiation during Wakefulness Locally Increases Slow Wave Activity during Sleep , 2007, PloS one.

[74]  N. Jausovec,et al.  Personality, gender and brain oscillations. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[75]  Tzyy-Ping Jung,et al.  Imaging brain dynamics using independent component analysis , 2001, Proc. IEEE.