Research Article
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Published Online: 15 March 2021

Reconfiguration of Electroencephalography Microstate Networks after Breath-Focused, Digital Meditation Training

Publication: Brain Connectivity
Volume 11, Issue Number 2

Abstract

Sustained attention and working memory were improved in young adults after they engaged in a recently developed, closed-loop, digital meditation practice. Whether this type of meditation also has a sustained effect on dominant resting-state networks is currently unknown. In this study, we examined the resting brain states before and after a period of breath-focused, digital meditation training versus placebo using an electroencephalography (EEG) microstate approach. We found topographical changes in postmeditation rest, compared with baseline rest, selectively for participants who were actively involved in the meditation training and not in participants who engaged with an active, expectancy-match, placebo control paradigm. Our results suggest a reorganization of brain network connectivity after 6 weeks of intensive meditation training in brain areas, mainly including the right insula, the superior temporal gyrus, the superior parietal lobule, and the superior frontal gyrus bilaterally. These findings provide an opening for the development of a novel noninvasive treatment of neuropathological states by low-cost, breath-focused, digital meditation practice, which can be monitored by the EEG microstate approach.

Abstract

Impact statement

Breath-focused, digital meditation training leads to sustained changes of resting-state, brain network functional connectivity, as assessed with electroencephalography microstates.

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References

Alzahabi R, Becker MW. 2013. The association between media multitasking, task-switching, and dual-task performance. J Exp Psychol Hum Percept Perform 39:1485–1495.
Bassett DS, Sporns O. 2017. Network neuroscience. Nat Neurosci 20:353–364.
Birot G, Spinelli L, Vulliemoz S, Megevand P, Brunet D, Seeck M, Michel CM. 2014. Head model and electrical source imaging: a study of 38 epileptic patients. Neuroimage Clin 5:77–83.
Biswal B, Yetkin FZ, Haughton VM, Hyde JS. 1995. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541.
Blanke O. 2012. Multisensory brain mechanisms of bodily self-consciousness. Nat Rev Neurosci 13:556–571.
Blanke O, Slater M, Serino A. 2015. Behavioral, neural, and computational principles of bodily self-consciousness. Neuron 88:145–166.
Bréchet L, Brunet D, Birot G, Gruetter R, Michel CM, Jorge J. 2019. Capturing the spatiotemporal dynamics of self-generated, task-initiated thoughts with EEG and fMRI. Neuroimage 194:82–92.
Bréchet L, Brunet D, Perogamvros L, Tononi G, Michel CM. 2020a. EEG microstates of dreams. Sci Rep 10:17069.
Bréchet L, Grivaz P, Gauthier B, Blanke O. 2018. Common recruitment of angular gyrus in episodic autobiographical memory and bodily self-consciousness. Front Behav Neurosci 12:270.
Bréchet L, Hausmann SB, Mange R, Herbelin B, Blanke O, Serino A. 2020b. Subjective feeling of re-experiencing past events using immersive virtual reality prevents a loss of episodic memory. Brain Behav 10:e01571.
Brechet L, Mange R, Herbelin B, Theillaud Q, Gauthier B, Serino A, Blanke O. 2019. First-person view of one's body in immersive virtual reality: influence on episodic memory. PLoS One 14:e0197763.
Britz J, Van De Ville D, Michel CM. 2010. BOLD correlates of EEG topography reveal rapid resting-state network dynamics. Neuroimage 52:1162–1170.
Brodbeck V, Kuhn A, von Wegner F, Morzelewski A, Tagliazucchi E, Borisov S, et al. 2012. EEG microstates of wakefulness and NREM sleep. Neuroimage 62:2129–2139.
Brunet D, Murray MM, Michel CM. 2011. Spatiotemporal analysis of multichannel EEG: CARTOOL. Comput Intell Neurosci 2011:813870.
Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ. 2004. Neural systems supporting interoceptive awareness. Nat Neurosci 7:189–195.
Croce P, Zappasodi F, Capotosto P. 2018a. Offline stimulation of human parietal cortex differently affects resting EEG microstates. Sci Rep 8:1287.
Croce P, Zappasodi F, Spadone S, Capotosto P. 2018b. Magnetic stimulation selectively affects pre-stimulus EEG microstates. Neuroimage 176:239–245.
Custo A, Van De Ville D, Wells WM, Tomescu MI, Brunet D, Michel CM. 2017. Electroencephalographic resting-state networks: source localization of microstates. Brain Connect 7:671–682.
D'Croz-Baron DF, Baker M, Michel CM, Karp T. 2019. EEG microstates analysis in young adults with autism spectrum disorder during resting-state. Front Hum Neurosci 13:173.
da Cruz JR, Favrod O, Roinishvili M, Chkonia E, Brand A, Mohr C, et al. 2020. EEG microstates are a candidate endophenotype for schizophrenia. Nat Commun 11:3089.
Devue C, Collette F, Balteau E, Degueldre C, Luxen A, Maquet P, Brédart S. 2007. Here I am: the cortical correlates of visual self-recognition. Brain Res 1143:169–182.
Enzi B, de Greck M, Prosch U, Tempelmann C, Northoff G. 2009. Is our self nothing but reward? Neuronal overlap and distinction between reward and personal relevance and its relation to human personality. PLoS One 4:e8429.
Faber PL, Travis F, Milz P, Parim N. 2017. EEG microstates during different phases of Transcendental Meditation practice. Cogn Process 18:307–314.
Farb NA, Segal ZV, Mayberg H, Bean J, McKeon D, Fatima Z, Anderson AK. 2007. Attending to the present: mindfulness meditation reveals distinct neural modes of self-reference. Soc Cogn Affect Neurosci 2:313–322.
Friston KJ, Holmes AP, Price CJ, Buchel C, Worsley KJ. 1999. Multisubject fMRI studies and conjunction analyses. Neuroimage 10:385–396.
Gazzaley A, Rosen LD. 2016. The Distracted Mind: Ancient Brains in a High-Tech World. Cambridge, MA, USA: The MIT Press.
Grave de Peralta Menendez R, Murray MM, Michel CM, Martuzzi R, Gonzalez Andino SL. 2004. Electrical neuroimaging based on biophysical constraints. Neuroimage 21:527–539.
Grieder M, Koenig T, Kinoshita T, Utsunomiya K, Wahlund LO, Dierks T, Nishida K. 2016. Discovering EEG resting state alterations of semantic dementia. Clin Neurophysiol 127:2175–2181.
Grivaz P, Blanke O, Serino A. 2017. Common and distinct brain regions processing multisensory bodily signals for peripersonal space and body ownership. Neuroimage 147:602–618.
Gschwind M, Hardmeier M, Van De Ville D, Tomescu MI, Penner IK, Naegelin Y, et al. 2016. Fluctuations of spontaneous EEG topographies predict disease state in relapsing-remitting multiple sclerosis. Neuroimage Clin 12:466–477.
Holzel BK, Ott U, Gard T, Hempel H, Weygandt M, Morgen K, Vaitl D. 2008. Investigation of mindfulness meditation practitioners with voxel-based morphometry. Soc Cogn Affect Neurosci 3:55–61.
Ionta S, Heydrich L, Lenggenhager B, Mouthon M, Fornari E, Chapuis D, et al. 2011. Multisensory mechanisms in temporo-parietal cortex support self-location and first-person perspective. Neuron 70:363–374.
Johnstone T, van Reekum CM, Oakes TR, Davidson RJ. 2006. The voice of emotion: an FMRI study of neural responses to angry and happy vocal expressions. Soc Cogn Affect Neurosci 1:242–249.
Katayama H, Gianotti LR, Isotani T, Faber PL, Sasada K, Kinoshita T, Lehmann D. 2007. Classes of multichannel EEG microstates in light and deep hypnotic conditions. Brain Topogr 20:7–14.
Kerr CE, Sacchet MD, Lazar SW, Moore CI, Jones SR. 2013. Mindfulness starts with the body: somatosensory attention and top-down modulation of cortical alpha rhythms in mindfulness meditation. Front Hum Neurosci 7:12.
Khanna A, Pascual-Leone A, Farzan F. 2014. Reliability of resting-state microstate features in electroencephalography. PLoS One 9:e114163.
Koenig T, Prichep L, Lehmann D, Sosa PV, Braeker E, Kleinlogel H, et al. 2002. Millisecond by millisecond, year by year: normative EEG microstates and developmental stages. Neuroimage 16:41–48.
Koenig T, Valdes-Sosa PA. 2018. Results obtained by combining different estimators of EEG connectivity become uninterpretable if the underlying models are incompatible. Brain Connect 8:57–59.
Lehmann D, Ozaki H, Pal I. 1987. EEG alpha map series: brain micro-states by space-oriented adaptive segmentation. Electroencephalogr Clin Neurophysiol 67:271–288.
Liu J, Xu J, Zou G, He Y, Zou QH, Gao J-H. 2020. Reliability and individual specificity of EEG microstate characteristics. Brain Topogr 30:438–449.
Loh KK, Kanai R. 2016. How has the Internet reshaped human cognition? Neuroscientist 22:506–520.
Michel CM, Brunet D. 2019. EEG source imaging: a practical review of the analysis steps. Front Neurol 10:325.
Michel CM, Koenig T. 2018. EEG microstates as a tool for studying the temporal dynamics of whole-brain neuronal networks: a review. Neuroimage 180:577–593.
Michel CM, Murray MM, Lantz G, Gonzalez S, Spinelli L, Grave de Peralta R. 2004. EEG source imaging. Clin Neurophysiol 115:2195–2222.
Milz P, Faber PL, Lehmann D, Koenig T, Kochi K, Pascual-Marqui RD. 2016. The functional significance of EEG microstates—associations with modalities of thinking. Neuroimage 125:643–656.
Minear M, Brasher F, McCurdy M, Lewis J, Younggren A. 2013. Working memory, fluid intelligence, and impulsiveness in heavy media multitaskers. Psychon Bull Rev 20:1274–1281.
Mishra J, Sagar R, Parveen S, Kumaran S, Modi K, Maric V, et al. 2020. Closed-loop digital meditation for neurocognitive and behavioral development in adolescents with childhood neglect. Transl Psychiatry 10:153.
Modinos G, Ormel J, Aleman A. 2009. Activation of anterior insula during self-reflection. PLoS One 4:e4618.
Moisala M, Salmela V, Hietajarvi L, Salo E, Carlson S, Salonen O, et al. 2016. Media multitasking is associated with distractibility and increased prefrontal activity in adolescents and young adults. Neuroimage 134:113–121.
Murphy M, Stickgold R, Parr ME, Callahan C, Wamsley EJ. 2018. Recurrence of task-related electroencephalographic activity during post-training quiet rest and sleep. Sci Rep 8:5398.
Nishida K, Morishima Y, Yoshimura M, Isotani T, Irisawa S, Jann K, et al. 2013. EEG microstates associated with salience and frontoparietal networks in frontotemporal dementia, schizophrenia and Alzheimer's disease. Clin Neurophysiol 124:1106–1114.
Ophir E, Nass C, Wagner AD. 2009. Cognitive control in media multitaskers. Proc Natl Acad Sci U S A 106:15583–15587.
Panda R, Bharath RD, Upadhyay N, Mangalore S, Chennu S, Rao SL. 2016. Temporal dynamics of the default mode network characterize meditation-induced alterations in consciousness. Front Hum Neurosci 10:372.
Park HD, Blanke O. 2019. Coupling inner and outer body for self-consciousness. Trends Cogn Sci 23:377–388.
Pascual-Marqui RD, Michel CM, Lehmann D. 1995. Segmentation of brain electrical activity into microstates: model estimation and validation. IEEE Trans Biomed Eng 42:658–665.
Poskanzer C, Denis D, Herrick A, Stickgold R. 2020. Using EEG microstates to examine post-encoding quiest rest and subsequent word-pair memory. bioRxiv (preprint).
Posner MI, Petersen SE. 1990. The attention system of the human brain. Annu Rev Neurosci 13:25–42.
Rideout VJ, Foehr UG, Roberts DF. 2010. Generation M2: Media in the Lives of 8- to 18-Year-Olds. Menlo Park, CA: The Henry J. Kaiser Family Foundation.
Rieger K, Diaz Hernandez L, Baenninger A, Koenig T. 2016. 15 years of microstate research in Schizophrenia - where are we? A meta-analysis. Front Psychiatry 7:22.
Seitzman BA, Abell M, Bartley SC, Erickson MA, Bolbecker AR, Hetrick WP. 2017. Cognitive manipulation of brain electric microstates. Neuroimage 146:533–543.
Sestieri C, Tosoni A, Mignogna V, McAvoy MP, Shulman GL, Corbetta M, Luca Romani G. 2014. Memory accumulation mechanisms in human cortex are independent of motor intentions. J Neurosci 34:6993–7006.
Shi W, Li Y, Liu Z, Li J, Wang Q, Yan X, Wang G. 2020. Non-canonical microstate becomes salient in high density EEG during propofol-induced altered states of consciousness. Int J Neural Syst 30:2050005.
Smallwood J, Andrews-Hanna J. 2013. Not all minds that wander are lost: the importance of a balanced perspective on the mind-wandering state. Front Psychol 4:441.
Stefan S, Schorr B, Lopez-Rolon A, Kolassa IT, Shock JP, Rosenfelder M, et al. 2018. Consciousness indexing and outcome prediction with resting-state EEG in severe disorders of consciousness. Brain Topogr 31:848–862.
Tomescu MI, Rihs TA, Rochas V, Hardmeier M, Britz J, Allali G, et al. 2018. From swing to cane: sex differences of EEG resting-state temporal patterns during maturation and aging. Dev Cogn Neurosci 31:58–66.
Vago DR, Silbersweig DA. 2012. Self-awareness, self-regulation, and self-transcendence (S-ART): a framework for understanding the neurobiological mechanisms of mindfulness. Front Hum Neurosci 6:296.
Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ, Bruno MA, Boveroux P, Schnakers C, et al. 2010. Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain 133:161–171.
Whitfield-Gabrieli S, Ford JM. 2012. Default mode network activity and connectivity in psychopathology. Annu Rev Clin Psychol 8:49–76.
Yap JY, Wee Hun Lim S. 2013. Media multitasking predicts unitary versus splitting visual focal attention. J Cogn Psychol 25:889–902.
Zanesco AP, King BG, Skwara AC, Saron CD. 2020. Within and between-person correlates of the temporal dynamics of resting EEG microstates. Neuroimage 211:116631.
Zappasodi F, Croce P, Giordani A, Assenza G, Giannantoni NM, Profice P, et al. 2017. Prognostic value of EEG microstates in acute stroke. Brain Topogr 30:698–710.
Ziegler DA, Simon AJ, Gallen CL, Skinner S, Janowich JR, Volponi JJ, et al. 2019. Closed-loop digital meditation improves sustained attention in young adults. Nat Hum Behav 3:746–757.

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Published In

cover image Brain Connectivity
Brain Connectivity
Volume 11Issue Number 2March 2021
Pages: 146 - 155
PubMed: 33403921

History

Published online: 15 March 2021
Published in print: March 2021
Published ahead of print: 9 February 2021
Published ahead of production: 6 January 2021

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Authors

Affiliations

Lucie Bréchet [email protected]
Functional Brain Mapping Laboratory, Department of Fundamental Neuroscience, University of Geneva, Geneva, Switzerland.
Center for Biomedical Imaging (CIBM), Lausanne, Switzerland.
David A. Ziegler
Department of Neurology, University of California San Francisco, San Francisco, California, USA.
Neuroscape, University of California San Francisco, San Francisco, California, USA.
Weill Institute for Neurosciences and Kavli Institute for Fundamental Neuroscience, University of California San Francisco, San Francisco, California, USA.
Alexander J. Simon
Department of Neurology, University of California San Francisco, San Francisco, California, USA.
Neuroscape, University of California San Francisco, San Francisco, California, USA.
Weill Institute for Neurosciences and Kavli Institute for Fundamental Neuroscience, University of California San Francisco, San Francisco, California, USA.
Denis Brunet
Functional Brain Mapping Laboratory, Department of Fundamental Neuroscience, University of Geneva, Geneva, Switzerland.
Center for Biomedical Imaging (CIBM), Lausanne, Switzerland.
Adam Gazzaley
Department of Neurology, University of California San Francisco, San Francisco, California, USA.
Department of Psychiatry, University of California San Francisco, San Francisco, California, USA.
Department of Physiology, University of California San Francisco, San Francisco, California, USA.
Neuroscape, University of California San Francisco, San Francisco, California, USA.
Weill Institute for Neurosciences and Kavli Institute for Fundamental Neuroscience, University of California San Francisco, San Francisco, California, USA.
Christoph M. Michel
Functional Brain Mapping Laboratory, Department of Fundamental Neuroscience, University of Geneva, Geneva, Switzerland.
Center for Biomedical Imaging (CIBM), Lausanne, Switzerland.

Notes

Address correspondence to: Lucie Bréchet, Department of Fundamental Neuroscience, University of Geneva, Campus Biotech, 9 Chemin des Mines, Geneva CH-1202, Switzerland [email protected]

Authors' Contributions

All authors contributed significantly to the work. D.A.Z. and A.J.S. collected the data and preprocessed the EEG. D.A.Z. and A.G. designed and supervised the experiment and the data collection. L.B., D.B., and C.M.M. analyzed the data. L.B. and C.M.M. wrote the manuscript. D.A.Z. and A.G. corrected the manuscript.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

The NIH, grants R21 AG041071 and R01 AG049424, provided financial support for the collection of data reported in this study. The data analysis was supported by the Swiss National Science Foundation, Grant No. 320030_184677 (to C.M.M.).

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