MEG Microstates: An Investigation of Underlying Brain Sources and Potential Neurophysiological Processes.

Magnetoencephalography Mismatch negativity Occipital alpha activity Resting-state microstates Source-reconstructed brain activation

Journal

Brain topography
ISSN: 1573-6792
Titre abrégé: Brain Topogr
Pays: United States
ID NLM: 8903034

Informations de publication

Date de publication:
08 Aug 2024
Historique:
received: 19 03 2024
accepted: 22 07 2024
medline: 8 8 2024
pubmed: 8 8 2024
entrez: 8 8 2024
Statut: aheadofprint

Résumé

Microstates are transient scalp configurations of brain activity measured by electroencephalography (EEG). The application of microstate analysis in magnetoencephalography (MEG) data remains challenging. In one MEG dataset (N = 113), we aimed to identify MEG microstates at rest, explore their brain sources, and relate them to changes in brain activity during open-eyes (ROE) or closed-eyes resting state (RCE) and an auditory Mismatch Negativity (MMN) task. In another dataset of simultaneously recorded EEG-MEG data (N = 21), we investigated the association between MEG and EEG microstates. Six MEG microstates (mMS) provided the best clustering of resting-state activity, each linked to different brain sources: mMS 1-2: left/right occipito-parietal; mMS 3: fronto-temporal; mMS 4: centro-medial; mMS 5-6: left/right fronto-parietal. Increases in occipital alpha power in RCE relative to ROE correlated with greater mMS 1-2 time coverage (τ

Identifiants

pubmed: 39115626
doi: 10.1007/s10548-024-01073-z
pii: 10.1007/s10548-024-01073-z
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Adrian ED, Mathews BHC (1934) The Berger rhythm: potential changes from the occipital lobe in man. Brain 57:355–385. https://doi.org/10.1093/brain/awp324
doi: 10.1093/brain/awp324
Antonova E, Holding M, Suen HC, Sumich A, Maex R, Nehaniv C (2022) EEG microstates: functional significance and short-term test-retest reliability. Neuroimage: Rep 2(2):100089. https://doi.org/10.1016/j.ynirp.2022.100089
doi: 10.1016/j.ynirp.2022.100089
Berger H (1929) Ueber das Elektroenzephalogramm des Menschen. Archives Psychiatry 87:527–570. https://doi.org/10.1007/BF01797193
doi: 10.1007/BF01797193
Biswal B, Zerrin Yetkin F, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34(4):537–541. https://doi.org/10.1002/mrm.1910340409
doi: 10.1002/mrm.1910340409 pubmed: 8524021
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. https://doi.org/10.1016/j.neuroimage.2019.03.029
doi: 10.1016/j.neuroimage.2019.03.029 pubmed: 30902640
Britz J, Van De Ville D, Michel CM (2010) BOLD correlates of EEG topography reveal rapid resting-state network dynamics. NeuroImage 52(4):1162–1170. https://doi.org/10.1016/j.neuroimage.2010.02.052
doi: 10.1016/j.neuroimage.2010.02.052 pubmed: 20188188
Brunet D, Murray MM, Michel CM (2011) Spatiotemporal analysis of multichannel EEG: CARTOOL. Comput Intell Neurosci 2011:1–15. https://doi.org/10.1155/2011/813870
Coquelet N, De Tiège X, Roshchupkina L, Peigneux P, Goldman S, Woolrich M, Wens V (2022) Microstates and power envelope hidden Markov modeling probe bursting brain activity at different timescales. NeuroImage 247:118850. https://doi.org/10.1016/j.neuroimage.2021.118850
doi: 10.1016/j.neuroimage.2021.118850 pubmed: 34954027
Corsi M-C (2023) Electroencephalography and Magnetoencephalography. In: Colliot O (ed) Machine learning for brain disorders. Humana, Totowa (New Jersey), pp 285–312
doi: 10.1007/978-1-0716-3195-9_9
Croce P, Quercia A, Costa S, Zappasodi F (2020) EEG microstates associated with intra-and inter-subject alpha variability. Sci Rep 10(1):2469. https://doi.org/10.1038/s41598-020-58787-w
doi: 10.1038/s41598-020-58787-w pubmed: 32051420 pmcid: 7015936
Cui R, Jiang J, Zeng L, Jiang L, Xia Z, Dong L, Yao D (2021) Action video gaming experience related to altered resting-state EEG temporal and spatial complexity. Front Hum Neurosci 15:640329. https://doi.org/10.3389/fnhum.2021.640329
doi: 10.3389/fnhum.2021.640329 pubmed: 34267631 pmcid: 8275975
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(10):671–682. https://doi.org/10.1089/brain.2016.0476
doi: 10.1089/brain.2016.0476 pubmed: 28938855 pmcid: 5736178
Deco G, Jirsa VK, McIntosh AR (2011) Emerging concepts for the dynamical organization of resting-state activity in the brain. Nat Rev Neurosci 12(1):43–56. https://doi.org/10.1038/nrn2961
doi: 10.1038/nrn2961 pubmed: 21170073
Destrieux C, Fischl B, Dale A, Halgren E (2010) Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. NeuroImage 53(1):1–15. https://doi.org/10.1016/j.neuroimage.2010.06.010
doi: 10.1016/j.neuroimage.2010.06.010 pubmed: 20547229
Diaz BA, Van Der Sluis S, Moens S, Benjamins JS, Migliorati F, Stoffers D, Linkenkaer-Hansen K (2013) The amsterdam resting-state questionnaire reveals multiple phenotypes of resting-state cognition. Front Hum Neurosci 7:446. https://doi.org/10.3389/fnhum.2013.00446
doi: 10.3389/fnhum.2013.00446 pubmed: 23964225 pmcid: 3737475
Diaz BA, Van Der Sluis S, Benjamins JS, Stoffers D, Hardstone R, Mansvelder HD, Linkenkaer-Hansen K (2014) The ARSQ 2.0 reveals age and personality effects on mind-wandering experiences. Front Psychol 5:271. https://doi.org/10.3389/fpsyg.2014.00271
doi: 10.3389/fpsyg.2014.00271 pubmed: 24772097 pmcid: 3982068
First MB, Skodol AE, Bender DS, Oldham JM (2017) User’s guide for the Structured Clinical Interview for the DSM-5
Garcés P, López-Sanz D, Maestú F, Pereda E (2017) Choice of magnetometers and gradiometers after signal space separation. Sensors 17(12):2926. https://doi.org/10.3390/s17122926
doi: 10.3390/s17122926 pubmed: 29258189 pmcid: 5751446
Hedrich T, Pellegrino G, Kobayashi E, Lina JM, Grova C (2017) Comparison of the spatial resolution of source imaging techniques in high-density EEG and MEG. NeuroImage 157:531–544. https://doi.org/10.1016/j.neuroimage.2017.06.022
doi: 10.1016/j.neuroimage.2017.06.022 pubmed: 28619655
Hohaia W, Saurels BW, Johnston A, Yarrow K, Arnold DH (2022) Occipital alpha-band brain waves when the eyes are closed are shaped by ongoing visual processes. Sci Rep 12(1):1194. https://doi.org/10.1038/s41598-022-05289-6
doi: 10.1038/s41598-022-05289-6 pubmed: 35075196 pmcid: 8786963
Jabès A, Klencklen G, Ruggeri P, Michel CM, Lavenex B, P., Lavenex P (2021) Resting-state EEG microstates parallel age‐related differences in allocentric spatial working memory performance. Brain Topogr 34:442–460. https://doi.org/10.1007/s10548-021-00835-3
doi: 10.1007/s10548-021-00835-3 pubmed: 33871737 pmcid: 8195770
Jawinski P, Markett S, Sander C, Huang J, Ulke C, Hegerl U, Hensch T (2021) The big five personality traits and brain arousal in the resting state. Brain Sci 11(10):1272. https://doi.org/10.3390/brainsci11101272
doi: 10.3390/brainsci11101272 pubmed: 34679337 pmcid: 8533901
Ke M, Li J, Wang L (2021) Alteration in resting-state EEG microstates following 24 hours of total sleep deprivation in healthy young male subjects. Front Hum Neurosci 15:636252. https://doi.org/10.3389/fnhum.2021.636252
doi: 10.3389/fnhum.2021.636252 pubmed: 33912019 pmcid: 8075097
Khanna A, Pascual-Leone A, Michel CM, Farzan F (2015) Microstates in resting-state EEG: current status and future directions. Neurosci Biobehavioral Reviews 49:105–113. https://doi.org/10.1016/j.neubiorev.2014.12.010
doi: 10.1016/j.neubiorev.2014.12.010
Korn U, Krylova M, Heck KL, Häußinger FB, Stark RS, Alizadeh S, Munk MH (2021) EEG-Microstates reflect auditory distraction after attentive audiovisual perception recruitment of cognitive control networks. Front Syst Neurosci 15:751226. https://doi.org/10.3389/fnsys.2021.751226
doi: 10.3389/fnsys.2021.751226 pubmed: 34955767 pmcid: 8696261
Mazziotta J, Toga A, Evans A, Fox P, Lancaster J, Zilles K, Mazoyer B (2001) A probabilistic atlas and reference system for the human brain: international consortium for brain mapping (ICBM). Philosophical Trans Royal Soc Lond Ser B: Biol Sci 356(1412):1293–1322. https://doi.org/10.1098/rstb.2001.0915
doi: 10.1098/rstb.2001.0915
Michel CM, Brunet D (2019) EEG source imaging: a practical review of the analysis steps. Front Neurol 10:325. https://doi.org/10.3389/fneur.2019.00325
doi: 10.3389/fneur.2019.00325 pubmed: 31019487 pmcid: 6458265
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. https://doi.org/10.1016/j.neuroimage.2017.11.062
doi: 10.1016/j.neuroimage.2017.11.062 pubmed: 29196270
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. https://doi.org/10.1016/j.neuroimage.2015.08.023
doi: 10.1016/j.neuroimage.2015.08.023 pubmed: 26285079
Näätänen R, Paavilainen P, Rinne T, Alho K (2007) The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clin Neurophysiol 118(12):2544–2590. https://doi.org/10.1016/j.clinph.2007.04.026
doi: 10.1016/j.clinph.2007.04.026 pubmed: 17931964
Oostenveld R, Fries P, Maris E, Schoffelen JM (2011) FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:1–9. https://doi.org/10.1155/2011/156869
Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24(Suppl D):5–12
pubmed: 12575463
Pascual-Marqui RD, Lehmann D, Faber P, Milz P, Kochi K, Yoshimura M, Kinoshita T (2014) The resting microstate networks (RMN): cortical distributions, dynamics, and frequency specific information flow. arXiv preprint arXiv:1411.1949
Schaefer A, Kong R, Gordon EM, Laumann TO, Zuo XN, Holmes AJ, Yeo BT (2018) Local-global parcellation of the human cerebral cortex from intrinsic functional connectivity MRI. Cereb Cortex 28(9):3095–3114. https://doi.org/10.1093/cercor/bhx179
doi: 10.1093/cercor/bhx179 pubmed: 28981612
Seitzman BA, Abell M, Bartley SC, Erickson MA, Bolbecker AR, Hetrick WP (2017) Cognitive manipulation of brain electric microstates. NeuroImage 146:533–543. https://doi.org/10.1016/j.neuroimage.2016.10.002
doi: 10.1016/j.neuroimage.2016.10.002 pubmed: 27742598
Seitzman BA, Snyder AZ, Leuthardt EC, Shimony JS (2019) The state of resting state networks. Top Magn Reson Imaging: TMRI 28(4):189. https://doi.org/10.1097/rmr.0000000000000214
doi: 10.1097/rmr.0000000000000214 pubmed: 31385898
Singh SP (2014) Magnetoencephalography: basic principles. Ann Indian Acad Neurol 17(Suppl 1):S107–S112. https://doi.org/10.4103/0972-2327.128676
doi: 10.4103/0972-2327.128676 pubmed: 24791076 pmcid: 4001219
Tadel F, Baillet S, Mosher JC, Pantazis D, Leahy RM (2011) Brainstorm: a user-friendly application for MEG/EEG analysis. Comput Intell Neurosci 2011:1–13. https://doi.org/10.1155/2011/879716
Tait L, Zhang J (2022) MEG cortical microstates: spatiotemporal characteristics, dynamic functional connectivity and stimulus-evoked responses. NeuroImage 251:119006. https://doi.org/10.1016/j.neuroimage.2022.119006
doi: 10.1016/j.neuroimage.2022.119006 pubmed: 35181551
Tarailis P, Šimkutė D, Koenig T, Griškova-Bulanova I (2021) Relationship between spatiotemporal dynamics of the brain at rest and self-reported spontaneous thoughts: an EEG microstate approach. J Personalized Med 11(11):1216. https://doi.org/10.3390/jpm11111216
doi: 10.3390/jpm11111216
Tarailis P, Koenig T, Michel CM, Griškova-Bulanova I (2024) The functional aspects of resting EEG microstates: a systematic review. Brain Topogr 37(2):181–217. https://doi.org/10.1007/s10548-023-00958-9
Taulu S, Simola J (2006) Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements. Phys Med Biol 51(7):1759. https://doi.org/10.1088/0031-9155/51/7/008
doi: 10.1088/0031-9155/51/7/008 pubmed: 16552102
Tomescu MI, Rihs TA, Rochas V, Hardmeier M, Britz J, Allali G, Michel CM (2018) From swing to cane: sex differences of EEG resting-state temporal patterns during maturation and aging. Dev Cogn Neurosci 31:58–66. https://doi.org/10.1016/j.dcn.2018.04.011
doi: 10.1016/j.dcn.2018.04.011 pubmed: 29742488 pmcid: 6969216
Valt C, Quarto T, Tavella A, Romanelli F, Fazio L, Arcara G, Bertolino A (2023) Reduced magnetic mismatch negativity: a shared deficit in psychosis and related risk. Psychol Med 53(13):6037–6045. https://doi.org/10.1017/s003329172200321x
doi: 10.1017/s003329172200321x pubmed: 36321391
Vrba J, Robinson SE (2001) Signal Processing in Magnetoencephalography. Methods 25(2):249–271. https://doi.org/10.1006/METH.2001.1238
doi: 10.1006/METH.2001.1238 pubmed: 11812209
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. https://doi.org/10.1016/j.neuroimage.2020.116631
doi: 10.1016/j.neuroimage.2020.116631 pubmed: 32062082
Zappasodi F, Perrucci MG, Saggino A, Croce P, Mercuri P, Romanelli R, Ebisch SJ (2019) EEG microstates distinguish between cognitive components of fluid reasoning. NeuroImage 189:560–573. https://doi.org/10.1016/j.neuroimage.2019.01.067
doi: 10.1016/j.neuroimage.2019.01.067 pubmed: 30710677

Auteurs

Christian Valt (C)

Department of Translational Biomedicine and Neuroscience, University of Bari Aldo Moro, Bari, Italy. christian.valt@uniba.it.

Angelantonio Tavella (A)

Department of Translational Biomedicine and Neuroscience, University of Bari Aldo Moro, Bari, Italy.
Department of Mental Health, ASL Bari, Bari, Italy.

Cristina Berchio (C)

Department of Translational Biomedicine and Neuroscience, University of Bari Aldo Moro, Bari, Italy.

Dylan Seebold (D)

Clinical Neurophysiology Research Laboratory, Western Psychiatric Hospital, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

Leonardo Sportelli (L)

Department of Translational Biomedicine and Neuroscience, University of Bari Aldo Moro, Bari, Italy.
Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, USA.

Antonio Rampino (A)

Department of Translational Biomedicine and Neuroscience, University of Bari Aldo Moro, Bari, Italy.
Psychiatric Unit, Bari University Hospital, Bari, Italy.

Dean F Salisbury (DF)

Clinical Neurophysiology Research Laboratory, Western Psychiatric Hospital, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

Alessandro Bertolino (A)

Department of Translational Biomedicine and Neuroscience, University of Bari Aldo Moro, Bari, Italy.
Psychiatric Unit, Bari University Hospital, Bari, Italy.

Giulio Pergola (G)

Department of Translational Biomedicine and Neuroscience, University of Bari Aldo Moro, Bari, Italy. giulio.pergola@uniba.it.
Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, USA. giulio.pergola@uniba.it.
Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, MD, USA. giulio.pergola@uniba.it.

Classifications MeSH