Individual slow wave events give rise to macroscopic fMRI signatures and drive the strength of the BOLD signal in human resting-state EEG-fMRI recordings.


Journal

Cerebral cortex (New York, N.Y. : 1991)
ISSN: 1460-2199
Titre abrégé: Cereb Cortex
Pays: United States
ID NLM: 9110718

Informations de publication

Date de publication:
20 10 2022
Historique:
received: 09 06 2021
revised: 08 12 2021
accepted: 09 12 2021
pubmed: 31 1 2022
medline: 4 11 2022
entrez: 30 1 2022
Statut: ppublish

Résumé

The slow wave state is a general state of quiescence interrupted by sudden bursts of activity or so-called slow wave events (SWEs). Recently, the relationship between SWEs and blood oxygen level-dependent (BOLD) functional magnetic resonance imaging (fMRI) signals was assessed in rodent models which revealed cortex-wide BOLD activation. However, it remains unclear which macroscopic signature corresponds to these specific neurophysiological events in the human brain. Therefore, we analyzed simultaneous electroencephalographic (EEG)-fMRI data during human non-REM sleep. SWEs individually detected in the EEG data were used as predictors in event-related fMRI analyses to examine the relationship between SWEs and fMRI signals. For all 10 subjects we identified significant changes in BOLD activity associated with SWEs covering substantial parts of the gray matter. As demonstrated in rodents, we observed a direct relation of a neurophysiological event to specific BOLD activation patterns. We found a correlation between the number of SWEs and the spatial extent of these BOLD activation patterns and discovered that the amplitude of the BOLD response strongly depends on the SWE amplitude. As altered SWE propagation has recently been found in neuropsychiatric diseases, it is critical to reveal the brain's physiological slow wave state networks to potentially establish early imaging biomarkers for various diseases long before disease onset.

Identifiants

pubmed: 35094045
pii: 6517440
doi: 10.1093/cercor/bhab516
pmc: PMC9627041
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4782-4796

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press.

Références

Neuron. 2009 Nov 12;64(3):404-18
pubmed: 19914188
Sleep. 2011 Mar 01;34(3):283-91A
pubmed: 21358845
Neuroimage. 2013 Jul 1;74:288-97
pubmed: 23481462
Cell Rep. 2014 Dec 11;9(5):1654-1660
pubmed: 25482555
Neuroimage. 2000 Aug;12(2):230-9
pubmed: 10913328
Science. 2009 May 22;324(5930):1084-7
pubmed: 19461004
Front Syst Neurosci. 2020 May 19;14:8
pubmed: 32508601
Neuroimage. 1998 Jan;7(1):30-40
pubmed: 9500830
Elife. 2018 Sep 04;7:
pubmed: 30179155
Cereb Cortex. 2000 Dec;10(12):1185-99
pubmed: 11073868
Sleep. 2011 Oct 01;34(10):1411-21
pubmed: 21966073
Neuron. 2013 Mar 20;77(6):1136-50
pubmed: 23522048
Nat Neurosci. 2010 Jan;13(1):9-17
pubmed: 19966841
Neuroscience. 2006;137(4):1087-106
pubmed: 16343791
Nat Neurosci. 2015 Nov;18(11):1623-30
pubmed: 26457554
PLoS One. 2007 Sep 12;2(9):e888
pubmed: 17849017
Neuron. 2011 Apr 14;70(1):153-69
pubmed: 21482364
IEEE Trans Biomed Eng. 2012 Oct;59(10):2808-17
pubmed: 22868527
Nature. 2011 Apr 28;472(7344):443-7
pubmed: 21525926
PLoS One. 2009 Oct 26;4(10):e7601
pubmed: 19855839
Nat Rev Neurosci. 2010 Feb;11(2):114-26
pubmed: 20046194
Physiol Rev. 2013 Apr;93(2):681-766
pubmed: 23589831
Neuroimage. 2005 Nov 15;28(3):720-37
pubmed: 16150610
Proc R Soc Med. 1937 Mar;30(5):579-98
pubmed: 19991061
Sleep. 2014 Oct 01;37(10):1621-37
pubmed: 25197810
Nat Rev Neurosci. 2018 Feb;19(2):107-118
pubmed: 29321683
Nat Protoc. 2018 May;13(5):840-855
pubmed: 29599439
Neuroimage. 2021 Aug 1;236:118117
pubmed: 33940148
Nat Neurosci. 2018 Oct;21(10):1392-1403
pubmed: 30258239
Front Hum Neurosci. 2018 Jun 19;12:248
pubmed: 29970995
Prog Brain Res. 2004;145:179-96
pubmed: 14650916
J Neurosci. 2014 Jun 25;34(26):8875-93
pubmed: 24966387
Curr Opin Neurobiol. 2015 Apr;31:72-80
pubmed: 25233254
Neuron. 2014 Jan 8;81(1):12-34
pubmed: 24411729
Elife. 2016 May 31;5:
pubmed: 27244241
Nat Neurosci. 2010 Oct;13(10):1283-91
pubmed: 20818384
Neurology. 2010 Jun 15;74(24):1969-76
pubmed: 20463288
Neuroimage. 2003 Jul;19(3):1233-9
pubmed: 12880848
Sleep. 2007 Dec;30(12):1643-57
pubmed: 18246974
Neuron. 2017 Sep 27;96(1):17-42
pubmed: 28957666
Elife. 2020 Jun 22;9:
pubmed: 32568067
J Neurosci. 2002 Dec 15;22(24):10941-7
pubmed: 12486189
J Neurophysiol. 2009 Apr;101(4):1921-31
pubmed: 19164101
Nat Sci Sleep. 2016 Jul 12;8:221-38
pubmed: 27471418
J Neurosci. 2015 Feb 4;35(5):2058-73
pubmed: 25653363
Arch Ital Biol. 2014 Jun-Sep;152(2-3):147-55
pubmed: 25828686
J Physiol. 2017 Mar 15;595(6):1885-1902
pubmed: 27619153
Proc Natl Acad Sci U S A. 2009 Feb 3;106(5):1608-13
pubmed: 19164756
Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15160-5
pubmed: 18815373
J Neurosci. 2018 Oct 24;38(43):9175-9185
pubmed: 30201768
Curr Opin Neurobiol. 2017 Jun;44:178-185
pubmed: 28544930
J Neurosci. 1993 Aug;13(8):3252-65
pubmed: 8340806
Ann Neurol. 2010 Dec;68(6):865-75
pubmed: 21194156
J Neurophysiol. 2001 May;85(5):1969-85
pubmed: 11353014
Comput Intell Neurosci. 2011;2011:598206
pubmed: 21461381
Nat Neurosci. 2000 Oct;3(10):1027-34
pubmed: 11017176
Nat Neurosci. 2006 Sep;9(9):1169-76
pubmed: 16936722
J Neurosci Methods. 2016 Dec 1;274:1-12
pubmed: 27663980
Cereb Cortex. 2020 May 18;30(6):3451-3466
pubmed: 31989160
J Neurophysiol. 2011 Dec;106(6):2910-21
pubmed: 21880935
J Neurosci. 2020 Jul 15;40(29):5589-5603
pubmed: 32541070
Curr Opin Neurobiol. 2017 Jun;44:116-126
pubmed: 28453998
Cell Rep. 2013 Jul 11;4(1):31-9
pubmed: 23810558
Neuroimage. 2014 Jan 1;84:1018-31
pubmed: 24071524
J Neurosci. 2012 Jan 4;32(1):243-53
pubmed: 22219286
Elife. 2017 Sep 15;6:
pubmed: 28914607
J Neurosci. 2004 Aug 4;24(31):6862-70
pubmed: 15295020
Neuron. 2009 Jul 30;63(2):178-88
pubmed: 19640477
Neuron. 2017 Jun 7;94(5):993-1001
pubmed: 28595056
Nature. 2004 Jul 1;430(6995):78-81
pubmed: 15184907
J Neurosci Methods. 2004 Mar 15;134(1):9-21
pubmed: 15102499
Neuroimage. 2009 May 1;45(4):1144-50
pubmed: 19349230

Auteurs

Merve Ilhan-Bayrakcı (M)

Systemic Mechanisms of Resilience, Leibniz Institute for Resilience Research (LIR), 55122 Mainz, Germany.

Yuranny Cabral-Calderin (Y)

Neural and Environmental Rhythms, Max Planck Institute for Empirical Aesthetics, 60322 Frankfurt, Germany.

Til Ole Bergmann (TO)

Systemic Mechanisms of Resilience, Leibniz Institute for Resilience Research (LIR), 55122 Mainz, Germany.
Neuroimaging Center (NIC), Focus Program Translational Neuroscience (FTN), University Medical Center of the Johannes Gutenberg University Mainz, 55131 Mainz, Germany.

Oliver Tüscher (O)

Systemic Mechanisms of Resilience, Leibniz Institute for Resilience Research (LIR), 55122 Mainz, Germany.
Department of Psychiatry and Psychotherapy, University Medical Center of the Johannes Gutenberg University Mainz, 55131 Mainz, Germany.

Albrecht Stroh (A)

Systemic Mechanisms of Resilience, Leibniz Institute for Resilience Research (LIR), 55122 Mainz, Germany.
Institute of Pathophysiology, University Medical Center of the Johannes Gutenberg University Mainz, 55131 Mainz, Germany.

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