An altered balance of integrated and segregated brain activity is a marker of cognitive deficits following sleep deprivation.


Journal

PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755

Informations de publication

Date de publication:
11 2021
Historique:
received: 14 04 2021
accepted: 28 09 2021
entrez: 4 11 2021
pubmed: 5 11 2021
medline: 22 12 2021
Statut: epublish

Résumé

Sleep deprivation (SD) leads to impairments in cognitive function. Here, we tested the hypothesis that cognitive changes in the sleep-deprived brain can be explained by information processing within and between large-scale cortical networks. We acquired functional magnetic resonance imaging (fMRI) scans of 20 healthy volunteers during attention and executive tasks following a regular night of sleep, a night of SD, and a recovery nap containing nonrapid eye movement (NREM) sleep. Overall, SD was associated with increased cortex-wide functional integration, driven by a rise of integration within cortical networks. The ratio of within versus between network integration in the cortex increased further in the recovery nap, suggesting that prolonged wakefulness drives the cortex towards a state resembling sleep. This balance of integration and segregation in the sleep-deprived state was tightly associated with deficits in cognitive performance. This was a distinct and better marker of cognitive impairment than conventional indicators of homeostatic sleep pressure, as well as the pronounced thalamocortical connectivity changes that occurs towards falling asleep. Importantly, restoration of the balance between segregation and integration of cortical activity was also related to performance recovery after the nap, demonstrating a bidirectional effect. These results demonstrate that intra- and interindividual differences in cortical network integration and segregation during task performance may play a critical role in vulnerability to cognitive impairment in the sleep-deprived state.

Identifiants

pubmed: 34735431
doi: 10.1371/journal.pbio.3001232
pii: PBIOLOGY-D-21-01005
pmc: PMC8568176
doi:

Substances chimiques

Biomarkers 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e3001232

Subventions

Organisme : CIHR
ID : MOP 142191
Pays : Canada
Organisme : CIHR
ID : PJT 153115
Pays : Canada
Organisme : CIHR
ID : PJT 156125
Pays : Canada
Organisme : CIHR
ID : PJT 166167
Pays : Canada
Organisme : CIHR
ID : PJT-159948
Pays : Canada
Organisme : CIHR
ID : MOP-133619
Pays : Canada

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Neuroimage. 2015 May 1;111:147-58
pubmed: 25700949
Brain Res. 2018 Jun 1;1688:22-32
pubmed: 29174693
Neuroimage. 2009 Feb 1;44(3):893-905
pubmed: 18976716
Sleep. 2016 Mar 01;39(3):687-98
pubmed: 26612392
Med Image Anal. 2008 Aug;12(4):484-96
pubmed: 18396441
Sci Transl Med. 2012 Aug 15;4(147):147ra111
pubmed: 22896675
J Exp Psychol. 1958 Apr;55(4):352-8
pubmed: 13539317
Neuroimage. 2006 Feb 15;29(4):1231-43
pubmed: 16246590
Neuroimage. 2011 Jun 15;56(4):2068-79
pubmed: 21459148
Hum Brain Mapp. 2020 Mar;41(4):994-1005
pubmed: 31680379
Proc Natl Acad Sci U S A. 2013 Sep 17;110(38):15419-24
pubmed: 24003146
J Neurophysiol. 2011 Sep;106(3):1125-65
pubmed: 21653723
iScience. 2020 Dec 10;24(1):101923
pubmed: 33409474
Neuroimage. 2012 Jun;61(2):407-26
pubmed: 22245638
Neuroimage. 2017 Jul 1;154:174-187
pubmed: 28302591
Neuroimage. 2019 Feb 1;186:497-509
pubmed: 30471387
Biol Bull. 2008 Dec;215(3):216-42
pubmed: 19098144
Proc Natl Acad Sci U S A. 2012 Apr 10;109(15):5856-61
pubmed: 22451917
Nat Methods. 2019 Jan;16(1):111-116
pubmed: 30532080
Curr Opin Neurobiol. 2013 Apr;23(2):162-71
pubmed: 23294553
Neuroimage. 2012 Jan 16;59(2):1745-51
pubmed: 21872664
Trends Cogn Sci. 2004 Sep;8(9):418-25
pubmed: 15350243
Neuroimage. 2018 Sep;178:540-551
pubmed: 29860082
Hum Brain Mapp. 2017 Jun;38(6):3300-3314
pubmed: 28370703
Proc Natl Acad Sci U S A. 1994 May 24;91(11):5033-7
pubmed: 8197179
BMC Neurosci. 2004 Nov 02;5:42
pubmed: 15522121
Neuroimage. 2019 Oct 15;200:382-390
pubmed: 31276798
J Neurosurg. 1981 Feb;54(2):151-69
pubmed: 7452329
Sci Rep. 2017 Aug 25;7(1):9422
pubmed: 28842597
Brain Res Brain Res Rev. 2002 Sep;39(2-3):107-40
pubmed: 12423763
Science. 2019 Nov 1;366(6465):628-631
pubmed: 31672896
Sleep. 2012 Aug 01;35(8):1163-72
pubmed: 22851812
Proc Natl Acad Sci U S A. 2005 Jul 5;102(27):9673-8
pubmed: 15976020
Cereb Cortex. 2018 Sep 1;28(9):3095-3114
pubmed: 28981612
Neuron. 2016 Oct 19;92(2):544-554
pubmed: 27693256
Science. 1993 Oct 29;262(5134):679-85
pubmed: 8235588
J Cogn Neurosci. 2002 Apr 1;14(3):340-7
pubmed: 11970796
J Neurosci. 2010 Aug 25;30(34):11379-87
pubmed: 20739559
Nat Rev Neurosci. 2001 Apr;2(4):229-39
pubmed: 11283746
PLoS One. 2013 Oct 25;8(10):e78830
pubmed: 24205327
Science. 1996 Jan 26;271(5248):512-5
pubmed: 8560267
Neuroimage. 2013 Dec;83:983-90
pubmed: 23899724
Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3829-33
pubmed: 20142493
Science. 2013 Oct 18;342(6156):373-7
pubmed: 24136970
Neuropsychiatr Dis Treat. 2007;3(5):553-67
pubmed: 19300585
Nat Commun. 2019 Sep 2;10(1):3910
pubmed: 31477706
J Neurosci. 2013 Mar 13;33(11):4672-82
pubmed: 23486941
Neuropsychiatr Dis Treat. 2016 Apr 12;12:801-7
pubmed: 27110113
Sci Adv. 2019 Feb 27;5(2):eaav5447
pubmed: 30820460
Proc Natl Acad Sci U S A. 2016 Aug 23;113(34):9653-8
pubmed: 27512040
Clin Neurophysiol. 2015 Sep;126(9):1677-83
pubmed: 25666728
Prog Neurobiol. 2021 Apr;199:101951
pubmed: 33189781
J Neuropathol Exp Neurol. 2012 Jun;71(6):531-46
pubmed: 22592840
J Psychol. 2000 Mar;134(2):153-61
pubmed: 10766107
Front Hum Neurosci. 2013 Sep 17;7:493
pubmed: 24062654
Brain Connect. 2011;1(3):195-206
pubmed: 22433048
Neuroimage. 2021 Feb 1;226:117547
pubmed: 33186718
Sci Rep. 2017 Nov 2;7(1):14889
pubmed: 29097703

Auteurs

Nathan E Cross (NE)

PERFORM Centre, Concordia University, Montreal, Canada.
Center for Studies in Behavioral Neurobiology, Department of Health, Kinesiology and Applied Physiology, Concordia University, Montreal, Canada.
Institut Universitaire de Gériatrie de Montréal and CRIUGM, CIUSSS du Centre-Sud-de-l'Île-de-Montréal, Montreal, Canada.

Florence B Pomares (FB)

PERFORM Centre, Concordia University, Montreal, Canada.
Center for Studies in Behavioral Neurobiology, Department of Health, Kinesiology and Applied Physiology, Concordia University, Montreal, Canada.
Institut Universitaire de Gériatrie de Montréal and CRIUGM, CIUSSS du Centre-Sud-de-l'Île-de-Montréal, Montreal, Canada.

Alex Nguyen (A)

PERFORM Centre, Concordia University, Montreal, Canada.
Center for Studies in Behavioral Neurobiology, Department of Health, Kinesiology and Applied Physiology, Concordia University, Montreal, Canada.
Multimodal Functional Imaging Lab, Department of Physics, Concordia University, Montreal, Canada.

Aurore A Perrault (AA)

PERFORM Centre, Concordia University, Montreal, Canada.
Center for Studies in Behavioral Neurobiology, Department of Health, Kinesiology and Applied Physiology, Concordia University, Montreal, Canada.
Institut Universitaire de Gériatrie de Montréal and CRIUGM, CIUSSS du Centre-Sud-de-l'Île-de-Montréal, Montreal, Canada.

Aude Jegou (A)

PERFORM Centre, Concordia University, Montreal, Canada.
Multimodal Functional Imaging Lab, Department of Physics, Concordia University, Montreal, Canada.

Makoto Uji (M)

PERFORM Centre, Concordia University, Montreal, Canada.
Center for Studies in Behavioral Neurobiology, Department of Health, Kinesiology and Applied Physiology, Concordia University, Montreal, Canada.
Multimodal Functional Imaging Lab, Department of Physics, Concordia University, Montreal, Canada.

Kangjoo Lee (K)

Multimodal Functional Imaging Lab, Department of Physics, Concordia University, Montreal, Canada.
Multimodal Functional Imaging Lab, Biomedical Engineering Department, Neurology and Neurosurgery Department, McGill University, Montreal, Quebec, Canada.
Department of Radiology and Biomedical Imaging, Yale University School of Medicine, New Haven, Connecticut, United States of America.

Fatemeh Razavipour (F)

PERFORM Centre, Concordia University, Montreal, Canada.
Multimodal Functional Imaging Lab, Department of Physics, Concordia University, Montreal, Canada.
Multimodal Functional Imaging Lab, Biomedical Engineering Department, Neurology and Neurosurgery Department, McGill University, Montreal, Quebec, Canada.

Obaï Bin Ka'b Ali (OBK)

PERFORM Centre, Concordia University, Montreal, Canada.
Multimodal Functional Imaging Lab, Department of Physics, Concordia University, Montreal, Canada.
Multimodal Functional Imaging Lab, Biomedical Engineering Department, Neurology and Neurosurgery Department, McGill University, Montreal, Quebec, Canada.

Umit Aydin (U)

PERFORM Centre, Concordia University, Montreal, Canada.
Multimodal Functional Imaging Lab, Department of Physics, Concordia University, Montreal, Canada.
Multimodal Functional Imaging Lab, Biomedical Engineering Department, Neurology and Neurosurgery Department, McGill University, Montreal, Quebec, Canada.
Social, Genetic, and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology, and Neuroscience, King's College London, London, United Kingdom.

Habib Benali (H)

PERFORM Centre, Concordia University, Montreal, Canada.

Christophe Grova (C)

PERFORM Centre, Concordia University, Montreal, Canada.
Multimodal Functional Imaging Lab, Department of Physics, Concordia University, Montreal, Canada.
Multimodal Functional Imaging Lab, Biomedical Engineering Department, Neurology and Neurosurgery Department, McGill University, Montreal, Quebec, Canada.

Thien Thanh Dang-Vu (TT)

PERFORM Centre, Concordia University, Montreal, Canada.
Center for Studies in Behavioral Neurobiology, Department of Health, Kinesiology and Applied Physiology, Concordia University, Montreal, Canada.
Institut Universitaire de Gériatrie de Montréal and CRIUGM, CIUSSS du Centre-Sud-de-l'Île-de-Montréal, Montreal, Canada.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH