Fractal dimension of cortical functional connectivity networks & severity of disorders of consciousness.


Journal

PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081

Informations de publication

Date de publication:
2020
Historique:
received: 26 09 2019
accepted: 17 12 2019
entrez: 14 2 2020
pubmed: 14 2 2020
medline: 12 5 2020
Statut: epublish

Résumé

Recent evidence suggests that the quantity and quality of conscious experience may be a function of the complexity of activity in the brain and that consciousness emerges in a critical zone between low and high-entropy states. We propose fractal shapes as a measure of proximity to this critical point, as fractal dimension encodes information about complexity beyond simple entropy or randomness, and fractal structures are known to emerge in systems nearing a critical point. To validate this, we tested several measures of fractal dimension on the brain activity from healthy volunteers and patients with disorders of consciousness of varying severity. We used a Compact Box Burning algorithm to compute the fractal dimension of cortical functional connectivity networks as well as computing the fractal dimension of the associated adjacency matrices using a 2D box-counting algorithm. To test whether brain activity is fractal in time as well as space, we used the Higuchi temporal fractal dimension on BOLD time-series. We found significant decreases in the fractal dimension between healthy volunteers (n = 15), patients in a minimally conscious state (n = 10), and patients in a vegetative state (n = 8), regardless of the mechanism of injury. We also found significant decreases in adjacency matrix fractal dimension and Higuchi temporal fractal dimension, which correlated with decreasing level of consciousness. These results suggest that cortical functional connectivity networks display fractal character and that this is associated with level of consciousness in a clinically relevant population, with higher fractal dimensions (i.e. more complex) networks being associated with higher levels of consciousness. This supports the hypothesis that level of consciousness and system complexity are positively associated, and is consistent with previous EEG, MEG, and fMRI studies.

Identifiants

pubmed: 32053587
doi: 10.1371/journal.pone.0223812
pii: PONE-D-19-27002
pmc: PMC7017993
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0223812

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 083660/Z/07/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : U.1055.01.002.00001.01
Pays : United Kingdom
Organisme : Department of Health
Pays : United Kingdom

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

J Neurosci. 2009 Dec 9;29(49):15595-600
pubmed: 20007483
Proc Natl Acad Sci U S A. 2012 Feb 21;109(8):2825-30
pubmed: 22308319
Neuroscientist. 2013 Dec 20;20(4):403-417
pubmed: 24362815
Brain Imaging Behav. 2009 Jun;3(2):154-166
pubmed: 20740072
Neuroimage. 2007 Aug 1;37(1):90-101
pubmed: 17560126
Sci Rep. 2017 Dec 15;7(1):17661
pubmed: 29247209
Brain Connect. 2012;2(3):125-41
pubmed: 22642651
Front Physiol. 2016 Sep 27;7:425
pubmed: 27729870
Biol Bull. 2008 Dec;215(3):216-42
pubmed: 19098144
Neurosci Lett. 2017 Jul 13;653:320-325
pubmed: 28572032
Hum Brain Mapp. 2014 Nov;35(11):5442-56
pubmed: 24989126
Clin EEG Neurosci. 2014 Jan;45(1):40-9
pubmed: 24403317
PLoS One. 2014 Mar 19;9(3):e92182
pubmed: 24647227
Sci Rep. 2017 Apr 19;7:46421
pubmed: 28422113
IEEE Trans Biomed Eng. 2001 Dec;48(12):1424-33
pubmed: 11759923
J R Soc Interface. 2016 Jan;13(114):20151027
pubmed: 26819336
Hum Brain Mapp. 2006 Dec;27(12):994-1003
pubmed: 16671080
Proc Natl Acad Sci U S A. 1994 May 24;91(11):5033-7
pubmed: 8197179
Lancet Neurol. 2004 Sep;3(9):537-46
pubmed: 15324722
Front Physiol. 2012 May 07;3:123
pubmed: 22586406
PLoS One. 2015 Aug 07;10(8):e0133532
pubmed: 26252378
Neuroimage. 2012 Jul 2;61(3):694-701
pubmed: 22510257
Neurosci Lett. 2005 Aug 12-19;384(1-2):172-6
pubmed: 15893428
Neuroimage. 2019 Feb 1;186:221-233
pubmed: 30391346
Front Physiol. 2012 Jun 07;3:163
pubmed: 22701101
Phys Rev Lett. 2019 Apr 26;122(16):168301
pubmed: 31075025
Neuroscientist. 2015 Feb;21(1):30-43
pubmed: 24362814
Cereb Cortex. 2018 Sep 1;28(9):3095-3114
pubmed: 28981612
IEEE Trans Biomed Eng. 2006 Jun;53(6):1067-77
pubmed: 16761834
Neurosci Conscious. 2017 Jan 25;2017(1):niw022
pubmed: 30042832
Neuroimage. 2010 Sep;52(3):1059-69
pubmed: 19819337
Neurosci Lett. 1998 Jul 3;250(2):91-4
pubmed: 9697926
Front Hum Neurosci. 2014 Feb 03;8:20
pubmed: 24550805
Chaos. 2017 Apr;27(4):047408
pubmed: 28456175
J Neurosci. 2011 Jan 5;31(1):55-63
pubmed: 21209189
Proc Natl Acad Sci U S A. 2006 Dec 19;103(51):19518-23
pubmed: 17159150
Sci Rep. 2013;3:1585
pubmed: 23558260
Front Hum Neurosci. 2018 Feb 16;12:42
pubmed: 29503611
Comput Methods Programs Biomed. 2019 Jul;175:129-137
pubmed: 31104702
Sci Rep. 2017 Aug 7;7(1):7388
pubmed: 28785066
Comput Intell Neurosci. 2011;2011:406391
pubmed: 21512582
Neuropharmacology. 2018 Nov;142:167-178
pubmed: 29548884
Prog Neurobiol. 2017 Nov;158:132-152
pubmed: 28734836
Nat Rev Neurosci. 2016 May;17(5):307-21
pubmed: 27094080
PLoS One. 2010 Dec 02;5(12):e14224
pubmed: 21151992
Chaos. 2007 Jun;17(2):026116
pubmed: 17614703
Hum Brain Mapp. 2014 Jul;35(7):2935-49
pubmed: 24142410
J Neurosci. 2012 Jan 18;32(3):1061-72
pubmed: 22262904
Int J Psychol. 2013;48(4):695-703
pubmed: 22519470
Conf Proc IEEE Eng Med Biol Soc. 2005;2:2041-3
pubmed: 17282627
Comput Methods Programs Biomed. 2016 Sep;133:55-70
pubmed: 27393800

Auteurs

Thomas F Varley (TF)

Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, Cambridgeshire, England, United Kingdom.
Department of Clinical Neurosciences, School of Clinical Medicine, University of Cambridge, Cambridgeshire, England, United Kingdom.
Department of Psychological & Brain Sciences, Indiana University, Bloomington, Indiana, United States of America.

Michael Craig (M)

Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, Cambridgeshire, England, United Kingdom.
Department of Clinical Neurosciences, School of Clinical Medicine, University of Cambridge, Cambridgeshire, England, United Kingdom.

Ram Adapa (R)

Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, Cambridgeshire, England, United Kingdom.

Paola Finoia (P)

Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, Cambridgeshire, England, United Kingdom.

Guy Williams (G)

Wolfson Brain Imaging Center, University of Cambridge, Cambridgeshire, England, United Kingdom.

Judith Allanson (J)

Department of Neurorehabilitation, Addenbrooke's Hospital, Cambridgeshire, England, United Kingdom.

John Pickard (J)

Wolfson Brain Imaging Center, University of Cambridge, Cambridgeshire, England, United Kingdom.
Division of Neurosurgery, School of Clinical Medicine, University of Cambridge, Cambridgeshire, England, United Kingdom.

David K Menon (DK)

Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, Cambridgeshire, England, United Kingdom.
Wolfson Brain Imaging Center, University of Cambridge, Cambridgeshire, England, United Kingdom.

Emmanuel A Stamatakis (EA)

Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, Cambridgeshire, England, United Kingdom.
Department of Clinical Neurosciences, School of Clinical Medicine, University of Cambridge, Cambridgeshire, England, United Kingdom.

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