Preserved fractal character of structural brain networks is associated with covert consciousness after severe brain injury

Self-similarity is ubiquitous throughout natural phenomena, including the human brain. Recent evidence indicates that fractal dimension of functional brain networks, a measure of self-similarity, is diminished in patients diagnosed with disorders of consciousness arising from severe brain injury. He...

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Main Authors: Andrea I. Luppi, Michael M. Craig, Peter Coppola, Alexander R.D. Peattie, Paola Finoia, Guy B. Williams, Judith Allanson, John D. Pickard, David K. Menon, Emmanuel A. Stamatakis
Format: Article
Language:English
Published: Elsevier 2021-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158221001261
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language English
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author Andrea I. Luppi
Michael M. Craig
Peter Coppola
Alexander R.D. Peattie
Paola Finoia
Guy B. Williams
Judith Allanson
John D. Pickard
David K. Menon
Emmanuel A. Stamatakis
spellingShingle Andrea I. Luppi
Michael M. Craig
Peter Coppola
Alexander R.D. Peattie
Paola Finoia
Guy B. Williams
Judith Allanson
John D. Pickard
David K. Menon
Emmanuel A. Stamatakis
Preserved fractal character of structural brain networks is associated with covert consciousness after severe brain injury
NeuroImage: Clinical
Disorders of consciousness
Brain injury
Diffusion MRI
Fractal
Brain network
Cognitive-motor dissociation
author_facet Andrea I. Luppi
Michael M. Craig
Peter Coppola
Alexander R.D. Peattie
Paola Finoia
Guy B. Williams
Judith Allanson
John D. Pickard
David K. Menon
Emmanuel A. Stamatakis
author_sort Andrea I. Luppi
title Preserved fractal character of structural brain networks is associated with covert consciousness after severe brain injury
title_short Preserved fractal character of structural brain networks is associated with covert consciousness after severe brain injury
title_full Preserved fractal character of structural brain networks is associated with covert consciousness after severe brain injury
title_fullStr Preserved fractal character of structural brain networks is associated with covert consciousness after severe brain injury
title_full_unstemmed Preserved fractal character of structural brain networks is associated with covert consciousness after severe brain injury
title_sort preserved fractal character of structural brain networks is associated with covert consciousness after severe brain injury
publisher Elsevier
series NeuroImage: Clinical
issn 2213-1582
publishDate 2021-01-01
description Self-similarity is ubiquitous throughout natural phenomena, including the human brain. Recent evidence indicates that fractal dimension of functional brain networks, a measure of self-similarity, is diminished in patients diagnosed with disorders of consciousness arising from severe brain injury. Here, we set out to investigate whether loss of self-similarity is observed in the structural connectome of patients with disorders of consciousness. Using diffusion MRI tractography from N = 11 patients in a minimally conscious state (MCS), N = 10 patients diagnosed with unresponsive wakefulness syndrome (UWS), and N = 20 healthy controls, we show that fractal dimension of structural brain networks is diminished in DOC patients. Remarkably, we also show that fractal dimension of structural brain networks is preserved in patients who exhibit evidence of covert consciousness by performing mental imagery tasks during functional MRI scanning. These results demonstrate that differences in fractal dimension of structural brain networks are quantitatively associated with chronic loss of consciousness induced by severe brain injury, highlighting the close connection between structural organisation of the human brain and its ability to support cognitive function.
topic Disorders of consciousness
Brain injury
Diffusion MRI
Fractal
Brain network
Cognitive-motor dissociation
url http://www.sciencedirect.com/science/article/pii/S2213158221001261
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spelling doaj-34729b6972334df585af9505780591632021-06-13T04:38:13ZengElsevierNeuroImage: Clinical2213-15822021-01-0130102682Preserved fractal character of structural brain networks is associated with covert consciousness after severe brain injuryAndrea I. Luppi0Michael M. Craig1Peter Coppola2Alexander R.D. Peattie3Paola Finoia4Guy B. Williams5Judith Allanson6John D. Pickard7David K. Menon8Emmanuel A. Stamatakis9Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United Kingdom; Department of Clinical Neurosciences, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United Kingdom; Corresponding author at: Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United Kingdom.Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United Kingdom; Department of Clinical Neurosciences, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United KingdomDivision of Anaesthesia, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United Kingdom; Department of Clinical Neurosciences, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United KingdomDivision of Anaesthesia, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United Kingdom; Department of Clinical Neurosciences, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United KingdomDivision of Anaesthesia, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United Kingdom; Division of Neurosurgery, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United KingdomDepartment of Clinical Neurosciences, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United Kingdom; Wolfson Brain Imaging Centre, University of Cambridge, Cambridge Biomedical Campus (Box 65), Cambridge CB2 0QQ, United KingdomDepartment of Clinical Neurosciences, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United Kingdom; Department of Neurosciences, Cambridge University Hospitals NHS Foundation, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United KingdomDepartment of Clinical Neurosciences, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United Kingdom; Division of Neurosurgery, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United Kingdom; Wolfson Brain Imaging Centre, University of Cambridge, Cambridge Biomedical Campus (Box 65), Cambridge CB2 0QQ, United KingdomDivision of Anaesthesia, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United Kingdom; Wolfson Brain Imaging Centre, University of Cambridge, Cambridge Biomedical Campus (Box 65), Cambridge CB2 0QQ, United KingdomDivision of Anaesthesia, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United Kingdom; Department of Clinical Neurosciences, School of Clinical Medicine, University of Cambridge, Addenbrooke's Hospital, Hills Rd, CB2 0SP, Cambridge, United KingdomSelf-similarity is ubiquitous throughout natural phenomena, including the human brain. Recent evidence indicates that fractal dimension of functional brain networks, a measure of self-similarity, is diminished in patients diagnosed with disorders of consciousness arising from severe brain injury. Here, we set out to investigate whether loss of self-similarity is observed in the structural connectome of patients with disorders of consciousness. Using diffusion MRI tractography from N = 11 patients in a minimally conscious state (MCS), N = 10 patients diagnosed with unresponsive wakefulness syndrome (UWS), and N = 20 healthy controls, we show that fractal dimension of structural brain networks is diminished in DOC patients. Remarkably, we also show that fractal dimension of structural brain networks is preserved in patients who exhibit evidence of covert consciousness by performing mental imagery tasks during functional MRI scanning. These results demonstrate that differences in fractal dimension of structural brain networks are quantitatively associated with chronic loss of consciousness induced by severe brain injury, highlighting the close connection between structural organisation of the human brain and its ability to support cognitive function.http://www.sciencedirect.com/science/article/pii/S2213158221001261Disorders of consciousnessBrain injuryDiffusion MRIFractalBrain networkCognitive-motor dissociation