Structural-functional connectivity bandwidth predicts processing speed in mild traumatic brain Injury: A multiplex network analysis

An emerging body of work has revealed alterations in structural (SC) and functional (FC) brain connectivity following mild TBI (mTBI), with mixed findings. However, these studies seldom integrate complimentary neuroimaging modalities within a unified framework. Multilayer network analysis is an emer...

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Main Authors: Nicholas Parsons, Andrei Irimia, Anar Amgalan, Julien Ugon, Kerri Morgan, Sergiy Shelyag, Alex Hocking, Govinda Poudel, Karen Caeyenberghs
Format: Article
Language:English
Published: Elsevier 2023-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158223001171
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author Nicholas Parsons
Andrei Irimia
Anar Amgalan
Julien Ugon
Kerri Morgan
Sergiy Shelyag
Alex Hocking
Govinda Poudel
Karen Caeyenberghs
author_facet Nicholas Parsons
Andrei Irimia
Anar Amgalan
Julien Ugon
Kerri Morgan
Sergiy Shelyag
Alex Hocking
Govinda Poudel
Karen Caeyenberghs
author_sort Nicholas Parsons
collection DOAJ
description An emerging body of work has revealed alterations in structural (SC) and functional (FC) brain connectivity following mild TBI (mTBI), with mixed findings. However, these studies seldom integrate complimentary neuroimaging modalities within a unified framework. Multilayer network analysis is an emerging technique to uncover how white matter organization enables functional communication. Using our novel graph metric (SC-FC Bandwidth), we quantified the information capacity of synchronous brain regions in 53 mild TBI patients (46 females; age mean = 40.2 years (y), σ = 16.7 (y), range: 18–79 (y). Diffusion MRI and resting state fMRI were administered at the acute and chronic post-injury intervals. Moreover, participants completed a cognitive task to measure processing speed (30 Seconds and Counting Task; 30-SACT). Processing speed was significantly increased at the chronic, relative to the acute post-injury intervals (p = <0.001). Nonlinear principal components of direct (t = -1.84, p = 0.06) and indirect SC-FC Bandwidth (t = 3.86, p = <0.001) predicted processing speed with a moderate effect size (R2 = 0.43, p < 0.001), while controlling for age. A subnetwork of interhemispheric edges with increased SC-FC Bandwidth was identified at the chronic, relative to the acute mTBI post-injury interval (pFDR = 0.05). Increased interhemispheric SC-FC Bandwidth of this network corresponded with improved processing speed at the chronic post-injury interval (partial r = 0.32, p = 0.02). Our findings revealed that mild TBI results in complex reorganization of brain connectivity optimized for maximum information flow, supporting improved cognitive performance as a compensatory mechanism. Moving forward, this measurement may complement clinical assessment as an objective marker of mTBI recovery.
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spelling doaj.art-0ec54d97676e49b2a406dcff63a4fca52023-06-15T04:55:58ZengElsevierNeuroImage: Clinical2213-15822023-01-0138103428Structural-functional connectivity bandwidth predicts processing speed in mild traumatic brain Injury: A multiplex network analysisNicholas Parsons0Andrei Irimia1Anar Amgalan2Julien Ugon3Kerri Morgan4Sergiy Shelyag5Alex Hocking6Govinda Poudel7Karen Caeyenberghs8Cognitive Neuroscience Unit, School of Psychology, Deakin University, Melbourne, VIC, Australia; BrainCast Neurotechnologies, Australia; School of Psychological Sciences, Faculty of Medicine, Nursing and Health Sciences, Monash University, AustraliaEthel Percy Andrus Gerontology Center, Leonard Davis School of Gerontology, University of Southern California, Los Angeles, CA, USAEthel Percy Andrus Gerontology Center, Leonard Davis School of Gerontology, University of Southern California, Los Angeles, CA, USASchool of Information Technology, Faculty of Science Engineering Built Environment, Deakin University, Melbourne, VIC, AustraliaSchool of Information Technology, Faculty of Science Engineering Built Environment, Deakin University, Melbourne, VIC, AustraliaSchool of Information Technology, Faculty of Science Engineering Built Environment, Deakin University, Melbourne, VIC, AustraliaSchool of Information Technology, Faculty of Science Engineering Built Environment, Deakin University, Melbourne, VIC, AustraliaBrainCast Neurotechnologies, Australia; Mary MacKillop Institute for Health Research, Australian Catholic University, Melbourne, VIC, AustraliaCognitive Neuroscience Unit, School of Psychology, Deakin University, Melbourne, VIC, AustraliaAn emerging body of work has revealed alterations in structural (SC) and functional (FC) brain connectivity following mild TBI (mTBI), with mixed findings. However, these studies seldom integrate complimentary neuroimaging modalities within a unified framework. Multilayer network analysis is an emerging technique to uncover how white matter organization enables functional communication. Using our novel graph metric (SC-FC Bandwidth), we quantified the information capacity of synchronous brain regions in 53 mild TBI patients (46 females; age mean = 40.2 years (y), σ = 16.7 (y), range: 18–79 (y). Diffusion MRI and resting state fMRI were administered at the acute and chronic post-injury intervals. Moreover, participants completed a cognitive task to measure processing speed (30 Seconds and Counting Task; 30-SACT). Processing speed was significantly increased at the chronic, relative to the acute post-injury intervals (p = <0.001). Nonlinear principal components of direct (t = -1.84, p = 0.06) and indirect SC-FC Bandwidth (t = 3.86, p = <0.001) predicted processing speed with a moderate effect size (R2 = 0.43, p < 0.001), while controlling for age. A subnetwork of interhemispheric edges with increased SC-FC Bandwidth was identified at the chronic, relative to the acute mTBI post-injury interval (pFDR = 0.05). Increased interhemispheric SC-FC Bandwidth of this network corresponded with improved processing speed at the chronic post-injury interval (partial r = 0.32, p = 0.02). Our findings revealed that mild TBI results in complex reorganization of brain connectivity optimized for maximum information flow, supporting improved cognitive performance as a compensatory mechanism. Moving forward, this measurement may complement clinical assessment as an objective marker of mTBI recovery.http://www.sciencedirect.com/science/article/pii/S2213158223001171Mild traumatic brain injuryStructural connectivityDiffusion MRIFunctional connectivityFunctional MRIMultiplex Network Analysis
spellingShingle Nicholas Parsons
Andrei Irimia
Anar Amgalan
Julien Ugon
Kerri Morgan
Sergiy Shelyag
Alex Hocking
Govinda Poudel
Karen Caeyenberghs
Structural-functional connectivity bandwidth predicts processing speed in mild traumatic brain Injury: A multiplex network analysis
NeuroImage: Clinical
Mild traumatic brain injury
Structural connectivity
Diffusion MRI
Functional connectivity
Functional MRI
Multiplex Network Analysis
title Structural-functional connectivity bandwidth predicts processing speed in mild traumatic brain Injury: A multiplex network analysis
title_full Structural-functional connectivity bandwidth predicts processing speed in mild traumatic brain Injury: A multiplex network analysis
title_fullStr Structural-functional connectivity bandwidth predicts processing speed in mild traumatic brain Injury: A multiplex network analysis
title_full_unstemmed Structural-functional connectivity bandwidth predicts processing speed in mild traumatic brain Injury: A multiplex network analysis
title_short Structural-functional connectivity bandwidth predicts processing speed in mild traumatic brain Injury: A multiplex network analysis
title_sort structural functional connectivity bandwidth predicts processing speed in mild traumatic brain injury a multiplex network analysis
topic Mild traumatic brain injury
Structural connectivity
Diffusion MRI
Functional connectivity
Functional MRI
Multiplex Network Analysis
url http://www.sciencedirect.com/science/article/pii/S2213158223001171
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