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

Journal article

Parsons, Nicholas, Irimia, Andrei, Amgalan, Anar, Ugon, Julien, Morgan, Kerri, Shelyag, Sergiy, Hocking, Alex, Poudel, Govinda and Caeyenberghs, Karen. (2023). Structural-functional connectivity bandwidth predicts processing speed in mild traumatic brain injury : A multiplex network analysis. NeuroImage: Clinical. 38, p. Article 103428. https://doi.org/10.1016/j.nicl.2023.103428
AuthorsParsons, Nicholas, Irimia, Andrei, Amgalan, Anar, Ugon, Julien, Morgan, Kerri, Shelyag, Sergiy, Hocking, Alex, Poudel, Govinda and Caeyenberghs, Karen
Abstract

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.

Keywordsmild traumatic brain injury; structural connectivity; diffusion MRI; functional connectivity; functional MRI; multiplex network analysis
Year2023
JournalNeuroImage: Clinical
Journal citation38, p. Article 103428
PublisherElsevier Inc.
ISSN2213-1582
Digital Object Identifier (DOI)https://doi.org/10.1016/j.nicl.2023.103428
PubMed ID37167841
Scopus EID2-s2.0-85158885946
PubMed Central IDPMC10196722
Open accessPublished as ‘gold’ (paid) open access
Page range1-13
FunderDeakin University Postgraduate Research Scholarship (DUPRS)
Australian Research Council (ARC)
Department of Health, Victorian Government
Association of Australian Medical Research Institutes
Victorian Department of Jobs, Precincts and Regions, Victorian Government
Deakin University
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Open
Output statusPublished
Publication dates
Online05 May 2023
Publication process dates
Accepted01 May 2023
Deposited31 Mar 2025
ARC Funded ResearchThis output has been funded, wholly or partially, under the Australian Research Council Act 2001
Grant IDDP180100602
Additional information

© 2023 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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Dominguez, Juan F., Ng, Amanda C. L., Poudel, Govinda, Stout, Julie C., Churchyard, A., Chua, Phyllis, Egan, Gary F. and Georgiou-Karistianis, Nellie. (2016). Iron accumulation in the basal ganglia in Huntington's disease: Cross-sectional data from the IMAGE-HD study. Journal of Neurology, Neurosurgery and Psychiatry. 87(5), pp. 545 - 549. https://doi.org/10.1136/jnnp-2014-310183
Subjective sleep problems in Huntington's disease: A pilot investigation of the relationship to brain structure, neurocognitive, and neuropsychiatric function
Baker, Chaya Rochel, Dominguez, Juan F., Stout, Julie C., Gabery, Sanaz, Churchyard, A., Chua, Phyllis, Egan, Gary F., Petersen, Asa, Georgiou-Karistianis, Nellie and Poudel, Govinda. (2016). Subjective sleep problems in Huntington's disease: A pilot investigation of the relationship to brain structure, neurocognitive, and neuropsychiatric function. Journal of the Neurological Sciences. 364, pp. 148 - 153. https://doi.org/10.1016/j.jns.2016.03.021
Microsleeps are associated with stage-2 sleep spindles from hippocampal-temporal network
Jonmohamadi, Yaqub, Poudel, Govinda, Innes, Carrie C. R. H. and Jones, Richard. (2016). Microsleeps are associated with stage-2 sleep spindles from hippocampal-temporal network. International Journal of Neural Systems. 26(4), pp. 1 - 12. https://doi.org/10.1142/S0129065716500155
Multimodal imaging biomarkers in premanifest and early Huntington's disease: 30-month IMAGE-HD data
Dominguez, Juan, Stout, Julie C., Poudel, Govinda, Churchyard, Andrew, Chua, Phyllis, Egan, Gary F. and Georgiou-Karistianis, Nellie. (2016). Multimodal imaging biomarkers in premanifest and early Huntington's disease: 30-month IMAGE-HD data. British Journal of Psychiatry. 208(6), pp. 571 - 578. https://doi.org/10.1192/bjp.bp.114.156588
Time-varying effective connectivity of the cortical neuroelectric activity associated with behavioural microsleeps
Toppi, Jlenia, Astolfi, Laura, Poudel, Govinda, H., Babiloni, Fabio, Jones, Richard and Innes, Carrie R. H.. (2016). Time-varying effective connectivity of the cortical neuroelectric activity associated with behavioural microsleeps. NeuroImage. 124, pp. 421 - 432. https://doi.org/10.1016/j.neuroimage.2015.08.059
Characterising upper limb movements in Huntington's Disease and the impact of restricted visual cues
Despard, Jessica, Ternes, Anne-Marie, Dimech-Betancourt, Bleydy, Poudel, Govinda, Churchyard, Andrew and Georgiou-Karistianis, Nellie. (2015). Characterising upper limb movements in Huntington's Disease and the impact of restricted visual cues. PLoS ONE. 10(8), pp. 1 - 18. https://doi.org/10.1371/journal.pone.0133709
Comparison of beamformers for EEG source signal reconstruction
Jonmohamadi, Yaqub, Poudel, Govinda, Innes, Carrie, Weiss, Daniel, Krueger, Rejko and Jones, Richard. (2014). Comparison of beamformers for EEG source signal reconstruction. Biomedical Signal Processing and Control. 14(1), pp. 175 - 188. https://doi.org/10.1016/j.bspc.2014.07.014
Source-space ICA for EEG source separation, localization, and time-course reconstruction
Jonmohamadi, Yaqub, Poudel, Govinda, Innes, Carrie and Jones, Richard. (2014). Source-space ICA for EEG source separation, localization, and time-course reconstruction. NeuroImage. 101(November), pp. 720 - 737. https://doi.org/10.1016/j.neuroimage.2014.07.052
The Multi-modal Australian ScienceS Imaging and Visualization Environment (MASSIVE) high performance computing infrastructure: Applications in neuroscience and neuroinformatics research
Goscinski, Wojtek J., McIntosh, Paul, Felzmann, Ulrich, Maksimenko, Anton, Hall, Christopher J., Gureyev, Timur, Thompson, Darren, Janke, Andrew, Galloway, Graham, Killeen, Neil E. B., Raniga, Parnesh, Kaluza, Owen, Ng, Amanda, Poudel, Govinda, Barnes, David G., Nguyen, Toan, Bonnington, Paul and Egan, Gary F.. (2014). The Multi-modal Australian ScienceS Imaging and Visualization Environment (MASSIVE) high performance computing infrastructure: Applications in neuroscience and neuroinformatics research. Frontiers in Neuroinformatics. 8(March), pp. 1 - 13. https://doi.org/10.3389/fninf.2014.00030
Functional magnetic resonance imaging of working memory in Huntington's disease: Cross-sectional data from the IMAGE-HD study
Georgiou-Karistianis, Nellie, Stout, Julie C., Domínguez, Juan F., Carron, Sarah P., Ando, Ayaka, Churchyard, Andrew, Chua, Phyllis, Bohanna, India, Dymowski, Alicia R., Poudel, Govinda and Egan, Gary F.. (2014). Functional magnetic resonance imaging of working memory in Huntington's disease: Cross-sectional data from the IMAGE-HD study. Human Brain Mapping. 35(5), pp. 1847 - 1864. https://doi.org/10.1002/hbm.22296
Voxel-ICA for reconstruction of source signal time-series and orientation in EEG and MEG
Jonmohamadi, Yaqub, Poudel, Govinda, Innes, Carrie and Jones, Richard. (2014). Voxel-ICA for reconstruction of source signal time-series and orientation in EEG and MEG. Australasian Physical and Engineering Sciences in Medicine. 37(2), pp. 457 - 464. https://doi.org/10.1007/s13246-014-0265-x
Multi-modal neuroimaging in premanifest and early Huntington's disease : 18 month longitudinal data from the IMAGE-HD study
Domínguez D, Juan F., Egan, Gary F., Gray, Marcus A., Poudel, Govinda R., Churchyard, Andrew, Chua, Phyllis, Stout, Julie C. and Georgiou-Karistianis, Nellie. (2013). Multi-modal neuroimaging in premanifest and early Huntington's disease : 18 month longitudinal data from the IMAGE-HD study. PLoS ONE. 8(9), pp. 1-10. https://doi.org/10.1371/journal.pone.0074131
Functional and connectivity changes during working memory in Huntington's disease : 18 month longitudinal data from the IMAGE-HD study
Georgiou-Karistianis, Nellie, Poudel, Govinda R., Domínguez D, Juan F., Langmaid, Rebecca, Gray, Marcus A., Churchyard, Andrew, Chua, Phyllis, Borowsky, Beth, Egan, Gary F. and Stout, Julie C.. (2013). Functional and connectivity changes during working memory in Huntington's disease : 18 month longitudinal data from the IMAGE-HD study. Brain and Cognition. 83(1), pp. 80-91. https://doi.org/10.1016/j.bandc.2013.07.004
Efficient and regular patterns of nighttime sleep are related to increased vulnerability to microsleeps following a single night of sleep restriction
Innes, Carrie R. H., Poudel, Govinda R. and Jones, Richard D.. (2013). Efficient and regular patterns of nighttime sleep are related to increased vulnerability to microsleeps following a single night of sleep restriction. Chronobiology International. 30(9), pp. 1187-1196. https://doi.org/10.3109/07420528.2013.810222
Distinct neural correlates of time-on-task and transient errors during a visuomotor tracking task after sleep restriction
Poudel, Govinda R., Innes, Carrie R. H. and Jones, Richard D.. (2013). Distinct neural correlates of time-on-task and transient errors during a visuomotor tracking task after sleep restriction. NeuroImage. 77, pp. 105-113. https://doi.org/10.1016/j.neuroimage.2013.03.054
Time-Varying Functional Connectivity for Understanding the Neural Basis of Behavioral Microsleeps
J Toppi, L Astolfi, GR Poudel, F Babiloni, L Macchiusi, D Mattia, S Salinari and RD Jones. (2012). Time-Varying Functional Connectivity for Understanding the Neural Basis of Behavioral Microsleeps. 34th Annual International Conference of the IEEE EMBS. IEEE, Institute of Electrical and Electronics Engineers. pp. 4708-4711 https://doi.org/10.1109/EMBC.2012.6347018
Performance of Beamformers on EEG Source Reconstruction
Yaqub Jon Mohamadi, Govinda Poudel, Carrie R H Innes and Richard Jones. (2012). Performance of Beamformers on EEG Source Reconstruction. 34th Annual International Conference of the IEEE EMBS. IEEE, Institute of Electrical and Electronics Engineers. https://doi.org/10.1109/EMBC.2012.6346476
Cerebral perfusion differences between drowsy and nondrowsy individuals after acute sleep restriction
Poudel, Govinda R., Innes, Carrie R. H. and Jones, Richard D.. (2012). Cerebral perfusion differences between drowsy and nondrowsy individuals after acute sleep restriction. Sleep. 35(8), pp. 1085-1096. https://doi.org/10.5665/sleep.1994