Cited by 123Functional Brain Connectivity StudiesTraumatic Brain Injury ResearchAdvanced Neuroimaging Techniques and Applications

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Disrupted modular organization of resting-state cortical functional connectivity in U.S. military personnel following concussive ‘mild’ blast-related traumatic brain injury

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Han, Kihwan, Mac Donald, Christine L., Johnson, Ann M., Barnes, Yolanda, Wierzechowski, Linda, Zonies, David, Oh, John, Flaherty, Stephen, Fang, Raymond, Raichle, Marcus E., Brody, David L.·2014·NeuroImage

DOI 10.1016/j.neuroimage.2013.08.017PMC PMC3849319

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Abstract

Blast-related traumatic brain injury (TBI) has been one of the "signature injuries" of the wars in Iraq and Afghanistan. However, neuroimaging studies in concussive 'mild' blast-related TBI have been challenging due to the absence of abnormalities in computed tomography or conventional magnetic resonance imaging (MRI) and the heterogeneity of the blast-related injury mechanisms. The goal of this study was to address these challenges utilizing single-subject, module-based graph theoretic analysis of resting-state functional MRI (fMRI) data. We acquired 20min of resting-state fMRI in 63 U.S. military personnel clinically diagnosed with concussive blast-related TBI and 21 U.S. military controls who had blast exposures but no diagnosis of TBI. All subjects underwent an initial scan within 90days post-injury and 65 subjects underwent a follow-up scan 6 to 12months later. A second independent cohort of 40 U.S. military personnel with concussive blast-related TBI served as a validation dataset. The second independent cohort underwent an initial scan within 30days post-injury. 75% of the scans were of good quality, with exclusions primarily due to excessive subject motion. Network analysis of the subset of these subjects in the first cohort with good quality scans revealed spatially localized reductions in the participation coefficient, a measure of between-module connectivity, in the TBI patients relative to the controls at the time of the initial scan. These group differences were less prominent on the follow-up scans. The 15 brain areas with the most prominent reductions in the participation coefficient were next used as regions of interest (ROIs) for single-subject analyses. In the first TBI cohort, more subjects than would be expected by chance (27/47 versus 2/47 expected, p<0.0001) had 3 or more brain regions with abnormally low between-module connectivity relative to the controls on the initial scans. On the follow-up scans, more subjects than expected by chance (5/37, p=0.044) but fewer subjects than on the initial scans had 3 or more brain regions with abnormally low between-module connectivity. Analysis of the second TBI cohort validation dataset with no free parameters provided a partial replication; again more subjects than expected by chance (8/31, p=0.006) had 3 or more brain regions with abnormally low between-module connectivity on the initial scans, but the numbers were not significant (2/27, p=0.276) on the follow-up scans. A single-subject, multivariate analysis by probabilistic principal component analysis of the between-module connectivity in the 15 identified ROIs, showed that 31/47 subjects in the first TBI cohort were found to be abnormal relative to the controls on the initial scans. In the second TBI cohort, 9/31 patients were found to be abnormal in identical multivariate analysis with no free parameters. Again, there were not substantial differences on the follow-up scans. Taken together, these results indicate that single-subject, module-based graph theoretic analysis of resting-state fMRI provides potentially useful information for concussive blast-related TBI if high quality scans can be obtained. The underlying biological mechanisms and consequences of disrupted between-module connectivity are unknown, thus further studies are required.

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Authors: Han, K., Mac Donald, C. L., Johnson, A. M., Barnes, Y., Wierzechowski, L., Zonies, D., Oh, J., Flaherty, S., Fang, R., Raichle, M. E., & Brody, D. L.
Affiliations: Washington University in St. Louis (US)
Landstuhl Regional Medical Center (DE)
Corresponding author: Brody, David L.
ORCID: Han, Kihwan
Zonies, David
Oh, John
Fang, Raymond
Raichle, Marcus E.
Brody, David L.
Venue: NeuroImage
Publisher: Elsevier BV
Published: 2014-01
Volume: 84
Pages: 76-96
ISSN: 1053-8119 (ISSN-L)
DOI: 10.1016/j.neuroimage.2013.08.017
PMC: PMC3849319
OpenAlex: W2012214808
Cited by: 123
References: 123
Citations by year: 2026: 4 · 2025: 4 · 2024: 5 · 2023: 11 · 2022: 11 · 2021: 7 · 2020: 8 · 2019: 7 · 2018: 13 · 2017: 13 · 2016: 16 · 2015: 15 · 2014: 8
FWCI: 7.13
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: NeuroImage (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Department of Defense CDMRP (PT075299, PT090444)
NCRR (1S10RR022984-01A1)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury Research
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
Keywords: blast-related traumatic brain injury, concussion, resting-state functional connectivity, participation coefficient, graph theory, military personnel, longitudinal follow-up, region of interest
MeSH terms: Adult, Blast Injuries, Brain Concussion, Brain Injuries, Cerebral Cortex, Humans, Male, Middle Aged, Military Personnel, Nerve Net, Neural Pathways, Rest, United States, Iraq War, 2003-2011, Young Adult, Afghan Campaign 2001-, Connectome

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Disrupted modular organization of resting-state cortical functional connectivity in U.S. military personnel following concussive ‘mild’ blast-related traumatic brain injury

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