Network diffusion model predicts neurodegeneration in limb-onset Amyotrophic Lateral Sclerosis

Journal article


Bhattarai, Anjan, Chen, Zhaolin, Chua, Phyllis, Talman, Paul, Mathers, Susan, Chapman, Caron, Howe, James, Lee, C. M. Sarah, Lie, Yenni, Poudel, Govinda R. and Egan, Gary F.. (2022). Network diffusion model predicts neurodegeneration in limb-onset Amyotrophic Lateral Sclerosis. PLoS ONE. 17(8), p. Article e0272736. https://doi.org/10.1371/journal.pone.0272736
AuthorsBhattarai, Anjan, Chen, Zhaolin, Chua, Phyllis, Talman, Paul, Mathers, Susan, Chapman, Caron, Howe, James, Lee, C. M. Sarah, Lie, Yenni, Poudel, Govinda R. and Egan, Gary F.
Abstract

Objective
Emerging evidences suggest that the trans-neural propagation of phosphorylated 43-kDa transactive response DNA-binding protein (pTDP-43) contributes to neurodegeneration in Amyotrophic Lateral Sclerosis (ALS). We investigated whether Network Diffusion Model (NDM), a biophysical model of spread of pathology via the brain connectome, could capture the severity and progression of neurodegeneration (atrophy) in ALS.

Methods
We measured degeneration in limb-onset ALS patients (n = 14 at baseline, 12 at 6-months, and 9 at 12 months) and controls (n = 12 at baseline) using FreeSurfer analysis on the structural T1-weighted Magnetic Resonance Imaging (MRI) data. The NDM was simulated on the canonical structural connectome from the IIT Human Brain Atlas. To determine whether NDM could predict the atrophy pattern in ALS, the accumulation of pathology modelled by NDM was correlated against atrophy measured using MRI. In order to investigate whether network spread on the brain connectome derived from healthy individuals were significant findings, we compared our findings against network spread simulated on random networks.

Results
The cross-sectional analyses revealed that the network diffusion seeded from the inferior frontal gyrus (pars triangularis and pars orbitalis) significantly predicts the atrophy pattern in ALS compared to controls. Whereas, atrophy over time with-in the ALS group was best predicted by seeding the network diffusion process from the inferior temporal gyrus at 6-month and caudal middle frontal gyrus at 12-month. Network spread simulated on the random networks showed that the findings using healthy brain connectomes are significantly different from null models.

Interpretation
Our findings suggest the involvement of extra-motor regions in seeding the spread of pathology in ALS. Importantly, NDM was able to recapitulate the dynamics of pathological progression in ALS. Understanding the spatial shifts in the seeds of degeneration over time can potentially inform further research in the design of disease modifying therapeutic interventions in ALS.

Year2022
JournalPLoS ONE
Journal citation17 (8), p. Article e0272736
PublisherPublic Library of Science
ISSN1932-6203
Digital Object Identifier (DOI)https://doi.org/10.1371/journal.pone.0272736
PubMed ID35951510
Scopus EID2-s2.0-85136339661
PubMed Central IDPMC9371353
Open accessPublished as ‘gold’ (paid) open access
Page range1-15
FunderMonash University
Australian Rotary Health
Rotary Club of Sandy Bay
Publisher's version
License
File Access Level
Open
Output statusPublished
Publication dates
Online11 Aug 2022
Publication process dates
Accepted25 Jul 2022
Deposited06 Dec 2022
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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