journal article·2024-05-15Open access

Brain Network Modularity and Resilience Signaled by Betweenness Centrality Percolation Spiking

Parker Kotlarz, Marcelo Febo, Juan C. Nino, on behalf of the Alzheimer’s Disease Neuroimaging Initiative

Applied Sciences· Volume 14· Issue 10

Abstract

Modularity and resilience are fundamental properties of brain network organization and function. The interplay of these network characteristics is integral to understanding brain vulnerability, network efficiency, and neurocognitive disorders. One potential methodology to explore brain network modularity and resilience is through percolation theory, a sub-branch of graph theory that simulates lesions across brain networks. In this work, percolation theory is applied to connectivity matrices derived from functional MRI from human, mice, and null networks. Nodes, or regions, with the highest betweenness centrality, a graph theory quantifier that examines shortest paths, were sequentially removed from the network. This attack methodology led to a rapid fracturing of the network, resulting in two terminal modules connected by one transfer module. Additionally, preceding the rapid network fracturing, the average betweenness centrality of the network peaked in value, indicating a critical point in brain network functionality. Thus, this work introduces a methodological perspective to identify hubs within the brain based on critical points that can be used as an architectural framework for a neural network. By applying percolation theory to functional brain networks through a network phase-transition lens, network sub-modules are identified using local spikes in betweenness centrality as an indicator of brain criticality. This modularity phase transition provides supporting evidence of the brain functioning at a near-critical point while showcasing a formalism to understand the computational efficiency of the brain as a neural network.
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Research context

OpenAlex topics: Functional Brain Connectivity Studies · Neural dynamics and brain function · Advanced Neuroimaging Techniques and Applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Materials Science and Engineering, University of Florida, Gainesville, FL 32611, USA

Harvard Medical School, Harvard University, Boston, MA 02115, USA

Department of Psychiatry, University of Florida, Gainesville, FL 32611, USA

Funding

University of Florida · National Institute on Aging · National Institute of Biomedical Imaging and Bioengineering · Canadian Institutes of Health Research

References (66)

Show source-provided references
1. Milano, M., Guzzi, P.H., and Cannataro, M. (2019). Network building and analysis in connectomics studies: A review of algorithms, databases and technologies. Netw. Model. Anal. Health Inform. Bioinform., 8.10.1007/s13721-019-0192-6 ↗
2. Complex network measures of brain connectivity: Uses and interpretations10.1016/j.neuroimage.2009.10.003 ↗
3. Modularity and community structure in networks10.1073/pnas.0601602103 ↗
5. Dissociable default-mode subnetworks subserve childhood attention and cognitive flexibility: Evidence from deep learning and stereotactic electroencephalography10.1016/j.neunet.2023.07.019 ↗
6. Connectomic analysis of Alzheimer’s disease using percolation theory10.1162/netn_a_00221 ↗
7. Investigating the network consequences of focal brain lesions through comparisons of real and simulated lesions10.1038/s41598-021-81107-9 ↗
8. Early path dominance as a principle for neurodevelopment10.1073/pnas.2218007120 ↗
9. A Resilient, Low-Frequency, Small-World Human Brain Functional Network with Highly Connected Association Cortical Hubs10.1523/JNEUROSCI.3874-05.2006 ↗
10. Simulation of robustness against lesions of cortical networks10.1111/j.1460-9568.2007.05574.x ↗
11. Functional connectivity and brain networks in schizophrenia10.1523/JNEUROSCI.0333-10.2010 ↗
12. Modeling the outcome of structural disconnection on resting-state functional connectivity10.1016/j.neuroimage.2012.06.007 ↗
13. Joyce, K.E., Hayasaka, S., and Laurienti, P.J. (2013). The Human Functional Brain Network Demonstrates Structural and Dynamical Resilience to Targeted Attack. PLoS Comput. Biol., 9.10.1371/journal.pcbi.1002885 ↗
14. Percolation Analysis of Brain Structural Network10.3389/fphy.2021.698077 ↗
15. The unbalanced reorganization of weaker functional connections induces the altered brain network topology in schizophrenia10.1038/s41598-021-94825-x ↗
16. Computation at the edge of chaos: Phase transitions and emergent computation10.1016/0167-2789(90)90064-V ↗
17. Real-Time Computation at the Edge of Chaos in Recurrent Neural Networks10.1162/089976604323057443 ↗
18. Universal resilience patterns in complex networks10.1038/nature16948 ↗
19. Optimal resilience of modular interacting networks10.1073/pnas.1922831118 ↗
20. Resilience of the Internet to Random Breakdowns10.1103/PhysRevLett.85.4626 ↗
21. Brain networks under attack: Robustness properties and the impact of lesions10.1093/brain/aww194 ↗
22. A robust core architecture of functional brain networks supports topological resilience and cognitive performance in middle- and old-aged adults10.1073/pnas.2203682119 ↗
23. The hubs of the human connectome are generally implicated in the anatomy of brain disorders10.1093/brain/awu132 ↗
24. Neurite orientation dispersion and density imaging reveals white matter and hippocampal microstructure changes produced by Interleukin-6 in the TgCRND8 mouse model of amyloidosis10.1016/j.neuroimage.2019.116138 ↗
25. Age-related decline in white matter integrity in a mouse model of tauopathy: An in vivo diffusion tensor magnetic resonance imaging study10.1016/j.neurobiolaging.2013.12.009 ↗
26. AFNI: Software for Analysis and Visualization of Functional Magnetic Resonance Neuroimages10.1006/cbmr.1996.0014 ↗
27. Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images10.1006/nimg.2002.1132 ↗
28. Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration10.1016/j.neuroimage.2008.12.037 ↗
29. Local-Global Parcellation of the Human Cerebral Cortex from Intrinsic Functional Connectivity MRI10.1093/cercor/bhx179 ↗
30. Xia, M., Wang, J., and He, Y. (2013). BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics. PLoS ONE, 8.10.1371/journal.pone.0068910 ↗
31. Weight-conserving characterization of complex functional brain networks10.1016/j.neuroimage.2011.03.069 ↗
32. Null models in network neuroscience10.1038/s41583-022-00601-9 ↗
33. Hosseini, S.M.H., and Kesler, S.R. (2013). Influence of Choice of Null Network on Small-World Parameters of Structural Correlation Networks. PLoS ONE, 8.10.1371/journal.pone.0067354 ↗
35. Fornito, A., Zalesky, A., and Bullmore, E.T. (2016). Fundamentals of Brain Network Analysis, Academic Press.
36. Percolation in Living Neural Networks10.1103/PhysRevLett.97.188102 ↗
37. Percolation on networks with weak and heterogeneous dependency10.1103/PhysRevE.95.032301 ↗
38. Network Robustness and Fragility: Percolation on Random Graphs10.1103/PhysRevLett.85.5468 ↗
39. Percolation critical exponents in scale-free networks10.1103/PhysRevE.66.036113 ↗
40. Fisher, R.A. (1958). Statistical Methods for Research Workers, Hafner. [13th ed.]. Rev. in Biological monographs and manuals.
41. Kendall, M., and Stuart, A. (1979). The Advanced Theory of Statistics. Volume 2: Inference and Relationship, Macmillan. [4th ed.].
42. Press, W.H., Flannery, B.P., Teukolsky, S.A., and Vetterling, W.T. (1992). Numerical Recipes in C: The Art of Scientific Computing, Cambridge University Press. [2nd ed.].
43. Intensity and coherence of motifs in weighted complex networks10.1103/PhysRevE.71.065103 ↗
44. Collective dynamics of ‘small-world’ networks10.1038/30918 ↗
45. Newman, M.E.J. (2016). The New Palgrave Dictionary of Economics, Palgrave Macmillan.
46. Efficient Behavior of Small-World Networks10.1103/PhysRevLett.87.198701 ↗
47. Cartography of complex networks: Modules and universal roles
48. Centrality in social networks conceptual clarification10.1016/0378-8733(78)90021-7 ↗
49. Rich-club in the brain’s macrostructure: Insights from graph theoretical analysis10.1016/j.csbj.2020.06.039 ↗
50. Prominence and Control: The Weighted Rich-Club Effect10.1103/PhysRevLett.101.168702 ↗
51. Rich-Club Organization of the Human Connectome10.1523/JNEUROSCI.3539-11.2011 ↗
52. Influence maximization in complex networks through optimal percolation10.1038/nature14604 ↗
53. Collective Influence Algorithm to find influencers via optimal percolation in massively large social media10.1038/srep30062 ↗
54. Improved collective influence of finding most influential nodes based on disjoint-set reinsertion10.1038/s41598-018-32874-5 ↗
55. Hagmann, P., Cammoun, L., Gigandet, X., Meuli, R., Honey, C.J., Wedeen, V.J., and Sporns, O. (2008). Mapping the Structural Core of Human Cerebral Cortex. PLoS Biol., 6.10.1371/journal.pbio.0060159 ↗
56. How critical is brain criticality?10.1016/j.tins.2022.08.007 ↗
57. Why Brain Criticality Is Clinically Relevant: A Scoping Review10.3389/fncir.2020.00054 ↗
58. Evidence for Quasicritical Brain Dynamics10.1103/PhysRevLett.126.098101 ↗
59. Ising-like dynamics in large-scale functional brain networks10.1103/PhysRevE.79.061922 ↗
60. Stability of neuronal avalanches and long-range temporal correlations during the first year of life in human infants10.1007/s00429-019-02014-4 ↗
61. Learning function from structure in neuromorphic networks10.1038/s42256-021-00376-1 ↗
62. Parker, T.S., and Chua, L.O. (1989). Practical Numerical Algorithms for Chaotic Systems, Springer.10.1007/978-1-4612-3486-9 ↗
63. Cognitive task information is transferred between brain regions via resting-state network topology10.1038/s41467-017-01000-w ↗
64. Constructing neural network models from brain data reveals representational transformations linked to adaptive behavior10.1038/s41467-022-28323-7 ↗
65. Connectome-based reservoir computing with the conn2res toolbox10.1038/s41467-024-44900-4 ↗
66. Using connectomics for predictive assessment of brain parcellations10.1016/j.neuroimage.2021.118170 ↗