Network community structure and resilience to localized damage: application to brain microcirculation

In cerebrovascular networks, some vertices are more connected to each other than with the rest of the vasculature, defining a community structure. Here, we introduce a class of model networks built by rewiring Random Regular Graphs, which enables reproduction of this community structure and other topological properties of cerebrovascular networks. We use these model networks to study the global flow reduction induced by the removal of a single edge. We analytically show that this global flow reduction can be expressed as a function of the initial flow rate in the removed edge and of a topological quantity, both of which display probability distributions following Cauchy laws, i.e. with large tails. As a result, we show that the distribution of blood flow reductions is strongly influenced by the community structure. In particular, the probability of large flow reductions increases substantially when the community structure is stronger, weakening the network resilience to single capillary occlusions. We discuss the implications of these findings in the context of Alzheimer’s Disease, in which the importance of vascular mechanisms, including capillary occlusions, is beginning to be uncovered.

[1]  P. Erdos,et al.  On the evolution of random graphs , 1984 .

[2]  C. Lee Giles,et al.  Self-Organization and Identification of Web Communities , 2002, Computer.

[3]  Allen J. Wood,et al.  Power Generation, Operation, and Control , 1984 .

[4]  Marc Timme,et al.  Network susceptibilities: Theory and applications. , 2016, Physical review. E.

[5]  A. Luft,et al.  Neutrophils Obstructing Brain Capillaries Are a Major Cause of No-Reflow in Ischemic Stroke. , 2020, Cell reports.

[6]  David Kleinfeld,et al.  Penetrating arterioles are a bottleneck in the perfusion of neocortex , 2007, Proceedings of the National Academy of Sciences.

[7]  Claudio Castellano,et al.  Community Structure in Graphs , 2007, Encyclopedia of Complexity and Systems Science.

[8]  Ajay Mehra The Development of Social Network Analysis: A Study in the Sociology of Science , 2005 .

[9]  G M Collins,et al.  Blood flow in the microcirculation. , 1966, Pacific medicine and surgery.

[10]  Nicholas C. Wormald,et al.  The asymptotic connectivity of labelled regular graphs , 1981, J. Comb. Theory B.

[11]  Sergey N. Dorogovtsev,et al.  Principles of statistical mechanics of random networks , 2002, ArXiv.

[12]  P. Anderson,et al.  A selfconsistent theory of localization , 1973 .

[13]  Marco Pellegrini,et al.  Extraction and classification of dense communities in the web , 2007, WWW '07.

[14]  Nozomi Nishimura,et al.  Occlusion of cortical ascending venules causes blood flow decreases, reversals in flow direction, and vessel dilation in upstream capillaries , 2011, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[15]  Myriam Peyrounette,et al.  Neutrophil adhesion in brain capillaries reduces cortical blood flow and impairs memory function in Alzheimer’s disease mouse models , 2018, Nature Neuroscience.

[16]  Timothy W. Secomb,et al.  Blood Flow in the Microcirculation , 2017 .

[17]  N. Michalski,et al.  Mapping the Fine-Scale Organization and Plasticity of the Brain Vasculature , 2020, Cell.

[18]  Kristie B. Hadden,et al.  2020 , 2020, Journal of Surgical Orthopaedic Advances.

[19]  A. Hudetz,et al.  Percolation phenomenon: the effect of capillary network rarefaction. , 1993, Microvascular research.

[20]  D. Attwell,et al.  Amyloid β oligomers constrict human capillaries in Alzheimer’s disease via signaling to pericytes , 2019, Science.

[21]  D. Kleinfeld,et al.  Correlations of Neuronal and Microvascular Densities in Murine Cortex Revealed by Direct Counting and Colocalization of Nuclei and Vessels , 2009, The Journal of Neuroscience.

[22]  蕭瓊瑞撰述,et al.  2009 , 2019, The Winning Cars of the Indianapolis 500.

[23]  M. Fiedler Algebraic connectivity of graphs , 1973 .

[24]  Shilpa Chakravartula,et al.  Complex Networks: Structure and Dynamics , 2014 .

[25]  M. Manole,et al.  Cerebral Hypoperfusion and Other Shared Brain Pathologies in Ischemic Stroke and Alzheimer’s Disease , 2017, Translational Stroke Research.

[26]  David Kleinfeld,et al.  The smallest stroke: occlusion of one penetrating vessel leads to infarction and a cognitive deficit , 2012, Nature Neuroscience.

[27]  V.E.Kravtsov,et al.  Non-ergodic delocalized phase in Anderson model on Bethe lattice and regular graph , 2017, 1712.00614.

[28]  S. Kirkpatrick Percolation and Conduction , 1973 .

[29]  Santo Fortunato,et al.  Community detection in graphs , 2009, ArXiv.

[30]  D. Kleinfeld,et al.  Targeted insult to subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke , 2006, Nature Methods.

[31]  C. Iadecola,et al.  The Pathobiology of Vascular Dementia , 2013, Neuron.

[32]  A. Pries,et al.  Biophysical aspects of blood flow in the microvasculature. , 1996, Cardiovascular research.

[33]  Sylvie Lorthois,et al.  During vertebrate development, arteries exert a morphological control over the venous pattern through physical factors. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[34]  Van H. Vu,et al.  Generating Random Regular Graphs , 2003, STOC '03.

[35]  C. Pozrikidis On the performance of damaged linear networks , 2012 .

[36]  Albert-László Barabási,et al.  Statistical mechanics of complex networks , 2001, ArXiv.

[37]  M. D’Esposito,et al.  Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging , 2003, Nature Reviews Neuroscience.

[38]  D. Kleinfeld,et al.  Two-Photon Microscopy as a Tool to Study Blood Flow and Neurovascular Coupling in the Rodent Brain , 2012, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[39]  N. Wormald Models of random regular graphs , 2010 .

[40]  Frank Winkler,et al.  Glioblastoma multiforme restructures the topological connectivity of cerebrovascular networks , 2019, Scientific Reports.

[41]  D. Kleinfeld,et al.  The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow , 2013, Nature Neuroscience.

[42]  Alan M. Frieze,et al.  Random graphs , 2006, SODA '06.

[43]  V. Latora,et al.  Complex networks: Structure and dynamics , 2006 .

[44]  Eric W. Weisstein,et al.  The CRC concise encyclopedia of mathematics , 1999 .

[45]  M E J Newman,et al.  Finding and evaluating community structure in networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[46]  B. Weber,et al.  The severity of microstrokes depends on local vascular topology and baseline perfusion , 2020, bioRxiv.

[47]  Norbert Schuff,et al.  Early role of vascular dysregulation on late-onset Alzheimer's disease based on multifactorial data-driven analysis , 2016, Nature Communications.

[48]  J. Whitwell,et al.  Alzheimer's disease neuroimaging , 2018, Current opinion in neurology.

[49]  E. Bogomolny,et al.  Calculation of mean spectral density for statistically uniform treelike random models. , 2013, Physical review. E, Statistical, nonlinear, and soft matter physics.

[50]  S. N. Dorogovtsev,et al.  Evolution of networks , 2001, cond-mat/0106144.

[51]  D. Attwell,et al.  Cerebral blood flow decrease as an early pathological mechanism in Alzheimer's disease , 2020, Acta Neuropathologica.

[52]  S. N. Dorogovtsev,et al.  Spectra of complex networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[53]  C. Iadecola The overlap between neurodegenerative and vascular factors in the pathogenesis of dementia , 2010, Acta Neuropathologica.

[54]  C. Iadecola,et al.  Alzheimer’s Disease and Vascular Aging , 2020, Journal of the American College of Cardiology.

[55]  Myriam Peyrounette,et al.  Brain Capillary Networks Across Species: A few Simple Organizational Requirements Are Sufficient to Reproduce Both Structure and Function , 2019, Front. Physiol..

[56]  Sylvie Lorthois,et al.  Fractal analysis of vascular networks: insights from morphogenesis. , 2010, Journal of theoretical biology.

[57]  Albert,et al.  Topology of evolving networks: local events and universality , 2000, Physical review letters.

[58]  Albert,et al.  Emergence of scaling in random networks , 1999, Science.

[59]  L. Ioffe,et al.  Non-ergodic delocalized phase in Anderson model on Bethe lattice and regular graph , 2017 .

[60]  Eleni Katifori,et al.  Resilience in hierarchical fluid flow networks. , 2018, Physical review. E.

[61]  J. V. Rauff,et al.  Introduction to Mathematical Sociology , 2012 .

[62]  Lisa J. Mellander,et al.  Robust and Fragile Aspects of Cortical Blood Flow in Relation to the Underlying Angioarchitecture , 2015, Microcirculation.