Influence of Wiring Cost on the Large-Scale Architecture of Human Cortical Connectivity

PLoS Computational Biology

Volumn 10, Issue 4, 2014, Pages

  Samu, David ^a   Seth, Anil K ^a   Nowotny, Thomas ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

STRUCTURAL PROPERTIES; TOPOLOGY;

BRAIN FUNCTIONS; CORTICAL NETWORK; FUNDAMENTAL PROPERTIES; HIERARCHICAL ORGANIZATIONS; HIGH RESOLUTION; LARGE-SCALES; LIMITED SPACE; MODULAR ORGANIZATIONS; SMALL WORLDS; SPATIAL CONSTRAINTS;

BRAIN;

ARTICLE; BRAIN CORTEX; BRAIN FUNCTION; COGNITION; CONNECTOME; CONSCIOUSNESS; CORTICAL CONNECTIVITY; ECONOMIC ASPECT; HUMAN; LARGE SCALE PRODUCTION; MEMBRANE STRUCTURE; NUCLEAR MAGNETIC RESONANCE IMAGING; WHITE MATTER; BIOLOGICAL MODEL; CLUSTER ANALYSIS; PHYSIOLOGY; VALIDATION STUDY;

CEREBRAL CORTEX; CLUSTER ANALYSIS; HUMANS; MODELS, BIOLOGICAL;

EID: 84901357586     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003557     Document Type: Article

References (97)

1. Sporns O, Tononi G, Kötter R, (2005) The human connectome: A structural description of the human brain. PLoS Comput Biol pp. 1-4 doi:10.1371/journal.pcbi.0010042.
2. Sporns O (2010) Networks of the Brain. The MIT Press. 424p.
3. Bressler SL, Menon V, (2010) Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci 14 (6):: 277-90.
4. Conturo TE, Lori NF, Cull TS, Akbudak E, Snyder AZ, et al. (1999) Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci U S A 96 (18):: 10422-10427.
5. Mori S, Crain BJ, Chacko VP, van Zijl PC, (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45 (2):: 265-269.
6. Johansen-Berg H, Rushworth MF, (2009) Using diffusion imaging to study human connectional anatomy. Annu Rev Neurosci 32: 75-94.
7. Pan H, Epstein J, Silbersweig DA, Stern E, (2011) New and emerging imaging techniques for mapping brain circuitry. Brain Res Rev 67 (1-2):: 226-251.
8. Cammoun L, Gigandet X, Meskaldji D, Thiran JP, Sporns O, et al. (2012) Mapping the human connectome at multiple scales with diffusion spectrum MRI. J Neurosci Methods 203 (2):: 386-397.
9. Sporns O, Tononi G, Edelman GM, (2000) Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices. Cereb Cortex 10 (2):: 127-141.
10. Bassett DS, Bullmore E, Verchinski BA, Mattay VS, Weinberger DR, et al. (2008) Hierarchical organisation of human cortical networks in health and schizophrenia. J Neurosci 28 (37):: 9239-9248.
11. Hilgetag CC, Burns GA, O'Neill MA, Scannell JW, Young MP, (2000) Anatomical connectivity defines the organisation of clusters of cortical areas in the macaque monkey and the cat. Philos Trans R Soc Lond B Biol Sci 355 (1393):: 91-110.
12. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, et al. (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6 (7), doi:10.1371/journal.pbio.0060159.
13. Van den Heuvel MP, Sporns O, (2011) Rich-club organisation of the human connectome. J Neurosci 31 (44):: 15775-15786.
14. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, et al. (2002) Network motifs: simple building blocks of complex networks. Science 298 (5594):: 824-827.
15. Rubinov M, Sporns O, (2010) Complex network measures of brain connectivity: Uses and interpretations. Neuroimage 52 (3):: 1059-69.
16. Boccaletti S, Latora V, Moreno Y, Chavez M, Hwang D, (2006) Complex networks: Structure and dynamics. Physics Reports 424 (4-5):: 175-308.
17. Zamora-López G, Zhou C, Kurths J, (2010) Cortical hubs form a module for multisensory integration on top of the hierarchy of cortical networks. Front Neuroinformatics 4: 1.
18. Bullmore E, Sporns O, (2012) The economy of brain network organization. Nat Rev Neurosci 13 (5):: 336-49.
19. Braitenberg V and Schuz A (1998) Cortex: Statistics and Geometry of Neuronal Connectivity. Springer-Verlag 2nd edition. 249p.
20. Sporns O, Kötter R, (2004) Motifs in Brain Networks. PLoS Biol 2 (11), doi:10.1371/journal.pbio.0020369.
21. Sporns O, (2006) Small-world connectivity, motif composition, and complexity of fractal neuronal connections. Biosystems 85 (1):: 55-64.
22. Sporns O, Honey CJ, Kötter R, (2007) Identification and classification of hubs in brain networks. PLoS One 2 (10), doi:10.1371/journal.pone.0001049.
23. Watts DJ, Strogatz SH, (1998) Collective dynamics of 'small-world' networks. Nature 393 (6684):: 440-442.
24. Echtermeyer C, Han CE, Rotarska-Jagiela A, Mohr H, Uhlhaas PJ, Kaiser M, (2011) Integrating temporal and spatial scales: human structural network motifs across age and region of interest size. Front Neuroinform 5: 10 doi:10.3389/fninf.2011.00010.
25. van den Heuvel MP, Kahn RS, Goñi J, Sporns O, (2012) High-cost, high-capacity backbone for global brain communication. Proc Natl Acad Sci U S A 109 (28):: 11372-7.
26. Cabral J, Hugues E, Sporns O, Deco G, (2011) Role of local network oscillations in resting-state functional connectivity. Neuroimage 57 (1):: 130-139.
27. Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, et al. (2009) Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci U S A 106 (6):: 2035-2040.
28. Shanahan M, Wildie M, (2012) Knotty-Centrality: Finding the Connective Core of a Complex Network. PLoS ONE 7 (5), doi:10.1371/journal.pone.0036579.
29. Fornito A, Zalesky A, Bullmore ET, (2010) Network scaling effects in graph analytic studies of human resting-state fmri data. Front Syst Neurosci 4: 22-22.
30. Zalesky A, Fornito A, Harding IH, Cocchi L, Yücel M, et al. (2010) Whole-brain anatomical networks: does the choice of nodes matter? Neuroimage 50 (3):: 970-983.
31. Maslov S, Sneppen K, (2002) Specificity and stability in topology of protein networks. Science 296 (5569):: 910-913.
32. Sørensen T, (1948) A method of establishing groups of equal amplitude in plant sociology based on similarity of species content. Kongelige Danske Videnskabernes Selskab Biol 4: 1-34.
33. Latora V, Marchiori M, (2001) Efficient behavior of small-world networks. Phys Rev Lett 87 (19):: 198701-198701.
34. Achard S, Bullmore E, (2007) Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3 (2), doi:10.1371/journal.pcbi.0030017.
35. Onnela JP, Saramäki J, Kertész J, Kaski K, (2005) Intensity and coherence of motifs in weighted complex networks. Phys Rev E Stat Nonlin Soft Matter Phys 71 (6 Pt 2), doi:10.1103/physreve.71.065103.
36. Sporns O, (2011) The non-random brain: efficiency, economy, and complex dynamics. Front Comput Neurosci 5: 5-5.
37. Humphries MD, Gurney K, (2008) Network 'small-world-ness': a quantitative method for determining canonical network equivalence. PLoS One 3 (4), doi:10.1371/journal.pone.0002051.
38. Ravasz E, Barabási AL, (2003) Hierarchical organisation in complex networks. Phys Rev E Stat Nonlin Soft Matter Phys 67 (2 Pt 2):: 026112-026112.
39. Newman ME, (2004) Fast algorithm for detecting community structure in networks. Phys Rev E Stat Nonlin Soft Matter Phys 69 (6 Pt 2):: 066133-066133.
40. Danon L, Díaz-Guilera A, Duch J, Arenas A, (2005) Comparing community structure identification. Journal of Statistical Mechanics: Theory and Experiment 2005 (09):: P09008.
41. Newman ME, (2006) Modularity and community structure in networks. Proc Natl Acad Sci U S A 103 (23):: 8577-8582.
42. Steen M, Hayasaka S, Joyce K, Laurienti P, (2011) Assessing the consistency of community structure in complex networks. Phys Rev E Stat Nonlin Soft Matter Phys Jul; 84 (1 Pt 2):: 016111.
43. Meila M, (2007) Comparing clusterings - an information based distance. J Multivar Anal 98 (5):: 873-895.
44. Karrer B, Levina E, Newman ME, (2008) Robustness of community structure in networks. Phys Rev E Stat Nonlin Soft Matter Phys 77 (4 Pt 2), doi:10.1103/physreve.77.046119.
45. Traud AL, Kelsic ED, Mucha PJ, Porter MA, (2011) Comparing Community Structure to Characteristics in Online Collegiate Social Networks. SIAM Review 53 (3):: 526-543.
46. Seidman SB, (1983) Network Structure and Minimum Degree. Social Networks 5: 269-287.
47. Zhou S, Mondragón RJ, (2004) The rich-club phenomenon in the internet topology. IEEE Comm Lett 8 (3):: 180-182.
48. Colizza V, Flammini A, Serrano MA, Vespignani A, (2006) Detecting rich-club ordering in complex networks. Nat Phys 2 (2):: 110-115.
49. Opsahl T, Colizza V, Panzarasa P, Ramasco JJ, (2008) Prominence and control: the weighted rich-club effect. Phys Rev Lett 101 (16):: 168702-16870 2.
50. Newman MEJ, (2002) Assortative mixing in networks. Phys Rev Lett 89 (20):: 208701.
51. Kaiser M, Hilgetag CC, (2006) Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput Biol 2 (7), doi:10.1371/journal.pcbi.0020095.
52. Ahn YY, Jeong H, Kim BJ, (2006) Wiring cost in the organization of a biological neuronal network. Physica A 367: 531-537.
53. Bassett DS, Greenfield DL, Meyer-Lindenberg A, Weinberger DR, Moore SW, Bullmore ET, (2010) Efficient physical embedding of topologically complex information processing networks in brains and computer circuits. PLoS Comput Biol 6 (4), doi:10.1371/journal.pcbi.1000748.
54. Chen Y, Wang S, Hilgetag CC, Zhou C, (2013) Trade-off between multiple constraints enables simultaneous formation of modules and hubs in neural systems. PLoS Comput Biol 9 (3), doi:10.1371/journal.pcbi.1002937.
55. Tononi G, Sporns O, Edelman GM, (1994) A measure for brain complexity: relating functional segregation and integration in the nervous system. Proc Natl Acad Sci USA 91 (11):: 5033-5037.
56. Humphries MD, Gurney K, Prescott TJ, (2006) The brainstem reticular formation is a small-world, not scale-free, network. Proceedings of the Royal Society B: Biological Sciences 273 (1585):: 503-511.
57. Sporns O, Honey CJ, (2006) Small worlds inside big brains. Proc Natl Acad Sci USA 103 (51):: 19219-19220.
58. Bassett DS, Bullmore E, (2006) Small-world brain networks. Neuroscientist 12 (6):: 512-523.
59. Kaiser M, Hilgetag CC, Kotter R, (2010) Hierarchy and dynamics of neural networks. Frontiers in Neuroinformatics 4 (0):: 112 doi:10.3389/fninf.2010.00112.
60. Newman MEJ, Girvan M, (2004) Finding and evaluating community structure in networks. Phys Rev E 69 (2):: 026113.
61. Simon HA (1962) The architecture of complexity. In Proceedings of the American Philosophical Society volume 106 pages 467-482.
62. Koch C, Laurent G, (1999) Complexity and the nervous system. Science 284 (5411):: 96-98.
63. Shanahan M, (2010) Metastable chimera states in community-structured oscillator networks. Chaos 20 (1):: 013108-013108.
64. Kaiser M, Goerner M, Hilgetag CC, (2008) Criticality of spreading dynamics in hierarchical cluster networks without inhibition. New Journal of Physics 9 (5):: 110-110.
65. Chen ZJ, He Y, Rosa-Neto P, Germann J, Evans AC, (2008) Revealing modular architecture of human brain structural networks by using cortical thickness from mri. Cereb Cortex 18 (10):: 2374-2381.
66. Valencia M, Pastor MA, Fernández-Seara MA, Artieda J, Martinerie J, et al. (2009) Complex modular structure of large-scale brain networks. Chaos 19 (2):: 023119-023119.
67. Meunier D, Lambiotte R, Fornito A, Ersche KD, Bullmore ET, (2009b) Hierarchical modularity in human brain functional networks. Front Neuroinform 3: 37-37.
68. He Y, Wang J, Wang L, Chen ZJ, Yan C, et al. (2009) Uncovering intrinsic modular organisation of spontaneous brain activity in humans. PLoS One 4 (4), doi:10.1371/journal.pone.0005226.
69. Meunier D, Achard S, Morcom A, Bullmore E, (2009a) Age-related changes in modular organisation of human brain functional networks. Neuroimage 44 (3):: 715-723.
70. Borgatti SP, Everett MG, (2000) Models of Core/Periphery Structures. Social Networks 21 (4):: 375-395.
71. Rossa FD, Dercole F, Piccardi C, (2013) Profiling core-periphery network structure by random walkers. Sci Rep 3: 1467.
72. Rombach MP, Porter MA, Fowler JH, Mucha PJ (2013) Core-Periphery Structure in Networks, submitted to SIAM Journal on Applied Mathematics, arXiv:1202.2684.
73. Zamora-López G, Zhou C, Kurths J, (2009) Graph analysis of cortical networks reveals complex anatomical communication substrate. Chaos 19 (1):: 015117-015117.
74. Gómez-Gardeñes J, Zamora-López G, Moreno Y, Arenas A, (2010) From modular to centralized organization of synchronization in functional areas of the cat cerebral cortex. PLoS One 5 (8), doi:10.1371/journal.pone.0012313.
75. Modha DS, Singh R, (2010) Network architecture of the long-distance pathways in the macaque brain. Proc Natl Acad Sci U S A 107 (30):: 13485-13490.
76. Kaiser M, Varier S, (2011) Evolution and development of brain networks: from Caenorhabditis elegans to Homo sapiens. Network 22 (1-4):: 143-7.
77. Sporns O, (2013) Network attributes for segregation and integration in the human brain. Curr Opin Neurobiol 23 (2):: 162-71.
78. Sporns O, (2013) The human connectome: Origins and challenges. NeuroImage 80: 53-61.
79. Baars BJ, (2002) The conscious access hypothesis: origins and recent evidence. Trends Cogn Sci 6 (1):: 47-52.
80. Tomasi D, Volkow ND, (2011) Association between functional connectivity hubs and brain networks. Cereb Cortex 21 (9):: 2003-13.
81. Tomasi D, Volkow ND, (2011) Functional connectivity hubs in the human brain. Neuroimage 57 (3):: 908-17.
82. Greicius MD, Supekar K, Menon V, Dougherty RF, (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19 (1):: 72-8.
83. Raichle ME, Snyder AZ, (2007) A default mode of brain function: a brief history of an evolving idea. Neuroimage 37 (4):: 1083-90.
84. Jbabdi S, Johansen-Berg H, (2011) Tractography: where do we go from here? Brain Connect 1 (3):: 169-183.
85. Sporns O, Chialvo DR, Kaiser M, Hilgetag CC, (2004) Organization, development and function of complex brain networks. Trends Cogn Sci 8 (9):: 418-25.
86. Van Essen DC, (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385 (6614):: 313-8.
87. Shanahan M, (2008) Dynamical complexity in small-world networks of spiking neurons. Phys Rev E Stat Nonlin Soft Matter Phys 78 (4 Pt 1), doi:10.1103/PhysRevE.78.041924.
88. Stam CJ, (2005) Nonlinear dynamical analysis of EEG and MEG: review of an emerging field. Clin Neurophysiol 116 (10):: 2266-301.
89. Seth AK, Barrett AB, Barnett L, (2011) Causal density and integrated information as measures of conscious level. Phil Trans R Soc A 369: 3748-3767.
90. Arthuis M, Valton L, Régis J, Chauvel P, Wendling F, et al. (2009) Impaired consciousness during temporal lobe seizures is related to increased long-distance cortical-subcortical synchronization. Brain 132 (Pt 8):: 2091-2101.
91. Bhowmik D, Shanahan M, (2013) Metastability and inter-band frequency modulation in networks of oscillating spiking neuron populations. PLoS One 8 (4), doi:10.1371/journal.pone.0062234.
92. Kaiser M, Hilgetag CC, (2010) Optimal hierarchical modular topologies for producing limited sustained activation of neural networks. Front Neuroinform 4: 8.
93. Kitzbichler MG, Smith ML, Christensen SR, Bullmore E, (2009) Broadband Criticality of Human Brain Network Synchronization. PLoS Comput Biol 5 (3), doi:10.1371/journal.pcbi.1000314.
94. Shanahan M, (2012) The brain's connective core and its role in animal cognition. Phil Trans Roy Soc B 367: 2704-2714.
95. Chklovskii DB, (2004) Synaptic connectivity and neuronal morphology: two sides of the same coin. Neuron 43: 609-617.
96. Rubinov M, Sporns O, van Leeuwen C, Breakspear M, (2009) Symbiotic relationship between brain structure and dynamics. BMC Neurosci 10: 55.
97. Holten D, (2006) Hierarchical edge bundles: visualization of adjacency relations in hierarchical data. IEEE Transactions on Visualization and Computer Graphics 12 (5):: 741-748.