Cited by 1,165Functional Brain Connectivity StudiesComplex Network Analysis TechniquesAdvanced Neuroimaging Techniques and Applications

Identification and classification of hubs in brain networks

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Sporns, Olaf, Honey, Christopher J., Kötter, Rolf·2007·PLoS ONE

Abstract

Brain regions in the mammalian cerebral cortex are linked by a complex network of fiber bundles. These inter-regional networks have previously been analyzed in terms of their node degree, structural motif, path length and clustering coefficient distributions. In this paper we focus on the identification and classification of hub regions, which are thought to play pivotal roles in the coordination of information flow. We identify hubs and characterize their network contributions by examining motif fingerprints and centrality indices for all regions within the cerebral cortices of both the cat and the macaque. Motif fingerprints capture the statistics of local connection patterns, while measures of centrality identify regions that lie on many of the shortest paths between parts of the network. Within both cat and macaque networks, we find that a combination of degree, motif participation, betweenness centrality and closeness centrality allows for reliable identification of hub regions, many of which have previously been functionally classified as polysensory or multimodal. We then classify hubs as either provincial (intra-cluster) hubs or connector (inter-cluster) hubs, and proceed to show that lesioning hubs of each type from the network produces opposite effects on the small-world index. Our study presents an approach to the identification and classification of putative hub regions in brain networks on the basis of multiple network attributes and charts potential links between the structural embedding of such regions and their functional roles.

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  1. [2]Scannell JW Burns GAPC Hilgetag CC O'Neil MA Young MP 1999 The connectional organization of the cortico-thalamic system of the cat. Cereb Cortex 9 277 299 10355908
  2. [3]Lewis JW Van Essen DC 2000 Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipital cortex. J Comp Neurol 428 79 111 11058226
  3. [4]Sporns O Chialvo D Kaiser M Hilgetag CC 2004 Organization, development and function of complex brain networks. Trends Cogn Sci 8 418 425 15350243
  4. [6]Hilgetag CC Kötter R Stephan KE Sporns O 2002 Computational methods for the analysis of brain connectivity. Ascoli GA Computational Neuroanatomy–Principles and Methods Totowa Humana Press 295 335
  5. [7]Hilgetag CC Burns GAPC O'Neill MA Scannell JW Young MP 2000 Anatomical connectivity defines the organization of clusters of cortical areas in the macaque monkey and the cat. Phil Trans R Soc Lond B 355 91 110 10703046 PMC1692723
  6. [8]Sporns O Tononi G Edelman GM 2000 Theoretical neuroanatomy: Relating anatomical and functional connectivity in graphs and cortical connection matrices. Cereb Cortex 10 127 141 10667981
  7. [9]Stephan KE Hilgetag CC Burns GAPC O'Neill MA Young MP 2000 Computational analysis of functional connectivity between areas of primate cerebral cortex. Phil Trans Roy Soc Lond B 355 111 126 10703047 PMC1692715
  8. [10]Sporns O Zwi J 2004 The small world of the cerebral cortex. Neuroinformatics 2 145 162 15319512
  9. [11]Bassett DS Bullmore E 2006 Small-world brain networks. The Neuroscientist 12 512 523 17079517
  10. [12]Tononi G Edelman GM Sporns O 1998 Complexity and coherency: Integrating information in the brain. Trends Cogn Sci 2 474 484 21227298
  11. [14]Sporns O 2006 Small-world connectivity, motif composition, and complexity of fractal neuronal connections. BioSystems 85 55 64 16757100
  12. [15]Kaiser M Hilgetag CC 2006 Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput. Biol. 2 805 815 PMC1513269 16848638
  13. [16]Buzsaki G Geisler C Henze DA Wang XJ 2004 Interneuron diversity series: Circuit complexity and axon wiring economy of cortical interneurons. Trends Neurosci 27 186 193 15046877
  14. [17]Masuda N Aihara K 2004 Global and local synchrony of coupled neurons in small-world networks. Biol. Cybern 90 302 309 15085349
  15. [19]Kötter R Stephan KE 2003 Network participation indices: Characterizing component roles for information processing in neural networks. Neural Networks 16 1261 1275 14622883
  16. [20]Sporns O Kötter R 2004 Motifs in brain networks. PLoS Biology 2 1910 1918 PMC524253 15510229
  17. [21]Achard S Salvador R Whitcher B Suckling J Bullmore E 2006 A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci 26 63 72 16399673 PMC6674299
  18. [24]Honey CJ Kötter R Breakspear M Sporns O 2007 Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc Natl Acad Sci U S A 104 10240 10245 17548818 PMC1891224
  19. [25]Milo R Shen-Orr S Itzkovitz S Kashtan N Chklovskii D 2002 Network motifs: simple building blocks of complex networks. Science 298 824 827 12399590
  20. [26]Milo R Itzkovitz S Kashtan N Levitt R Shen-Orr S 2004 Superfamilies of evolved and designed networks. Science 303 1538 1542 15001784
  21. [29]Stephan KE Kamper L Bozkurt A Burns GA Young MP 2001 Advanced database methodology for the collation of the connectivity data on the macaque brain (CoCoMac). Philos Trans R Soc Lond B Biol Sci. 356 1159 1186 11545697 PMC1088509
  22. [30]Kötter R 2004 Online retrieval, processing, and visualization of primate connectivity data from the CoCoMac database. Neuroinformatics 2 127 144 15319511
  23. [31]Kötter R Wanke E 2005 Mapping brains without coordinates. Phil. Trans. R. Soc. Lond. B 360 751 766 15971361 PMC1569487
  24. [32]Van Essen DC Dickson J Harwell J Hanlon D Anderson CH 2001 An integrated software system for surface-based analyses of cerebral cortex. J Amer Med Inform Assoc 8 443 359 11522765 PMC131042
  25. [33]Watts DJ Strogatz SH 1998 Collective dynamics of ‘small-world’ networks. Nature 393 440 442 9623998
  26. [34]Humphries MD Gurney K Prescott TJ 2006 The brainstem reticular formation is a small-world, not scale-free, network. Proc Roy Soc B Biol Sci 273 503 511 PMC1560205 16615219
  27. [35]Maslov S Sneppen K 2002 Specificity and stability in topology of protein networks. Science 296 910 913 11988575
  28. [36]Artzy-Randrup Y Fleishman SJ Ben-Tal N Stone L 2004 Comment on “Network motifs: Simple building blocks of complex networks” and “Superfamilies of evolved and designed networks”. Science 305 1107c 15326338
  29. [39]Latora V Marchiori M 2001 Efficient behavior of small-world networks. Phys. Rev, Lett. 87 (19) 198701 198704 11690461
  30. [42]Guimera R Sales-Pardo M Amaral LAN 2007 Classes of complex networks defined by role-to-role connectivity profiles. Nature Physics 3 63 69 18618010 PMC2447920
  31. [43]Stein BE Meredith MA 1993 The merging of the senses. Cambridge MIT Press
  32. [44]Mesulam MM 1998 From sensation to cognition. Brain 121 1013 1052 9648540
  33. [45]Wallace MT Ramachandran R Stein BE 2004 A revised view of sensory cortical parcellation. Proc Natl Acad Sci U S A 101 2167 2172 14766982 PMC357070
  34. [46]Kaiser M Hilgetag CC 2004 Edge vulnerability in neural and metabolic networks. Biol Cybern 90 311 317 15221391
  35. [47]Kaiser M Robert M Andras P Young MP 2007 Simulation of robustness against lesions of cortical networks. Eur J Neurosci 25 3185 3192 17561832
  36. [48]Schiller PH Lee K 1991 The role of primate extrastriate area V4 in vision. Science 251 1251 1253 2006413
  37. [49]Schiller PH 1995 Effect of lesions in visual cortical area V4 on the recognition of transformed objects. Nature 376 342 344 7630401
  38. [50]De Weerd P Desimone R Ungerleider L 2003 Generalized deficits in visual selective attention after V4 and TEO lesions in macaques. Eur J. Neurosci. 18 1671 1691 14511346
  39. [51]Goldman-Rakic PS 1996 The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. Philos Trans R Soc Lond B Biol Sci 351 1445 1453 8941956
  40. [52]Quintana J Fuster JM 1999 From perception to action: temporal integrative functions of prefrontal and parietal neurons. Cereb Cortex. 9 213 221 10355901
  41. [53]Fuster JM 1997 The Prefrontal Cortex (Third Edition), Philadelphia Lippincott-Raven
  42. [54]Miller EK Cohen JD 2001 An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 24 167 202 11283309
  43. [55]Sakai K Rowe JB Passingham RE 2002 Active maintenance in prefrontal area 46 creates distractor-resistant memory. Nature Neurosci 5 479 484 11953754
  44. [56]Leon MI Shadlen MN 1999 Effect of expected reward magnitude on the response of neurons in the dorsolateral prefrontal cortex of the macaque. Neuron 24 415 425 10571234
  45. [57]Sommer MA Wurtz RH 2001 Frontal eye field sends delay activity related to movement, memory, and vision to the superior colliculus. J Neurophysiol 85 1673 1685 11287490
  46. [58]Vezoli J Falchier A Jouve B Knoblauch K Young M 2004 Quantitative analysis of connectivity in the visual cortex: Extracting function from structure. Neuroscientist 10 476 482 15359013
  47. [60]Heintz N 2004 Gene Expression Nervous System Atlas (GENSAT). Nature Neurosci 7 483 15114362
  48. [61]Wickersham IR Finke S Conzelmann KK Callaway EM 2007 Retrograde neuronal tracing with a deletion-mutant rabies virus. Nature Methods 4 47 49 17179932 PMC2755236
  49. [62]Dodt H-U Leischner U Schierloh A Jahrling N Mauch CP 2007 Ultramicroscopy: Three-dimensional visualization of neuronal networks in the whole mouse brain. Nature Methods 4 331 336 17384643
  50. [63]LeBihan D 2003 Looking into the functional architecture of the brain with diffusion MRI. Nature Rev Neurosci 4 469 480 12778119
  51. [64]Hagmann P Kurant M Gigandet X Thiran P Wedeen V 2007 Mapping networks of structural connectivity in the brain with diffusion MRI. PLoS ONE 2 e597 17611629 PMC1895920
  52. [65]Sporns O Tononi G Kötter R 2005 The human connectome: A structural description of the human brain. PLoS Comput Biol 1 245 251 PMC1239902 16201007
  53. [66]Kasthuri N Lichtman JW 2007 The rise of the ‘projectome’. Nature Methods 4 307 308 17396125
  54. [68]Itturia-Medina Y Canales-Rodriguez EJ Melia-Garcia L Valdes-Hernandez PA Martinez-Montes E 2007 Characterizing brain anatomical connections using diffusion weighted MRI and graph theory. NeuroImage 36 645 660 17466539

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Authors
Sporns, O., Honey, C. J., & Kötter, R.
Affiliations
  • Indiana University Bloomington (US)
  • Radboud University Medical Center (NL)
Corresponding author
Sporns, Olaf
Venue
PLoS ONE
Published
2007-10-17
Volume
2
Issue
10
Pages
e1049
ISSN
1932-6203 (ISSN-L)
OpenAlex
W2033078279
Cited by
1,165
References
8
Citations by year
2026: 40 · 2025: 48 · 2024: 42 · 2023: 58 · 2022: 78 · 2021: 65 · 2020: 78 · 2019: 64 · 2018: 77 · 2017: 79 · 2016: 89 · 2015: 78 · 2014: 91 · 2013: 71 · 2012: 74
FWCI
15.03
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Radboud Repository (Radboud University) (submittedVersion)
  • Radboud Repository (Radboud University) (submittedVersion, other-oa)
Funders
  • James S. McDonnell Foundation
  • Deutsche Forschungsgemeinschaft
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › Complex Network Analysis Techniques
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
Keywords
brain network hubs, cerebral cortex, structural connectivity, network centrality, betweenness centrality, closeness centrality, degree distribution, cats, macaque, lesion effects
MeSH terms
Algorithms, Animals, Brain, Brain Mapping, Cats, Cerebral Cortex, Computer Simulation, Macaca, Models, Anatomic, Models, Biological, Nerve Net, Neural Pathways, Species Specificity, Models, Statistical, Protein Interaction Mapping

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