The anatomical distance of functional connections predicts brain network topology in health and schizophrenia

Cerebral Cortex

Volumn 23, Issue 1, 2013, Pages 127-138

  Alexander Bloch, Aaron F ^a,b,c,d   Vértes, Petra E ^a   Stidd, Reva ^b   Lalonde, François ^b   Clasen, Liv ^b   Rapoport, Judith ^b   Giedd, Jay ^b   Bullmore, Edward T ^a   Gogtay, Nitin ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Cambridge Biomedical Campus ^*  (United Kingdom)

Author keywords

brain network; functional connectivity; graph theory; normal development; schizophrenia

Indexed keywords

ADULT; ARTICLE; ASSOCIATION CORTEX; BRAIN FUNCTION; BRAIN REGION; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; DISTANCE PERCEPTION; DORSAL PREFRONTAL CORTEX; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HUMAN; MALE; MEMBRANE STRUCTURE; NERVE CELL NETWORK; PARIETAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; SCHIZOPHRENIA; TEMPORAL CORTEX; VENTROMEDIAL PREFRONTAL CORTEX;

ADOLESCENT; BRAIN; BRAIN MAPPING; CONNECTOME; HUMANS; MALE; NERVE NET; NEURAL PATHWAYS; PROGNOSIS; REFERENCE VALUES; REPRODUCIBILITY OF RESULTS; SCHIZOPHRENIA; SENSITIVITY AND SPECIFICITY; STATISTICS AS TOPIC; YOUNG ADULT;

EID: 84870818294     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr388     Document Type: Article

References (71)

1. Achard S, Bullmore ET. 2007. Efficiency and cost of economical brain functional networks. PLoS Comput Biol. 3:e17
2. Alexander-Bloch AF, Gogtay N, Meunier D, Birn R, Clasen L, Lalonde F, Lenroot R, Giedd J, Bullmore ET. 2010. Disrupted modularity and local connectivity of brain functional networks in childhood-onset schizophrenia. Front Syst Neurosci. 4:147
3. Barthelemy M. 2011. Physics Reports 499:1-101.
4. Bassett DS, Bullmore ET, Meyer-Lindenberg A, Apud JA, Weinberger DR, Coppola R. 2009. Cognitive fitness of cost-efficient brain functional networks. Proc Natl Acad Sci USA. 106:11747-11752.
5. Bassett DS, Bullmore E, Verchinski BA, Mattay VS, Weinberger DR, Meyer-Lindenberg A. 2009. Hierarchical organization of human cortical networks in health and schizophrenia. J Neurosci. 28:9239-9248.
6. 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:e1000748
7. Bellec P, Perlbarg V, Jbabdi S, Pele grini-Issac M, Anton JL, Doyon J, Benali H. 2006. Identification of large-scale networks in the brain using fMRI. Neuroimage. 29:1231-1243.
8. Bullmore ET, Sporns O. 2009. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci. 10:1-13.
9. Bullmore ET, Bassett DS. 2011. Brain graphs: graphical models of the human brain connectome. Annu Rev Clin Psychol. 7:113-140.
10. Burgund ED, Kang HC, Kelly JE, Buckner RL, Snyder AZ, Petersen SE, Schlaggar BL. 2002. The feasibility of a common stereotactic space for children and adults in fMRI studies of development. Neuroimage. 17:184-200.
11. Chen BL, Hall DH, Chklovskii DB. 2006. Wiring optimization can relate neuronal structure and function. Proc Natl Acad Sci USA. 103:4723-4728.
12. Cherniak C, Mokhtarzada Z, Rodriguez-Esteban R, Changizi K. 2004. Global optimization of cerebral cortex layout. Proc Natl Acad Sci USA. 101:1081-1086.
13. Chklovskii DB. 2004. Synaptic connectivity and neuronal morphology: two sides of the same coin. Neuron. 43:609-617.
14. Cox RW. 1996. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res. 29:162-173.
15. Csardi G, Nepusz T. 2006. The igraph software package for complex network research. InterJ Complex Syst. 1695.
16. Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N. 2009. A probabilistic MR atlas of the human cerebellum. Neuroimage. 46:39-46.
17. Fair DA, Cohen AL, Power JD, Dosenbach NU, Church JA, Miezin FM, Schlaggar BL, Petersen SE. 2009. Functional brainnetworks develop from a "local to distributed" organization. PLoS Comput Biol. 5:e1000381.
18. Ellison-Wright I, Bullmore E. 2009. Meta-analysis of diffusion tensor imaging studies in schizophrenia. Schizophr Res. 108:3-10.
19. Erdos P, Renyi A 1959. On random graphs I. Publicationes Mathematicae 6, 290-297.
20. Feinberg I. 1982. Schizophrenia and late maturational brain changes in man. Psychopharmacol Bull. 18:29-31.
21. Feinberg I. 1983. Schizophrenia: caused by a fault in programmed synaptic elimination during adolescence J Psychiatr Res. 17:319-334.
22. Feinberg I, Campbell IG. 2010. Sleep EEG changes during adolescence: an index of a fundamental brain reorganization. Brain Cogn. 72: 56-65.
23. 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
24. Fornito A, Zalesky A, Bassett DS, Meunier D, Ellison-Wright I, Yucel M, Wood SJ, Shaw K, O'Connor J, Nertney D, et al. 2011. Genetic influences on cost-efficient organization of human cortical functional networks. J Neurosci. 31:3261-3270.
25. Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF 3rd, Herman DH, Clasen LS, Toga AW, et al. 2004. Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA. 101:8174-8179.
26. Guimerà R, Amaral LAN. 2005. Functional cartography of complex metabolic networks. Nature. 433:895-900.
27. Harrison PJ. 1999. The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain. 122:593-624.
28. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O. 2008. Mapping the structural core of human cerebral cortex. PLoS Biol. 6:e159.
29. He Y, Evans AC. 2010. Graph theoretical modeling of brain connectivity. Curr Opin Neurol. 23:341-350.
30. Heinrichs RW, Zakzanis KK. 1998. Neurocognitive deficit in schizophrenia: a quantitative review of the evidence. Neuropsychology. 12:426-445.
31. Honey CJ, Kotter R, Breakspear M, Sporns O. 2007. Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc Natl Acad Sci USA. 104:10240-10245.
32. Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, Meuli R, Hagmann P. 2009. Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci USA. 106:2035-2040.
33. Jenkinson M, Smith S. 2001. A global optimisation method for robust affine registration of brain images. Med Image Anal. 5:143-156.
34. Jenkinson M, Bannister P, Brady M, Smith S. 2002. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 17:825-884.
35. Kaiser M. 2011. A tutorial in connectome analysis: topological and spatial features of brain networks. Neuroimage. 57:892-907.
36. Kaiser M, Hilgetag CC. 2004. Spatial growth of real-world networks. Phys Rev E Stat Nonlin Soft Matter Phys. 69:036103.
37. Kaiser M, Hilgetag CC. 2006. Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput Biol. 2:e95.
38. Kaiser M, Hilgetag CC, van Ooyen A. 2009. A simple rule for axon outgrowth and synaptic competition generates realistic connection lengths and filling fractions. Cereb Cortex. 19:3001-3010.
39. Kang HC, Burgund ED, Lugar HM, Petersen SE, Schlaggar BL. 2003. Comparison of functional activation foci in children and adults using a common stereotactic space. Neuroimage. 19:16-28.
40. Keshavan MS, Anderson S, Pettegrew JW. 1994. Is schizophrenia due to excessive synaptic pruning in the prefrontal cortex? The Feinberg hypothesis revisited. J Psychiatr Res. 28:239-265.
41. Latora V, Marchiori M. 2001. Efficient behavior of small-world networks. Phys Rev Lett. 87:198701.
42. Lee KH, Williams LM, Breakspear M, Gordon E. 2003. Synchronous gamma activity: a review and contribution to an integrative neuroscience model of schizophrenia. Brain Res Brain Res Rev. 41:57-78.
43. Li Y, Liu Y, Li J, Qin W, Li K, Yu C, et al. 2009. Brain anatomical network and intelligence. PLoS Comput Biol. 5:e1000395.
44. Liu Y, Liang M, Zhou Y, He Y, Hao Y, Song M, Yu C, Liu H, Liu Z, Jiang T. 2008. Disrupted small-world networks in schizophrenia. Brain. 131:945-961.
45. Lynall ME, Bassett DS, Kerwin R, McKenna PJ, Kitzbichler M, Muller U, Bullmore E. 2010. Functional connectivity and brain networks in schizophrenia. J Neurosci. 30:9477-9487.
46. McGlashan TH, Hoffman RE. 2000. Schizophrenia as a disorder of developmentally reduced synaptic connectivity. Arch Gen Psychiatry. 57:637-648.
47. Meunier D, Achard S, Morcom A, Bullmore ET. 2009. Age-related changes in modular organization of human brain functional networks. Neuroimage. 44:715-723.
48. Meunier D, Lambiotte R, Bullmore ET. 2010. Modular and hierarchically modular organization of brain networks. Front Neurosci. 4:200.
49. Newman MEJ, Girvan M. 2004. Finding and evaluating community structure in networks. Phys Rev E Stat Nonlin Soft Matter Phys. 69: 026113.
50. Ramo n y Cajal S. 1899. Texture of the nervous system of man and vertebrates. Madrid (Spain): Nicolas Moya.
51. Rapoport JL, Addington AM, Frangou S, Psych MRC. 2005. The neurodevelopmental model of schizophrenia: update 2005. Mol Psychiatry. 10:434-449.
52. Rubinov M, Knock SA, Stam CJ, Micheloyannis S, Harris AW, Williams LM, et al. 2009. Small-world properties of nonlinear brain activity in schizophrenia. Hum Brain Mapp. 30:403-416.
53. Sepulcre J, Liu H, Talukdar T, Martincorena I, Yeo BT, Buckner RL. 2010. The organization of local and distant functional connectivity in the human brain. PLoS Comput Biol. 6:e1000808.
54. Salvador R, Martínez A, Pomarol-Clotet E, Gomar J, Vila F, Sarro S, Capdevila A, Bullmore E. 2008. A simple view of the brain through a frequency-specific functional connectivity measure. Neuroimage. 39:279-289.
55. Salvador R, Suckling J, Coleman MR, Pickard JD, Menon D, Bullmore E. 2005. Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb Cortex. 15:1332-1342.
56. Spencer KM, Nestor PG, Perlmutter R, Niznikiewicz MA, Klump MC, Frumin M, Shenton ME, McCarley RW. 2004. Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc Natl Acad Sci USA. 101:17288-17293.
57. Sporns O. 2010. Networks of the brain. Cambridge (MA): MIT Press.
58. Sporns O. 2011. The non-random brain: efficiency, economy, and complex dynamics. Front Comput Neurosci. 5:5.
59. Symond MP, Harris AW, Gordon E, Williams LM. 2005. "Gamma synchrony" in first-episode schizophrenia: a disorder of temporal connectivity? Am J Psychiatry. 162(3):459-465.
60. Stephan KE, Baldeweg T, Friston KJ. 2006. Synpatic plasticity and dysconnection in schizophrenia. Biol Psychiatry. 59:929-939.
61. Stephan KE, Friston KJ, Frith CD. 2009. Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophr Bull. 35(3):509-527.
62. Supekar K, Musen M, Menon V. 2009. Development of large-scale functional brain networks in children. PLoS Biol. 7:e1000157.
63. Viger F, Latapy M. 2005. Efficient and simple generation of random simple connected graphs with prescribed degree sequence. In: Wang L, editor. Computing and combinatorics. Lecture notes in computer science. Vol. 3595. Berlin: Springer. p. 440-449.
64. Van den Heuvel MP, Stam CJ, Kahn RS, Hulshoff Pol HE. 2009. Efficiency of functional brain networks and intellectual performance. J Neurosci. 29:7619-7624.
65. Van den Heuvel MP, Mandl RCW, Stam CJ, Kahn RS, Pol HEH. 2010. Aberrant frontal and temporal complex network structure in schizophrenia: a graph theoretical analysis. J Neurosci. 30:15915-15926.
66. Van den Heuvel MP, Sporns O. 2011. Rich club organization of the human connectome. J Neurosci. 31(44):15775-15786.
67. Van Essen DC. 1997. A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature. 385:313-318.
68. Varier S, Kaiser M. 2011. Neural development features: spatio-temporal development of the Caenorhabditis elegans neuronal network. PLoS Comput Biol. 7:e1001044.
69. Watts DJ, Strogatz SH. 1998. Collective dynamics of 'small-world' networks. Nature. 393:440-442.
70. Wickham H. 2009. ggplot2: elegant graphics for data analysis. New York: Springer.
71. Zalesky A, Fornito A, Seal ML, Cocchi L, Westin CF, Bullmore ET, Egan GF, Pantelis C. 2011. Disrupted axonal fiber connectivity in schizophrenia. Biol Psychiatry. 69:80-89.