Genetic influences on cost-efficient organization of human cortical functional networks

Journal of Neuroscience

Volumn 31, Issue 9, 2011, Pages 3261-3270

  Fornito, Alex ^a,b   Zalesky, Andrew ^b   Bassett, Danielle S ^a,c   Meunier, David ^a   Ellison Wright, Ian ^a,d   Yücel, Murat ^b   Wood, Stephen J ^b,e   Shaw, Karen ^b   O'Connor, Jennifer ^b   Nertney, Deborah ^f   Mowry, Bryan J ^f   Pantelis, Christos ^b   Bullmore, Edward T ^a,g  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^d AVON AND WILTSHIRE MENTAL HEALTH PARTNERSHIP NHS TRUST   (United Kingdom)

^e UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^f UNIVERSITY OF QUEENSLAND   (Australia)

^g ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BOLD SIGNAL; BRAIN CORTEX; BRAIN FUNCTION; CONTROLLED STUDY; DIZYGOTIC TWINS; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEREDITY; HUMAN; HUMAN EXPERIMENT; MALE; MONOZYGOTIC TWINS; NORMAL HUMAN; OCCIPITAL LOBE; PARIETAL CORTEX; POSTERIOR CINGULATE; PREFRONTAL CORTEX; PRIORITY JOURNAL; TEMPORAL LOBE;

ADULT; BRAIN MAPPING; CEREBRAL CORTEX; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; TWINS, DIZYGOTIC; TWINS, MONOZYGOTIC; YOUNG ADULT;

EID: 79952274702     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4858-10.2011     Document Type: Article

References (73)

1. Achard S, Bullmore E (2007) Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3:e17.
2. 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. (Pubitemid 43090914)
3. Achard S, Bassett DS, Meyer-Lindenberg A, Bullmore E (2008) Fractal connectivity of long-memory networks. Phys Rev E Stat Nonlin Soft Matter Phys 77:036104.
4. Albert R, Barabási AL (2002) Statistical mechanics of complex networks. Rev Mod Phys 74:47-97.
5. Bassett DS, Bullmore E, Verchinski BA, Mattay VS, Weinberger DR, Meyer-Lindenberg A (2008) Hierarchical organization of human cortical networks in health and schizophrenia. J Neurosci 28:9239-9248.
6. 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 U S A 106:11747-11752.
7. 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.
8. Behzadi Y, Restom K, Liau J, Liu TT (2007) A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37:90-101. (Pubitemid 47068987)
9. Boomsma D, Busjahn A, Peltonen L (2002) Classical twin studies and beyond. Nat Rev Genet 3:872-882. (Pubitemid 35303519)
10. Bouchard TJ Jr (1998) Genetic and environmental influences on adult intelligence and special mental abilities. Hum Biol 70:257-279.
11. Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1-38. (Pubitemid 351506788)
12. Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, Hedden T, Andrews-Hanna JR, Sperling RA, Johnson KA (2009) Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J Neurosci 29:1860-1873.
13. Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186-198.
14. Bullmore ET, Suckling J, Overmeyer S, Rabe-Hesketh S, Taylor E, Brammer MJ (1999) Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans Med Imaging 18:32-42.
15. Bullmore E, Fadili J, Maxim V, Sendur L, Whitcher B, Suckling J, Brammer M, Breakspear M (2004) Wavelets and functional magnetic resonance imaging of the human brain. Neuroimage 23 [Suppl 1]:S234-S249.
16. Buzsáki G, Geisler C, Henze DA, Wang XJ (2004) Interneuron diversity series: circuit complexity and axon wiring economy of cortical interneurons. Trends in neurosciences 27:186-193. (Pubitemid 38376405)
17. Chen BL, Hall DH, Chklovskii DB (2006) Wiring optimization can relate neuronal structure and function. Proc Natl Acad Sci U S A 103:4723-4728.
18. Cherniak C, Mokhtarzada Z, Rodriguez-Esteban R, Changizi K (2004) Global optimization of cerebral cortex layout. Proc Natl Acad Sci U S A 101:1081-1086. (Pubitemid 38160587)
19. Chiang MC, Barysheva M, Shattuck DW, Lee AD, Madsen SK, Avedissian C, Klunder AD, Toga AW, McMahon KL, de Zubicaray GI, Wright MJ, Srivastava A, Balov N, Thompson PM (2009) Genetics of brain fiber architecture and intellectual performance. J Neurosci 29:2212-2224.
20. Chklovskii DB, Schikorski T, Stevens CF (2002) Wiring optimization in cortical circuits. Neuron 34:341-347. (Pubitemid 34465493)
21. Christian JC, Norton JA Jr, Sorbel J, Williams CJ (1995) Comparison of analysis of variance and maximum likelihood based path analysis of twin data: partitioning genetic and environmental sources of covariance. Genet Epidemiol 12:27-35.
22. Cole DM, Smith SM, Beckmann CF (2010) Advances and pitfalls in the analysis and interpretation of resting-state FMRI data. Front Syst Neurosci 4:8.
23. Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, Moritz CH, Quigley MA, Meyerand ME (2001) Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. AJNR Am J Neuroradiol 22:1326-1333.
24. Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179-194.
25. Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A 103:13848-13853. (Pubitemid 44413996)
26. Efron B (1987) Better bootstrap confidence intervals. J Am Stat Assoc 82:171-185.
27. Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195-207.
28. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341-355. (Pubitemid 34162530)
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.
30. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700-711. (Pubitemid 47283145)
31. Fox MD, Snyder AZ, Vincent JL, Raichle ME (2007) Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron 56:171-184. (Pubitemid 47484178)
32. Garrity AG, Pearlson GD, McKiernan K, Lloyd D, Kiehl KA, Calhoun VD (2007) Aberrant "default mode" functional connectivity in schizophrenia. Am J Psychiatry 164:450-457. (Pubitemid 46513159)
33. Glahn DC, Winkler AM, Kochunov P, Almasy L, Duggirala R, Carless MA, Curran JC, Olvera RL, Laird AR, Smith SM, Beckmann CF, Fox PT, Blangero J (2010) Genetic control over the resting brain. Proc Natl Acad Sci U S A 107:1223-1228.
34. Hagmann P, Kurant M, Gigandet X, Thiran P, Wedeen VJ, Meuli R, Thiran JP (2007) Mapping human whole-brain structural networks with diffusion MRI. PLoS ONE 2:e597.
35. 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.
36. Hayasaka S, Laurienti PJ (2010) Comparison of characteristics between region-and voxel-based network analyses in resting-state fMRI data. Neuroimage 50:499-508.
37. He BJ, Snyder AZ, Zempel JM, Smyth MD, Raichle ME (2008) Electrophysiological correlates of the brain's intrinsic large-scale functional architecture. Proc Natl Acad Sci U S A 105:16039-16044.
38. 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 U S A 106:2035-2040.
39. Humphries MD, Gurney K, Prescott TJ (2006) The brainstem reticular formation is a small-world, not scale-free, network. Proc Biol Sci 273:503-511. (Pubitemid 46780559)
40. Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143-156. (Pubitemid 35282800)
41. 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.
42. Koten JW Jr, Wood G, Hagoort P, Goebel R, Propping P, Willmes K, Boomsma DI (2009) Genetic contribution to variation in cognitive function: an FMRI study in twins. Science 323:1737-1740.
43. Latora V, Marchiori M (2001) Efficient behavior of small-world networks. Phys Rev Lett 87:198701.
44. Latora V, Marchiori M (2003) Economic small-world behavior in weighted networks. Eur Phys J B 32:249-263. (Pubitemid 41201142)
45. Laughlin SB, Sejnowski TJ (2003) Communication in neuronal networks. Science 301:1870-1874. (Pubitemid 37221384)
46. Li Y, Liu Y, Li J, Qin W, Li K, Yu C, Jiang T (2009) Brain anatomical network and intelligence. PLoS Comput Biol 5:e1000395.
47. Lowe MJ, Mock BJ, Sorenson JA (1998) Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 7:119-132. (Pubitemid 28355547)
48. Malinen S, Vartiainen N, Hlushchuk Y, Koskinen M, Ramkumar P, Forss N, Kalso E, Hari R (2010) Aberrant temporal and spatial brain activity during rest in patients with chronic pain. Proc Natl Acad Sci U S A 107:6493-6497.
49. Maslov S, Sneppen K (2002) Specificity and stability in topology of protein networks. Science 296:910-913. (Pubitemid 34464896)
50. McClearn GE, Johansson B, Berg S, Pedersen NL, Ahern F, Petrill SA, Plomin R (1997) Substantial genetic influence on cognitive abilities in twins 80 or more years old. Science 276:1560-1563. (Pubitemid 27255319)
51. Neale MC, Boker SM, Xie G, Maes HH (2003) Mx: statistical modeling. Box 980126 MCV, Richmond, VA 23298.
52. Newman MJE (2003) The structure and function of complex networks. SIAM Rev 45:167-256.
53. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1-25. (Pubitemid 34020610)
54. National Institute of Mental Health (1992) Family interview for genetic studies. Bethesda, MD: National Institute of Mental Health.
55. Peper JS, Brouwer RM, Boomsma DI, Kahn RS, Hulshoff Pol HE (2007) Genetic influences on human brain structure: a review of brain imaging studies in twins. Hum Brain Mapp 28:464-473. (Pubitemid 46849363)
56. Percival DB, Walden AT (2000) Wavelet methods for time series analysis. Cambridge, UK: Cambridge UP.
57. Poline JB, Worsley KJ, Evans AC, Friston KJ (1997) Combining spatial extent and peak intensity to test for activations in functional imaging. Neuroimage 5:83-96. (Pubitemid 27481515)
58. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci U S A 98:676-682. (Pubitemid 32105102)
59. Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059-1069.
60. Salvador R, Martínez A, Pomarol-Clotet E, Gomar J, Vila F, Sarró S, Capdevila A, Bullmore E (2008) Asimple view of the brain through a frequency-specific functional connectivity measure. Neuroimage 39:279-289. (Pubitemid 350110534)
61. Simon HA (1962) The architecture of complexity. Proc Am Philos Soc 106:467-482.
62. Skudlarski P, Jagannathan K, Calhoun VD, Hampson M, Skudlarska BA, Pearlson G (2008) Measuring brain connectivity: diffusion tensor imaging validates resting state temporal correlations. Neuroimage 43:554-561.
63. Smit DJ, Stam CJ, Posthuma D, Boomsma DI, de Geus EJ (2008) Heritability of "small-world" networks in the brain: a graph theoretical analysis of resting-state EEG functional connectivity. Hum Brain Mapp 29:1368-1378.
64. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci U S A 106:13040-13045.
65. The Psychological Corporation (2001) Wechsler test of adult reading: manual. San Antonio: The Psychological Corporation.
66. Thompson PM, Cannon TD, Narr KL, van Erp T, Poutanen V-P, Huttunen M, Lönnqvist J, Standertskjöld-Nordenstam CG, Kaprio J, Khaledy M, Dail R, Zoumalan CI, Toga AW (2001) Genetic influences on brain structure. Nat Neurosci 4:1253-1258. (Pubitemid 33135632)
67. van den Heuvel MP, Stam CJ, Boersma M, Hulshoff Pol HE (2008) Smallworld and scale-free organization of voxel-based resting-state functional connectivity in the human brain. Neuroimage 43:528-539.
68. 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.
69. Vincent JL, Patel GH, Fox MD, Snyder AZ, Baker JT, Van Essen DC, Zempel JM, Snyder LH, Corbetta M, Raichle ME (2007) Intrinsic functional architecture in the anaesthetized monkey brain. Nature 447:83-86. (Pubitemid 46685840)
70. Whitcher B, Guttorp P, Percival DB (2000) Wavelet analysis of covariance with application to atmospheric time series. J Geophys Res Atmos 105:14941-14962.
71. Zalesky A, Fornito A (2009) A DTI-derived measure of cortico-cortical connectivity. IEEE Trans Med Imaging 28:1023-1036.
72. Zalesky A, Fornito A, Harding IH, Cocchi L, Yücel M, Pantelis C, Bullmore ET (2010) Whole-brain anatomical networks: does the choice of nodes matter? Neuroimage 50:970-983.
73. 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.