Developmental changes in brain network hub connectivity in late adolescence

Journal of Neuroscience

Volumn 35, Issue 24, 2015, Pages 9078-9087

  Baker, Simon T E ^a,b   Lubman, Dan I ^a   Yücel, Murat ^a,b   Allen, Nicholas B ^c,d   Whittle, Sarah ^b   Fulcher, Ben D ^a   Zalesky, Andrew ^b,e   Fornito, Alex ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d THE NATIONAL CENTRE OF EXCELLENCE IN YOUTH MENTAL HEALTH   (Australia)

^e The University of Melbourne   (Australia)

Author keywords

Adolescence; Connectome; Development; Graph theory; MRI; Structural connectivity

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; BRAIN DEVELOPMENT; CAUDATE NUCLEUS; DIFFUSION WEIGHTED IMAGING; FEMALE; FOLLOW UP; FRONTAL CORTEX; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; INSULA; MALE; NERVE CELL NETWORK; NORMAL HUMAN; PARIETAL CORTEX; PRIORITY JOURNAL; PUTAMEN; SPATIAL ORIENTATION; TEMPORAL LOBE; THALAMUS; AGE; BRAIN; BRAIN MAPPING; CONNECTOME; DIFFUSION TENSOR IMAGING; GROWTH, DEVELOPMENT AND AGING; NERVE TRACT; PROCEDURES; YOUNG ADULT;

ADOLESCENT; AGE FACTORS; BRAIN; BRAIN MAPPING; CONNECTOME; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; MALE; NERVE NET; NEURAL PATHWAYS; YOUNG ADULT;

EID: 84931401338     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5043-14.2015     Document Type: Article

References (67)

1. Ahuja RK, Magnanti TL, Orlin JB (1993) Network flows: theory, algorithms, and applications. Upper Saddle River, NJ: Prentice Hall.
2. Ball G, Aljabar P, Zebari S, Tusor N, Arichi T, Merchant N, Robinson EC, Ogundipe E, Rueckert D, Edwards AD, Counsell SJ (2014) Rich-club organization of the newborn human brain. Proc Natl Acad Sci U S A 111:7456 -7461.
3. Benes FM, Turtle M, Khan Y, Farol P (1994) Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Arch Gen Psychiatry 51:477- 484.
4. Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186-198.
5. Colizza V, Flammini A, Serrano MA, Vespignani A (2006) Detecting richclub ordering in complex networks. Nat Phys 2:110 -115.
6. Crossley NA, Mechelli A, Scott J, Carletti F, Fox PT, McGuire P, Bullmore ET (2014) The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain 137:2382-2395.
7. Davey CG, Yücel M, Allen NB (2008) The emergence of depression in adolescence: development of the prefrontal cortex and the representation of reward. Neurosci Biobehav Rev 32:1-19.
8. Dennis EL, Jahanshad N, McMahon KL, de Zubicaray GI, Martin NG, Hickie IB, Toga AW, Wright MJ, Thompson PM (2013) Development of brain structural connectivity between ages 12 and 30: a 4-Tesla diffusion imaging study in 439 adolescents and adults. Neuroimage 64:671- 684.
9. de Reus MA, van den Heuvel MP (2013) Rich club organization and intermodule communication in the cat connectome. J Neurosci 33:12929-12939.
10. Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968-980.
11. Di Martino A, Fair DA, Kelly C, Satterthwaite TD, Castellanos FX, Thomason ME, Craddock RC, Luna B, Leventhal BL, Zuo XN, Milham MP (2014) Unraveling the miswired connectome: a developmental perspective. Neuron 83:1335-1353.
12. Dosenbach NU, Nardos B, Cohen AL, Fair DA, Power JD, Church JA, Nelson SM, Wig GS, Vogel AC, Lessov-Schlaggar CN, Barnes KA, Dubis JW, Feczko E, Coalson RS, Pruett JR Jr, Barch DM, Petersen SE, Schlaggar BL (2010) Prediction of individual brain maturity using fMRI. Science 329: 1358-1361.
13. Dwyer DB, Harrison BJ, Yücel M, Whittle S, Zalesky A, Pantelis C, Allen NB, Fornito A (2014) Large-scale brain network dynamics supporting adolescent cognitive control. J Neurosci 34:14096 -14107.
14. Fair DA, Dosenbach NU, Church JA, Cohen AL, Brahmbhatt S, Miezin FM, Barch DM, Raichle ME, Petersen SE, Schlaggar BL (2007) Development of distinct control networks through segregation and integration. Proc Natl Acad Sci U S A 104:13507-13512.
15. Fair DA, Cohen AL, Power JD, Dosenbach NU, Church JA, Miezin FM, Schlaggar BL, Petersen SE (2009) Functional brain networks develop from a “local to distributed” organization. PLoS Comput Biol 5:e1000381.
16. Fischl B (2012) FreeSurfer. Neuroimage 62:774 -781
17. 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.
18. 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.
19. Fornito A, Zalesky A, Bassett DS, Meunier D, Ellison-Wright I, Yücel M, Wood SJ, Shaw K, O’Connor J, Nertney D, Mowry BJ, Pantelis C, Bullmore ET (2011) Genetic influences on cost-efficient organization of human cortical functional networks. J Neurosci 31:3261-3270.
20. Fornito A, Zalesky A, Breakspear M (2013) Graph analysis of the human connectome: promise, progress, and pitfalls. Neuroimage 80:426-444.
21. Fornito A, Zalesky A, Breakspear M (2015) The connectomics of brain disorders. Nat Rev Neurosci 16:159 -172.
22. Giedd JN, Raznahan A, Alexander-Bloch A, Schmitt E, Gogtay N, Rapoport JL (2015) Child psychiatry branch of the national institute of mental health longitudinal structural magnetic resonance imaging study of human brain development. Neuropsychopharmacology 40: 43- 49.
23. Grayson DS, Ray S, Carpenter S, Iyer S, Dias TG, Stevens C, Nigg JT, Fair DA (2014) Structural and functional rich club organization of the brain in children and adults. PLoS One 9:e88297.
24. Hagmann P, Sporns O, Madan N, Cammoun L, Pienaar R, Wedeen VJ, Meuli R, Thiran JP, Grant PE (2010) White matter maturation reshapes structural connectivity in the late developing human brain. Proc Natl Acad Sci U S A 107:19067-19072.
25. Harriger L, van den Heuvel MP, Sporns O (2012) Rich club organization of macaque cerebral cortex and its role in network communication. PLoS One 7:e46497.
26. Huttenlocher PR (1979) Synaptic density in human frontal cortex - developmental changes and effects of aging. Brain Res 163:195-205.
27. Hwang K, Velanova K, Luna B (2010) Strengthening of top-down frontal cognitive control networks underlying the development of inhibitory control: a functional magnetic resonance imaging effective connectivity study. J Neurosci 30:15535-15545.
28. Hwang K, Hallquist MN, Luna B (2013) The development of hub architecture in the human functional brain network. Cereb Cortex 23:2380 -2393.
29. 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- 841.
30. Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM (2012) FSL. Neuroimage 62:782-790.
31. Jeurissen B, Leemans A, Jones DK, Tournier JD, Sijbers J (2011) Probabilistic fiber tracking using the residual bootstrap with constrained spherical deconvolution. Hum Brain Mapp 32:461- 479
32. Jones DK, Knösche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage 73:239 -254.
33. Kelly AM, Di Martino A, Uddin LQ, Shehzad Z, Gee DG, Reiss PT, Margulies DS, Castellanos FX, Milham MP (2009) Development of anterior cingulated functional connectivity from late childhood to early adulthood. Cereb Cortex 19:640-657.
34. Lewis MD, Todd RM (2007) The self-regulating brain: cortical-subcortical feedback and the development of intelligent action. Cogn Dev 22:406-430.
35. Liston C, Watts R, Tottenham N, Davidson MC, Niogi S, Ulug AM, Casey BJ (2006) Frontostriatal microstructure modulates efficient recruitment of cognitive control. Cereb Cortex 16:553-560.
36. 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.
37. Maslov S, Sneppen K (2002) Specificity and stability in topology of protein networks. Science 296:910 -913.
38. Opsahl T, Colizza V, Panzarasa P, Ramasco JJ (2008) Prominence and control: the weighted rich-club effect. Phys Rev Lett 101:168702.
39. Panksepp J (1998) Affective neuroscience: the foundations of human and animal emotion. New York: Oxford UP.
40. Paus T (2010) Growth of white matter in the adolescent brain: myelin or axon? Brain Cogn 72:26 -35.
41. Paus T, Collins DL, Evans AC, Leonard G, Pike B, Zijdenbos A (2001) Maturation of white matter in the human brain: a review of magnetic resonance studies. Brain Res Bull 54:255-266.
42. Paus T, Keshavan M, Giedd JN (2008) Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9:947-957.
43. Ramirez-Manzanares A, Cook PA, Hall M, Ashtari M, Gee JC (2011) Resolving axon fiber crossings at clinical b-values: an evaluation study. Med Phys 38:5239 -5253.
44. Reese TG, Heid O, Weisskoff RM, Wedeen VJ (2003) Reduction of eddycurrent-induced distortion in diffusion MRI using a twice-refocused spin echo. Magn Reson Med 49:177-182.
45. Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059 -1069.
46. Schmithorst VJ, Yuan W (2010) White matter development during adolescence as shown by diffusion MRI. Brain Cogn 72:16 -25.
47. Sowell ER, Thompson PM, Holmes CJ, Jernigan TL, Toga AW (1999) In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci 2:859-861.
48. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417- 463.
49. Steinberg L (2005) Cognitive and affective development in adolescence. Trends Cogn Sci 9:69 -74.
50. Suckling J, Bullmore E (2004) Permutation tests for factorially designed neuroimaging experiments. Hum Brain Mapp 22:193-205.
51. Tau GZ, Peterson BS (2010) Normal development of brain circuits. Neuropsychopharmacology 35:147-168.
52. Tournier JD, Yeh CH, Calamante F, Cho KH, Connelly A, Lin CP (2008) Resolving crossing fibres using constrained spherical deconvolution: validation using diffusion-weighted imaging phantom data. Neuroimage 42:617- 625.
53. Tournier JD, Calamante F, Connelly A (2012) MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol 22:53- 66.
54. Towlson EK, Ve´rtes PE, Ahnert SE, Schafer WR, Bullmore ET (2013) The rich club of the C. elegans neuronal connectome. J Neurosci 33:6380-6387.
55. Uddin LQ, Supekar KS, Ryali S, Menon V (2011) Dynamic reconfiguration of structural and functional connectivity across core neurocognitive brain networks with development. J Neurosci 31:18578 -18589.
56. van den Heuvel MP, Sporns O (2011) Rich-club organization of the human connectome. J Neurosci 31:15775-15786.
57. van den Heuvel MP, Sporns O (2013) An anatomical substrate for integration among functional networks in human cortex. J Neurosci 33:14489- 14500.
58. van den Heuvel MP, Kahn RS, Goni J, Sporns O (2012) High-cost, highcapacity backbone for global brain communication. Proc Natl Acad Sci U S A 109:11372-11377.
59. van den Heuvel MP, Sporns O, Collin G, Scheewe T, Mandl RC, Cahn W, Goni J, Hulshoff Pol HE, Kahn RS (2013) Abnormal rich club organiza- tion and functional brain dynamics in schizophrenia. JAMA Psychiatry 70:783-792.
60. Wechsler D (1999) Wechsler Abbreviated Scale of Intelligence (WASI). San Antonio, TX: Harcourt.
61. Wechsler D (2003) Wechsler Intelligence Scale for children—4th Edition (WISC-IV). San Antonio, TX: Harcourt.
62. Whittle S, Yap MB, Yücel M, Fornito A, Simmons JG, Barrett A, Sheeber L, Allen NB (2008) Prefrontal and amygdala volumes are related to adolescents’ affective behaviors during parent-adolescent interactions. Proc Natl Acad Sci U S A 105:3652-3657.
63. Xia M, Wang J, He Y (2013) BrainNet Viewer: a network visualization tool for human brain connectomics. PLoS One 8:e68910.
64. Yakovlev P, Lecours A (1967) The myelogenetic cycles of regional maturation of the brain. In: Regional development of the brain in early life (Minkowski A, ed), pp 3-70. Oxford: Blackwell Scientific.
65. Zalesky A, Fornito A, Bullmore ET (2010a) Network-based statistic: identifying differences in brain networks. Neuroimage 53:1197-1207.
66. Zalesky A, Fornito A, Harding IH, Cocchi L, Yücel M, Pantelis C, Bullmore ET (2010b) Whole-brain anatomical networks: does the choice of nodes matter? Neuroimage 50:970 -983.
67. 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.