White matter maturation reshapes structural connectivity in the late developing human brain

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 44, 2010, Pages 19067-19072

  Hagmann, P ^a,b   Sporns, O ^c   Madan, N ^d   Cammoun, L ^b   Pienaar, R ^e   Wedeen, V J ^f   Meuli, R ^a   Thiran, J P ^b   Grant, P E ^e,f  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b EPFL   (Switzerland)

^c INDIANA UNIVERSITY   (United States)

^d TUFTS MEDICAL CENTER   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Connectome; Development; Graph; Network dynamics; Tractography

Indexed keywords

ADOLESCENT; ADULT; BRAIN DEVELOPMENT; BRAIN MATURATION; CHILD; CLINICAL ARTICLE; CONFERENCE PAPER; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MYELIN SHEATH; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; WHITE MATTER;

EID: 78650504202     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1009073107     Document Type: Article

References (58)

1. Barabasi A, Albert R, Jeong H (2000) Scale-free characteristics of random networks: The topology of the World-Wide Web. Physica A 281:69-77.
2. Barabasi AL, Albert R (1999) Emergence of scaling in random networks. Science 286: 509-512.
3. Albert R, Jeong H, Barabasi AL (2000) Error and attack tolerance of complex networks. Nature 406:378-382.
4. Barabasi AL, et al. (2002) Evolution of the social network of scientific collaborations. Physica A 311:590-614.
5. Holme P, Edling CR, Liljeros F (2004) Structure and time evolution of an Internet dating community. Soc Networks 26:155-174.
6. Innocenti GM, Price DJ (2005) Exuberance in the development of cortical networks. Nat Rev Neurosci 6:955-965.
7. Luo L, O'Leary DD (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28:127-156.
8. Low LK, Cheng HJ (2006) Axon pruning: An essential step underlying the developmental plasticity of neuronal connections. Philos Trans R Soc Lond B Biol Sci 361:1531-1544.
9. van der Knaap M, Valk J (2005) Magnetic Resonance of Myelin, Myelination, and Myelin Disorders (Springer, New York).
10. Paus T (2010) Growth of white matter in the adolescent brain: Myelin or axon? Brain Cogn 72:26-35.
11. Giedd JN (2004) Structural magnetic resonance imaging of the adolescent brain. Ann N Y Acad Sci 1021:77-85.
12. Giedd JN, et al. (1999) Brain development during childhood and adolescence: A longitudinal MRI study. Nat Neurosci 2:861-863.
13. Rademacher J, Engelbrecht V, Bürgel U, Freund H, Zilles K (1999) Measuring in vivo myelination of human white matter fiber tracts with magnetization transfer MR. Neuroimage 9:393-406.
14. Barkovich AJ, Kjos BO, Jackson DE, Jr, Norman D (1988) Normal maturation of the neonatal and infant brain: MR imaging at 1.5 T. Radiology 166:173-180.
15. Fornari E, Knyazeva MG, Meuli R, Maeder P (2007) Myelination shapes functional activity in the developing brain. Neuroimage 38:511-518.
16. Salami M, Itami C, Tsumoto T, Kimura F (2003) Change of conduction velocity by regional myelination yields constant latency irrespective of distance between thalamus and cortex. Proc Natl Acad Sci USA 100:6174-6179.
17. Uhlhaas PJ, et al. (2009) Neural synchrony in cortical networks: History, concept and current status. Front Integr Neurosci 3:17.
18. Fair DA, et al. (2007) Development of distinct control networks through segregation and integration. Proc Natl Acad Sci USA 104:13507-13512.
19. Fair DA, et al. (2009) Functional brain networks develop from a "local to distributed" organization. PLOS Comput Biol 5:e1000381.
20. Supekar K, Musen M, Menon V (2009) Development of large-scale functional brain networks in children. PLoS Biol 7:e1000157.
21. Chen R, Cohen LG, Hallett M (2002) Nervous system reorganization following injury. Neuroscience 111:761-773.
22. Bütefisch CM (2004) Plasticity in the human cerebral cortex: Lessons from the normal brain and from stroke. Neuroscientist 10:163-173.
23. Koch MA, Norris DG, Hund-Georgiadis M (2002) An investigation of functional and anatomical connectivity using magnetic resonance imaging. Neuroimage 16:241-250.
24. Greicius MD, Supekar K, Menon V, Dougherty RF (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19:72-78.
25. Hagmann P, et al. (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6:e159.
26. Honey CJ, et al. (2009) Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci USA 106:2035-2040.
27. Hagmann P (2005) From diffusion MRI to brain connectomics. PhD Thesis (Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland).
28. Sporns O, Tononi G, Kötter R (2005) The human connectome: A structural description of the human brain. PLOS Comput Biol 1:e42.
29. Teipel SJ, et al. (2009) Regional networks underlying interhemispheric connectivity: An EEG and DTI study in healthy ageing and amnestic mild cognitive impairment. Hum Brain Mapp 30:2098-2119.
30. Desikan RS, et al. (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31: 968-980.
31. Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 15:435-455.
32. Sakuma H, et al. (1991) Adult and neonatal human brain: Diffusional anisotropy and myelination with diffusion-weighted MR imaging. Radiology 180:229-233.
33. Neil JJ, et al. (1998) Normal brain in human newborns: Apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. Radiology 209:57-66.
34. Löbel U, et al. (2009) Diffusion tensor imaging: The normal evolution of ADC, RA, FA, and eigenvalues studied in multiple anatomical regions of the brain. Neuroradiology 51:253-263.
35. Kimura F, Itami C (2009) Myelination and isochronicity in neural networks. Front Neuroanat 3:12.
36. Morriss MC, Zimmerman RA, Bilaniuk LT, Hunter JV, Haselgrove JC (1999) Changes in brain water diffusion during childhood. Neuroradiology 41:929-934.
37. Engelbrecht V, Scherer A, Rassek M, Witsack HJ, Mödder U (2002) Diffusion-weighted MR imaging in the brain in children: Findings in the normal brain and in the brain with white matter diseases. Radiology 222:410-418.
38. Cohen Y, Assaf Y (2002) High b-value q-space analyzed diffusion-weighted MRS and MRI in neuronal tissues - a technical review. NMR Biomed 15:516-542.
39. Lebel C, Walker L, Leemans A, Phillips L, Beaulieu C (2008) Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 40:1044-1055.
40. Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059-1069.
41. Hagmann P, et al. (2007) Mapping human whole-brain structural networks with diffusion MRI. PLoS ONE 2:e597.
42. Newman ME (2006) Modularity and community structure in networks. Proc Natl Acad Sci USA 103:8577-8582.
43. Smith RS, Koles ZJ (1970) Myelinated nerve fibers: Computed effect of myelin thickness on conduction velocity. Am J Physiol 219:1256-1258.
44. Ullén F (2009) Is activity regulation of late myelination a plastic mechanism in the human nervous system? Neuron Glia Biol 5:29-34.
45. Tamnes CK, et al. (2010) Brain maturation in adolescence and young adulthood: Regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb Cortex 20:534-548.
46. Mulkern RV, et al. (1999) Multi-component apparent diffusion coefficients in human brain. NMR Biomed 12:51-62.
47. Clark CA, Le Bihan D (2000) Water diffusion compartmentation and anisotropy at high b values in the human brain. Magn Reson Med 44:852-859.
48. Fields RD (2005) Myelination: An overlooked mechanism of synaptic plasticity? Neuroscientist 11:528-531.
49. Bengtsson SL, et al. (2005) Extensive piano practicing has regionally specific effects on white matter development. Nat Neurosci 8:1148-1150.
50. Fair DA, et al. (2008) The maturing architecture of the brain's default network. Proc Natl Acad Sci USA 105:4028-4032.
51. Haber SN, Calzavara R (2009) The cortico-basal ganglia integrative network: The role of the thalamus. Brain Res Bull 78:69-74.
52. Hashimoto T, et al. (2009) Protracted developmental trajectories of GABAA receptor alpha1 and alpha2 subunit expression in primate prefrontal cortex. Biol Psychiatry 65: 1015-1023.
53. Niessing J, et al. (2005) Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science 309:948-951.
54. Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66:259-267.
55. Tuch DS, Reese TG, Wiegell MR, Wedeen VJ (2003) Diffusion MRI of complex neural architecture. Neuron 40:885-895.
56. Raichle ME, et al. (2001) A default mode of brain function. Proc Natl Acad Sci USA 98: 676-682.
57. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34: 537-541.
58. Basser PJ (1995) Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed 8:333-344.