Quantitative in vivo evidence for broad regional gradients in the timing of white matter maturation during adolescence

NeuroImage

Volumn 54, Issue 1, 2011, Pages 25-31

  Colby, John B ^a,b   Van Horn, John D ^a   Sowell, Elizabeth R ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Development; Diffusion; DTI; Gradient; Myelin; White matter

Indexed keywords

ADOLESCENT; ADULT; AGE DISTRIBUTION; ARTICLE; BRAIN MAPPING; BRAIN MATURATION; CHILD; CONTROLLED STUDY; DIFFUSION WEIGHTED IMAGING; FEMALE; HUMAN; IN VIVO STUDY; MALE; NERVE CELL PLASTICITY; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRESCHOOL CHILD; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SCHOOL CHILD; WHITE MATTER MATURATION;

ADOLESCENT; AGING; BODY WATER; BRAIN; CHILD; CHILD, PRESCHOOL; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; HUMANS; MALE; MYELIN SHEATH; PATIENT SELECTION; PYRAMIDAL TRACTS; REFERENCE VALUES;

EID: 77957969023     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.08.014     Document Type: Article

References (49)

1. Anderson V.A., Anderson P., Northam E., Jacobs R., Catroppa C. Development of executive functions through late childhood and adolescence in an Australian sample. Dev. Neuropsychol. 2001, 20:385-406.
2. Asato M.R., Terwilliger R., Woo J., Luna B. White matter development in adolescence: A DTI study. Cereb. Cortex 2010, 20:2122-2131.
3. Behrens T.E.J., Johansen-Berg H., Woolrich M.W., Smith S.M., Wheeler-Kingshott C.A.M., Boulby P.A., Barker G.J., Sillery E.L., Sheehan K., Ciccarelli O., Thompson A.J., Brady J.M., Matthews P.M. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat. Neurosci. 2003, 6:750-757.
4. Bengtsson S.L., Nagy Z., Skare S., Forsman L., Forssberg H., Ullén F. Extensive piano practicing has regionally specific effects on white matter development. Nat. Neurosci. 2005, 8:1148-1150.
5. Bunge S.A., Dudukovic N.M., Thomason M.E., Vaidya C.J., Gabrieli J.D.E. Immature frontal lobe contributions to cognitive control in children: evidence from fMRI. Neuron 2002, 33:301-311.
6. Casey B.J., Cohen J.D., Jezzard P., Turner R., Noll D.C., Trainor R.J., Giedd J., Kaysen D., Hertz-Pannier L., Rapoport J.L. Activation of prefrontal cortex in children during a nonspatial working memory task with functional MRI. Neuroimage 1995, 2:221-229.
7. Casey B.J., Tottenham N., Liston C., Durston S. Imaging the developing brain: what have we learned about cognitive development?. Trends Cogn. Sci. 2005, 9:104-110.
8. Casey B.J., Epstein J.N., Buhle J., Liston C., Davidson M.C., Tonev S.T., Spicer J., Niogi S., Millner A.J., Reiss A., Garrett A., Hinshaw S.P., Greenhill L.L., Shafritz K.M., Vitolo A., Kotler L.A., Jarrett M.A., Glover G. Frontostriatal connectivity and its role in cognitive control in parent-child dyads with ADHD. Am. J. Psychiatry 2007, 164:1729-1736.
9. Chau D.T., Roth R.M., Green A.I. The neural circuitry of reward and its relevance to psychiatric disorders. Curr. Psychiatry Rep. 2004, 6:391-399.
10. Davis S.W., Dennis N.A., Buchler N.G., White L.E., Madden D.J., Cabeza R. Assessing the effects of age on long white matter tracts using diffusion tensor tractography. Neuroimage 2009, 46:530-541.
11. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., Paus T., Evans A.C., Rapoport J.L. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 1999, 2:861-863.
12. Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., Nugent T.F., Herman D.H., Clasen L.S., Toga A.W., Rapoport J.L., Thompson P.M. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:8174-8179.
13. Hsu J., Hecke W.V., Bai C., Lee C., Tsai Y., Chiu H., Jaw F., Hsu C., Leu J., Chen W., Leemans A. Microstructural white matter changes in normal aging: a diffusion tensor imaging study with higher-order polynomial regression models. Neuroimage 2010, 49:32-43.
14. Huttenlocher P.R. Morphometric study of human cerebral cortex development. Neuropsychologia 1990, 28:517-527.
15. Kemper T.L. Neuroanatomical and neuropathological changes during aging. Clinical Neurology of Aging 1994, 8-9. Oxford University Press, New York, NY. 2nd ed. M.L. Albert, J.E. Knoefel (Eds.).
16. Le Bihan D. Looking into the functional architecture of the brain with diffusion MRI. Nat. Rev. Neurosci. 2003, 4:469-480.
17. Lebel C., Walker L., Leemans A., Phillips L., Beaulieu C. Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 2008, 40:1044-1055.
18. Liston C., Watts R., Tottenham N., Davidson M.C., Niogi S., Ulug A.M., Casey B.J. Frontostriatal microstructure modulates efficient recruitment of cognitive control. Cereb. Cortex 2006, 16:553-560.
19. Luna B., Thulborn K.R., Munoz D.P., Merriam E.P., Garver K.E., Minshew N.J., Keshavan M.S., Genovese C.R., Eddy W.F., Sweeney J.A. Maturation of widely distributed brain function subserves cognitive development. Neuroimage 2001, 13:786-793.
20. Luna B., Garver K.E., Urban T.A., Lazar N.A., Sweeney J.A. Maturation of cognitive processes from late childhood to adulthood. Child Dev. 2004, 75:1357-1372.
21. Luna B., Padmanabhan A., O'Hearn K. What has fMRI told us about the development of cognitive control through adolescence?. Brain Cogn. 2010, 72:101-113.
22. Madsen K.S., Baaré W.F.C., Vestergaard M., Skimminge A., Ejersbo L.R, Ramsøy T.Z., Gerlach C., Akeson P., Paulson O.B., Jernigan T.L. Response inhibition is associated with white matter microstructure in children. Neuropsychologia 2010, 48:854-862.
23. Mori S., Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 2006, 51:527-539.
24. Mukherjee P., Miller J.H., Shimony J.S., Conturo T.E., Lee B.C., Almli C.R., McKinstry R.C. Normal brain maturation during childhood: developmental trends characterized with diffusion-tensor MR imaging. Radiology 2001, 221:349-358.
25. Nichols T.E., Holmes A.P. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 2002, 15:1-25.
26. Nomura Y., Sakuma H., Takeda K., Tagami T., Okuda Y., Nakagawa T. Diffusional anisotropy of the human brain assessed with diffusion-weighted MR: relation with normal brain development and aging. AJNR Am. J. Neuroradiol. 1994, 15:231-238.
27. Olson E.A., Collins P.F., Hooper C.J., Muetzel R., Lim K.O., Luciana M. White matter integrity predicts delay discounting behavior in 9- to 23-year-olds: a diffusion tensor imaging study. J. Cogn. Neurosci. 2009, 21:1406-1421.
28. Qiu D., Tan L., Zhou K., Khong P. Diffusion tensor imaging of normal white matter maturation from late childhood to young adulthood: Voxel-wise evaluation of mean diffusivity, fractional anisotropy, radial and axial diffusivities, and correlation with reading development. Neuroimage 2008, 41:223-232.
29. Reichenberg A., Caspi A., Harrington H., Houts R., Keefe R.S.E., Murray R.M., Poulton R., Moffitt T.E. Static and dynamic cognitive deficits in childhood preceding adult schizophrenia: A 30-Year study. Am. J. Psychiatry 2010, 167:160-169.
30. Rex D.E., Ma J.Q., Toga A.W. The LONI Pipeline processing environment. Neuroimage 2003, 19:1033-1048.
31. Romine C.B., Reynolds C.R. A model of the development of frontal lobe functioning: findings from a meta-analysis. Appl. Neuropsychol. 2005, 12:190-201.
32. Schmithorst V., Yuan W. White matter development during adolescence as shown by diffusion MRI. Brain Cogn. 2010, 72:16-25.
33. Schmithorst V.J., Holland S.K., Dardzinski B.J. Developmental differences in white matter architecture between boys and girls. Hum. Brain Mapp. 2008, 29:696-710.
34. Schneider J.F.L., Il'yasov K.A., Hennig J., Martin E. Fast quantitative diffusion-tensor imaging of cerebral white matter from the neonatal period to adolescence. Neuroradiology 2004, 46:258-266.
35. Scholz J., Klein M.C., Behrens T.E.J., Johansen-Berg H. Training induces changes in white-matter architecture. Nat. Neurosci. 2009, 12:1367-1368.
36. Shaw P., Greenstein D., Lerch J., Clasen L., Lenroot R., Gogtay N., Evans A., Rapoport J., Giedd J. Intellectual ability and cortical development in children and adolescents. Nature 2006, 440:676-679.
37. Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002, 17:143-155.
38. Smith S., Nichols T.E. Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 2009, 44:83-98.
39. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E.J., Johansen-Berg H., Bannister P.R., Luca M.D., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., Stefano N.D., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23:S208-S219.
40. Smith S.M., Jenkinson M., Johansen-Berg H., Rueckert D., Nichols T.E., Mackay C.E., Watkins K.E., Ciccarelli O., Cader M.Z., Matthews P.M., Behrens T.E.J. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006, 31:1487-1505.
41. Snook L., Paulson L., Roy D., Phillips L., Beaulieu C. Diffusion tensor imaging of neurodevelopment in children and young adults. Neuroimage 2005, 26:1164-1173.
42. Sowell E.R., Johnson A., Kan E., Lu L.H., Van Horn J.D., Toga A.W., O'Connor M.J., Bookheimer S.Y. Mapping white matter integrity and neurobehavioral correlates in children with fetal alcohol spectrum disorders. J. Neurosci. 2008, 28:1313-1319.
43. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 2000, 24:417-463.
44. Tamnes C., østby Y., Fjell A., Westlye L., Due-Tønnessen P., Walhovd K. Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb. Cortex 2010, 20:534-548.
45. Tuch D.S., Salat D.H., Wisco J.J., Zaleta A.K., Hevelone N.D., Rosas H.D. Choice reaction time performance correlates with diffusion anisotropy in white matter pathways supporting visuospatial attention. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:12212-12217.
46. Tzarouchi L.C., Astrakas L.G., Xydis V., Zikou A., Kosta P., Drougia A., Andronikou S., Argyropoulou M.I. Age-related grey matter changes in preterm infants: an MRI study. Neuroimage 2009, 47:1148-1153.
47. Versace A., Almeida J.R.C., Hassel S., Walsh N.D., Novelli M., Klein C.R., Kupfer D.J., Phillips M.L. Elevated left and reduced right orbitomedial prefrontal fractional anisotropy in adults with bipolar disorder revealed by tract-based spatial statistics. Arch. Gen. Psychiatry 2008, 65:1041-1052.
48. Woolrich M.W., Jbabdi S., Patenaude B., Chappell M., Makni S., Behrens T., Beckmann C., Jenkinson M., Smith S.M. Bayesian analysis of neuroimaging data in FSL. Neuroimage 2009, 45:S173-S186.
49. Yakovlev P.I., Lecours A.R. The myelogenetic cycles of regional maturation of the brain. Regional Development of the Brain Early in Life 1967, 3-70. Blackwell Scientific Publications Inc, Oxford, England. A. Minkowski (Ed.).