Neurite density index is sensitive to age related differences in the developing brain

NeuroImage

Volumn 148, Issue , 2017, Pages 373-380

  Genc, Sila ^a,b   Malpas, Charles B ^a,c   Holland, Scott K ^d   Beare, Richard ^a,e   Silk, Timothy J ^a,b  

^a MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF CINCINNATI   (United States)

^e MONASH UNIVERSITY   (Australia)

Author keywords

Age; Development; DTI; Neurite density; NODDI; White matter

Indexed keywords

ADOLESCENT; ADULT; AGE; ARTICLE; BRAIN DEVELOPMENT; CHILD; COHORT ANALYSIS; DIFFUSION WEIGHTED IMAGING; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; MALE; NERVOUS SYSTEM PARAMETERS; NEURITE; NEURITE DENSITY INDEX; NEURITE ORIENTATION DISPERSION DENSITY IMAGING; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; RECEIVER OPERATING CHARACTERISTIC; WHITE MATTER; AGING; ANISOTROPY; BIOLOGICAL MODEL; BRAIN; CYTOLOGY; DIFFUSION TENSOR IMAGING; GROWTH, DEVELOPMENT AND AGING; IMAGE PROCESSING; PHYSIOLOGY; PRESCHOOL CHILD; YOUNG ADULT;

ADOLESCENT; AGING; ANISOTROPY; BRAIN; CHILD; CHILD, PRESCHOOL; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MODELS, NEUROLOGICAL; NEURITES; NEUROIMAGING; WHITE MATTER; YOUNG ADULT;

EID: 85012306160     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2017.01.023     Document Type: Article

References (42)

1. Andersson, J.L.R., Sotiropoulos, S.N., An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage 125 (2016), 1063–1078.
2. Basser, P.J., Pierpaoli, C., Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. Ser. B 111 (1996), 209–219.
3. Beaulieu, C., The basis of anisotropic water diffusion in the nervous system – a technical review. NMR Biomed. 15 (2002), 435–455.
4. Beaulieu, C., The biological basis of diffusion anisotropy. Diffus. MRI: Quant. Meas. Vivo Neuroanat., 2009, 105–126.
5. Chang, Y.S., Owen, J.P., Pojman, N.J., Thieu, T., Bukshpun, P., Wakahiro, M.L.J., Berman, J.I., Roberts, T.P.L., Nagarajan, S.S., Sherr, E.H., Mukherjee, P., White matter changes of neurite density and fiber orientation dispersion during human brain maturation. Plos One, 10, 2015, e0123656.
6. Cook, P.A., Symms, M., Boulby, P.A., Alexander, D.C., Optimal acquisition orders of diffusion-weighted MRI measurements. J. Magn. Reson. Imaging 25 (2007), 1051–1058.
7. Counsell, S.J., Zhang, H., Hughes, E., Steele, H., Tusor, N., Ball, G., Makropoulos, A., Alexander, D.C., Hajnal, J.V., Edwards, D., In vivo assement of neurite density in the preterm brain using diffusion magnetic resonance imaging. Proc. Int. Soc. Mag. Reson. Med., 22, 2014.
8. De Santis, S., Drakesmith, M., Bells, S., Assaf, Y., Jones, D.K., Why diffusion tensor MRI does well only some of the time: variance and covariance of white matter tissue microstructure attributes in the living human brain. Neuroimage 89 (2014), 35–44.
9. 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. 2 (1999), 861–863.
10. Graham, M.S., Drobnjak, I., Zhang, H., Realistic simulation of artefacts in diffusion MRI for validating post-processing correction techniques. Neuroimage 125 (2016), 1079–1094.
11. Grussu, F., Schneider, T., Prados, F., Tur, C., Ourselin, S., Zhang, H., Alexander, D.C., Wheeler-Kingshott, C.A.M.G., Axon diameter distribution influences diffusion-derived axonal density estimation in the human spinal cord: in silico and in vivo evidence. Proc. Int. Soc. Mag. Reson. Med., 24, 2016.
12. Haász, J., Westlye, E.T., Fjær, S., Espeseth, T., Lundervold, A., Lundervold, A.J., General fluid-type intelligence is related to indices of white matter structure in middle-aged and old adults. Neuroimage 83 (2013), 372–383.
13. Hanley, J.A., The robustness of the “binormal” assumptions used in fitting ROC curves. Med. Decis. Mak. 8 (1988), 197–203.
14. Holland, S.K., Vannest, J., Mecoli, M., Jacola, L.M., Tillema, J.M., Karunanayaka, P.R., Schmithorst, V.J., Yuan, W., Plante, E., Byars, A.W., Functional MRI of language lateralization during development in children. Int. J. Audiol. 46 (2007), 533–551.
15. Holland, S., Schmithorst, V.J., Wagner, M., Lee, G., Rajagopal, A., Sroka, M., Felicelli, N., Rupert, A., Clark, K., Toga, A., Freund, L., C-MIND Consortium, 2015. The C-MIND project: normative MRI and behavioral data from children from birth to 18 years. In: Proceedings of the 21st Annual Meeting of the Organization for Human Brain Mapping (OHBM), Honolulu, HA.
16. Jelescu, I.O., Veraart, J., Adisetiyo, V., Milla, S.S., Novikov, D.S., Fieremans, E., One diffusion acquisition and different white matter models: how does microstructure change in human early development based on WMTI and NODDI?. Neuroimage 107 (2015), 242–256.
17. Jenkinson, M., Smith, S., A global optimisation method for robust affine registration of brain images. Med. Image Anal. 5 (2001), 143–156.
18. Jones, D.K., Knosche, T.R., Turner, R., White matter integrity, fiber count, and other fallacies: the do's and don'ts of diffusion MRI. Neuroimage 73 (2013), 239–254.
19. Kelly, C.E., Thompson, D.K., Chen, J., Leemans, A., Adamson, C.L., Inder, T.E., Cheong, J.L., Doyle, L.W., Anderson, P.J., Axon density and axon orientation dispersion in children born preterm. Hum. Brain Mapp. 37 (2016), 3080–3102.
20. Kodiweera, C., Alexander, A.L., Harezlak, J., McAllister, T.W., Wu, Y.C., Age effects and sex differences in human brain white matter of young to middle-aged adults: a DTI, NODDI, and q-space study. Neuroimage 128 (2016), 180–192.
21. Krogsrud, S.K., Fjell, A., Tamnes, C.K., Grydeland, H., Mork, L., Due-Tonnessen, P., Bjornerud, A., Sampaio-Baptista, C., Andersson, J., Johansen-Berg, H., Walhovd, K.B., Changes in white matter microstructure in the developing brain-A longitudinal diffusion tensor imaging study of children from 4 to 11 years of age. Neuroimage 124 (2016), 473–486.
22. Lebel, C., Gee, M., Camicioli, R., Wieler, M., Martin, W., Beaulieu, C., Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage 60 (2012), 340–352.
23. Lebel, C., Walker, L., Leemans, A., Phillips, L., Beaulieu, C., Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 40 (2008), 1044–1055.
24. Malpas, C.B., Genc, S., Saling, M.M., Velakoulis, D., Desmond, P.M., O'Brien, T.J., MRI correlates of general intelligence in neurotypical adults. J. Clin. Neurosci. 24 (2016), 128–134.
25. Merluzzi, A.P., Dean, D.C., Adluru, N., Suryawanshi, G.S., Okonkwo, O.C., Oh, J.M., Hermann, B.P., Sager, M.A., Asthana, S., Zhang, H., Johnson, S.C., Alexander, A.L., Bendlin, B.B., Age-dependent differences in brain tissue microstructure assessed with neurite orientation dispersion and density imaging. Neurobiol. Aging 43 (2016), 79–88.
26. Mori, S., Zhang, J.Y., Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51 (2006), 527–539.
27. Owen, J.P., Chang, Y.S., Pojman, N.J., Bukshpun, P., Wakahiro, M.L., Marco, E.J., Berman, J.I., Spiro, J.E., Chung, W.K., Buckner, R.L., Roberts, T.P., Nagarajan, S.S., Sherr, E.H., Mukherjee, P., Aberrant white matter microstructure in children with 16p11.2 deletions. J Neurosci. 34 (2014), 6214–6223.
28. Paus, T., Growth of white matter in the adolescent brain: myelin or axon?. Brain Cogn. 72 (2010), 26–35.
29. Paus, T., Zijdenbos, A., Worsley, K., Collins, D.L., Blumenthal, J., Giedd, J.N., Rapoport, J.L., Evans, A.C., Structural maturation of neural pathways in children and adolescents: in vivo study. Science 283 (1999), 1908–1911.
30. Sepehrband, F., Clark, K.A., Ullmann, J.F.P., Kurniawan, N.D., Leanage, G., Reutens, D.C., Yang, Z.Y., Brain tissue compartment density estimated using diffusion-weighted MRI yields tissue parameters consistent with histology. Human. Brain Mapp. 36 (2015), 3687–3702.
31. Simmonds, D.J., Hallquist, M.N., Asato, M., Luna, B., Developmental stages and sex differences of white matter and behavioral development through adolescence: a longitudinal diffusion tensor imaging (DTI) study. Neuroimage 92 (2014), 356–368.
32. Smith, S.M., Jenkinson, M., Woolrich, M.W., Beckmann, C.F., Behrens, T.E.J., Johansen-Berg, H., Bannister, P.R., De Luca, M., Drobnjak, I., Flitney, D.E., Niazy, R.K., Saunders, J., Vickers, J., Zhang, Y.Y., De Stefano, N., Brady, J.M., Matthews, P.M., Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 (2004), S208–S219.
33. Sowell, E.R., Peterson, B.S., Thompson, P.M., Welcome, S.E., Henkenius, A.L., Toga, A.W., Mapping cortical change across the human life span. Nat. Neurosci. 6 (2003), 309–315.
34. Veraart, J., Fieremans, E., Novikov, D.S., Diffusion MRI noise mapping using random matrix theory. Magn. Reson. Med., 2016.
35. Vernooij, M.W., Smits, M., Wielopolski, P.A., Houston, G.C., Krestin, G.P., van der Lugt, A., Fiber density asymmetry of the arcuate fasciculus in relation to functional hemispheric language lateralization in both right- and left-handed healthy subjects: a combined fMRI and DTI study. Neuroimage 35 (2007), 1064–1076.
36. Wakana, S., Van Zijl, P., Mori, S., Wakana, S., van Zijl, P., MRI Atlas of Human White Matter. 2005, Elsevier Science & Technology.
37. Wierenga, L.M., Langen, M., Oranje, B., Durston, S., Unique developmental trajectories of cortical thickness and surface area. Neuroimage 87 (2014), 120–126.
38. Xu, J., Moeller, S., Auerbach, E.J., Strupp, J., Smith, S.M., Feinberg, D.A., Yacoub, E., Ugurbil, K., Evaluation of slice accelerations using multiband echo planar imaging at 3 T. Neuroimage 83 (2013), 991–1001.
39. Zhang, H., Hubbard, P.L., Parker, G.J.M., Alexander, D.C., Axon diameter mapping in the presence of orientation dispersion with diffusion MRI. Neuroimage 56 (2011), 1301–1315.
40. Zhang, H., Schneider, T., Wheeler-Kingshott, C.A., Alexander, D.C., NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage 61 (2012), 1000–1016.
41. Zhang, H., Yushkevich, P.A., Alexander, D.C., Gee, J.C., Deformable registration of diffusion tensor MR images with explicit orientation optimization. Med. Image Anal. 10 (2006), 764–785.
42. Zhang, H., Yushkevich, P.A., Rueckert, D., Gee, J.C., A computational white matter atlas for aging with surface-based representation of fasciculi. Fischer, B., Dawant, B.M., Lorenz, C., (eds.) Biomedical Image Registration, 2010, 83–90.