Normal Brain Maturation during Childhood: Developmental Trends Characterized with Diffusion-Tensor MR Imaging

PURPOSE: To characterize the maturational changes in water diffusion within central gray matter nuclei and central white matter pathways of the human brain by using diffusion-tensor magnetic resonance (MR) imaging.

MATERIALS AND METHODS: Retrospective analysis of normal MR examination findings in 153 subjects (age range, 1 day to 11 years) referred for clinical neuroimaging was performed. All studies included diffusion tensor-encoded echo-planar MR imaging. Isotropic diffusion coefficient (D̄) and diffusion anisotropy (Aσ) were measured in the corpus callosum, internal capsule, caudate nucleus, lentiform nucleus, and thalamus.

RESULTS: D̄ exhibited biexponential decay with age in gray and white matter regions, except for monoexponential decay in the genu of the corpus callosum. There was a steep nonlinear increase of Aσ in white matter tracts that paralleled the time course of the decline in D̄. In basal ganglia, only a small linear increase in Aσ was observed in patients. Aσ changes in the thalamus were intermediate between basal ganglia and white matter structures.

CONCLUSION: Changes in magnitude and anisotropy of water diffusion follow stereotypical time courses during brain development that can be empirically described with multiexponential regression models, which suggests that quantitative scalar parameters derived from diffusion-tensor MR imaging may provide clinically useful developmental milestones for brain maturity. Supplemental material: radiology.rsnajnls.org/cgi/content/full/2212001702/DC1.

References

  • 1 Yakovlev PI, Lecours AR. The myelogenetic cycles of regional maturation of the brain. In: Minkowski A, eds. Regional development of the brain in early life. Oxford, England: Blackwell Scientific, 1967; 3-70. Google Scholar
  • 2 Richardson EP, Jr. Myelination in the human central nervous system. In: Haymaker W, Adams RD, eds. Histology and histopathology of the nervous system. Springfield, Ill: Thomas, 1982; 146-173. Google Scholar
  • 3 Barkovich AJ, Kjos BO, Jackson DE, Jr, Norman D. Normal brain maturation of the neonatal and infant brain: MR imaging at 1.5 T. Radiology 1988; 166:173-180. LinkGoogle Scholar
  • 4 LeBihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986; 161:401-407. LinkGoogle Scholar
  • 5 LeBihan D, Moonen CT, van Zijl PC, Pekar J, DesPres D. Measuring random microscopic motion of water in tissues with MR imaging: a cat brain study. J Comput Assist Tomogr 1991; 15:19-25. Crossref, MedlineGoogle Scholar
  • 6 Moseley ME, Cohen Y, Mintorovich J, et al. Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy. Magn Reson Med 1990; 14:330-346. Crossref, MedlineGoogle Scholar
  • 7 Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G. Diffusion tensor MR imaging of the human brain. Radiology 1996; 201:637-648. LinkGoogle Scholar
  • 8 Sakuma H, Nomura Y, Takeda K, et al. Adult and neonatal human brain: diffusional anisotropy and myelination with diffusion-weighted MR imaging. Radiology 1991; 180:229-233. LinkGoogle Scholar
  • 9 Nomura Y, Sakuma H, 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. MedlineGoogle Scholar
  • 10 Takeda K, Nomura Y, Sakuma H, Tagami T, Okuda Y, Nakagawa T. MR assessment of normal brain development in neonates and infants: comparative study of T1- and diffusion-weighted images. J Comput Assist Tomogr 1997; 21:1-7. Crossref, MedlineGoogle Scholar
  • 11 Huppi PS, Maier SE, Peled S, et al. Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 1998; 44:584-590. Crossref, MedlineGoogle Scholar
  • 12 Neil JJ, Shiran SI, McKinstry RC, et al. Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. Radiology 1998; 209:57-66. LinkGoogle Scholar
  • 13 Morriss MC, Zimmerman RA, Bilaniuk LT, Hunter JV, Haselgrove JC. Changes in brain water diffusion during childhood. Neuroradiology 1999; 41:929-934. Crossref, MedlineGoogle Scholar
  • 14 Wimberger DM, Roberts TP, Barkovich AJ, Prayer LM, Moseley ME, Kucharczyk J. Identification of “premyelination” by diffusion-weighted MRI. J Comput Assist Tomogr 1995; 19:28-33. Crossref, MedlineGoogle Scholar
  • 15 Basser PJ, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative diffusion tensor MRI. J Magn Reson B 1996; 111:209-219. Crossref, MedlineGoogle Scholar
  • 16 Conturo TE, McKinstry RC, Akbudak E, Robinson BH. Encoding of anisotropic diffusion with tetrahedral gradients: a general mathematical diffusion formalism and experimental results. Magn Reson Med 1996; 35:399-412. Crossref, MedlineGoogle Scholar
  • 17 Colton T.. Statistics in medicine Boston, Mass: Little, Brown, 1974; 153-158. Google Scholar
  • 18 Shimony JS, McKinstry RC, Akbudak E, et al. Quantitative diffusion-tensor anisotropy imaging: normative human data and anatomic analysis. Radiology 1999; 212:770-784. LinkGoogle Scholar
  • 19 Mukherjee P, Bahn MM, McKinstry RC, et al. Differences between gray matter and white matter water diffusion in stroke: diffusion-tensor MR imaging in 12 patients. Radiology 2000; 215:211-220. LinkGoogle Scholar
  • 20 van Gelderen P, de Vleeschouwer MH, DesPres D, Prekar J, van Zijl PC, Moonen CT. Water diffusion and acute stroke. Magn Reson Med 1994; 31:154-163. Crossref, MedlineGoogle Scholar
  • 21 Ulug AM, Beauchamp N, Bryan RN, van Zijl PCM. Absolute quantitation of diffusion constants in human stroke. Stroke 1997; 28:483-490. Crossref, MedlineGoogle Scholar
  • 22 Press WH, Teukolsky SA, Vetterling WT, Flannery BP. Numerical recipes in C: the art of scientific computing 2nd ed. Cambridge, Mass: Cambridge University Press, 1992; 681-699. Google Scholar
  • 23 Bevington PR. Data reduction and error analysis in the physical sciences New York, NY: McGraw-Hill, 1969; 200-203. Google Scholar
  • 24 Seber GAF, Wild CF. Nonlinear regression New York, NY: Wiley, 1989; 197. Google Scholar
  • 25 Shimony JS, McKinstry RC, Akbudak E, Snyder AZ, Aronovitz JA, Conturo TE. Cerebral diffusion tensor imaging: normative data, signal to noise measurements, and anatomical findings (abstr) In: Proceedings of the Fifth Meeting of the International Society for Magnetic Resonance in Medicine. Berkeley, Calif: International Society for Magnetic Resonance in Medicine, 1997; 225. Google Scholar
  • 26 Zacharopoulos N, Narayana P. Selective measurement of white matter and gray matter diffusion trace values in normal human brain. Med Phys 1998; 25:2237-2241. Crossref, MedlineGoogle Scholar
  • 27 Feinberg DA, Jakab PD. Tissue perfusion in humans studied by Fourier velocity distribution, line scan, and echo-planar imaging. Magn Reson Med 1990; 16:280-293. Crossref, MedlineGoogle Scholar
  • 28 Conturo TE, McKinstry RC, Aronovitz JA, Neil JJ. Diffusion MRI: precision, accuracy, and flow effects. NMR Biomed 1995; 8:307-332. Crossref, MedlineGoogle Scholar
  • 29 Pfefferbaum A, Sullivan EV, Hedehus M, Lim KO, Adalsteinsson E, Moseley M. Age-related decline in brain white matter anisotropy measured with spatially corrected echo-planar diffusion tensor imaging. Magn Reson Med 2000; 44:259-268. Crossref, MedlineGoogle Scholar
  • 30 Kwong KK, McKinstry RC, Chien D, Crawley AP, Pearlman JD, Rosen BR. CSF-suppressed quantitative single-shot diffusion imaging. Magn Reson Med 1991; 21:157-163. Crossref, MedlineGoogle Scholar
  • 31 Engelbrecht V, Rassek M, Preiss S, Wald C, Modder U. Age-dependent changes in magnetization transfer contrast of white matter in the pediatric brain. AJNR Am J Neuroradiol 1998; 19:1923-1929. MedlineGoogle Scholar
  • 32 Davis JM, Himwich WA. Amino acids and proteins of developing mammalian brain. In: Himwich WA, eds. Biochemistry of the developing brain. New York, NY: Dekker, 1973; 55-110. Google Scholar
  • 33 Autti T, Raininko R, Vanhanen SL, Kallio M, Santavuori P. MRI of the normal brain from early childhood to middle age. II. Age dependence of signal intensity changes on T2-weighted images. Neuroradiology 1994; 36:649-651. Google Scholar
  • 34 Steen RG, Ogg RJ, Reddick WE, Kingsley PB. Age-related changes in the pediatric brain: quantitative MR evidence of maturational changes during adolescence. AJNR Am J Neuroradiol 1997; 19:819-828. Google Scholar
  • 35 Paus T, Zijdenbos A, Worsley K, et al. Structural maturation of neural pathways in children and adolescents: in vivo study. Science 1999; 283:1908-1911. Crossref, MedlineGoogle Scholar
  • 36 Baratti C, Barnett AS, Pierpaoli C. Comparative MR imaging study of brain maturation in kittens with T1, T2, and the trace of the diffusion tensor. Radiology 1999; 210:133-142. LinkGoogle Scholar
  • 37 Melhem ER, Itoh R, Jones L, Barker PB. Diffusion tensor MR imaging of the brain: effect of diffusion weighting on trace and anisotropy measurements. AJNR Am J Neuroradiol 2000; 21:1813-1820. MedlineGoogle Scholar
  • 38 DeLano MC, Cooper TG, Siebert JE, Potchen MJ, Kuppusamy K. High-b-value diffusion-weighted MR imaging of adult brain: image contrast and apparent diffusion coefficient map features. AJNR Am J Neuroradiol 2000; 21:1830-1836. MedlineGoogle Scholar
  • 39 Klingberg T, Hedehus M, Temple E, et al. Microstructure of temporo-parietal white matter as a basis for reading ability: evidence from diffusion tensor magnetic resonance imaging. Neuron 2000; 25:493-500. Crossref, MedlineGoogle Scholar
  • 40 Conturo TE, Lori NF, Cull TS, et al. Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci U S A 1999; 96:10422-10427. Crossref, MedlineGoogle Scholar
  • 41 Barkovich AJ. Pediatric neuroimaging 3rd ed. Philadelphia, Pa: Lippincott, 2000; 13-69. Google Scholar

Article History

Published in print: Nov 2001