Neuroimaging of cortical development and brain connectivity in human newborns and animal models

Journal of Anatomy

Volumn 217, Issue 4, 2010, Pages 418-428

  Lodygensky, Gregory A ^a   Vasung, Lana ^a,b   Sizonenko, Stéphane V ^a   Hüppi, Petra S ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF ZAGREB   (Croatia)

Author keywords

DTI; Hypoxic ischemic; Inflammatory; MRI; Newborn; Preterm

Indexed keywords

ANIMAL MODEL; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; DIFFUSION TENSOR IMAGING; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MATHEMATICAL ANALYSIS; NEUROIMAGING; NEWBORN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PREMATURITY; PRIORITY JOURNAL; WHITE MATTER;

ANIMALS; CEREBRAL CORTEX; CHILD BEHAVIOR DISORDERS; DISEASE MODELS, ANIMAL; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; INFANT, NEWBORN; INFANT, PREMATURE; MAGNETIC RESONANCE IMAGING; NERVE FIBERS; PHENOTYPE;

ANIMALIA;

EID: 77956486569     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2010.01280.x     Document Type: Article

References (99)

1. Abernethy LJ, Palaniappan M, Cooke RW. Quantitative magnetic resonance imaging of the brain in survivors of very low birth weight. Arch Dis Child 2002, 87:279-283.
2. Allin M, Matsumoto H, Santhouse AM. Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term 3. Brain 2001, 124:60-66.
3. Anbeek P, Vincken KL, Groenendaal F. Probabilistic brain tissue segmentation in neonatal magnetic resonance imaging. Pediatr Res 2008, 63:158-163.
4. Anderson NG, Laurent I, Woodward LJ. Detection of impaired growth of the corpus callosum in premature infants. Pediatrics 2006, 118:951-960.
5. Anjari M, Srinivasan L, Allsop JM. Diffusion tensor imaging with tract-based spatial statistics reveals local white matter abnormalities in preterm infants. Neuroimage 2007, 35:1021-1027.
6. Ashburner J, Friston KJ. Why voxel-based morphometry should be used. Neuroimage 2001, 14:1238-1243.
7. Assaf Y, Blumenfeld-Katzir T, Yovel Y. AxCaliber: a method for measuring axon diameter distribution from diffusion MRI. Magn Reson Med 2008, 59:1347-1354.
8. Barnette AR, Neil JJ, Kroenke CD. Characterization of brain development in the ferret via MRI. Pediatr Res 2009, 66:80-84.
9. Battin MR, Maalouf EF, Counsell SJ. Magnetic resonance imaging of the brain in very preterm infants: visualization of the germinal matrix, early myelination, and cortical folding. Pediatrics 1998, 101:957-962.
10. Bengtsson SL, Nagy Z, Skare S. Extensive piano practicing has regionally specific effects on white matter development. Nat. Neurosci. 2005, 8:1148-1150.
11. Born P, Leth H, Miranda MJ. Visual activation in infants and young children studied by functional magnetic resonance imaging. Pediatr Res 1998, 44:578-583.
12. Borradori Tolsa C, Zimine S, Warfield S. Postnatal growth and neurodevelopmental outcome of premature infants born with intrauterine growth restriction. Pediatr Res 2004, 55:411A.
13. Cachia A, Mangin JF, Riviere D. A primal sketch of the cortex mean curvature: a morphogenesis based approach to study the variability of the folding patterns. IEEE Trans Med Imaging 2003, 22:754-765.
14. Colonnese MT, Phillips MA, Constantine-Paton M. Development of hemodynamic responses and functional connectivity in rat somatosensory cortex. Nat Neurosci 2008, 11:72-79.
15. Counsell SJ, Maalouf EF, Fletcher AM. MR imaging assessment of myelination in the very preterm brain. AJNR Am J Neuroradiol 2002, 23:872-881.
16. Dehaene-Lambertz G, Dehaene S, Hertz-Pannier L. Functional neuroimaging of speech perception in infants. Science 2002, 298:2013-2015.
17. Deipolyi AR, Mukherjee P, Gill K. Comparing microstructural and macrostructural development of the cerebral cortex in premature newborns: diffusion tensor imaging versus cortical gyration. Neuroimage 2005, 27:579-586.
18. Dubois J, Benders M, Borradori-Tolsa C. Primary cortical folding in the human newborn: an early marker of later functional development. Brain 2008a, 131:2028-2041.
19. Dubois J, Benders M, Cachia A. Mapping the early cortical folding process in the preterm newborn brain. Cereb Cortex 2008b, 18:1444-1454.
20. Dubois J, Benders M, Lazeyras F. Structural asymmetries of perisylvian regions in the preterm newborn. Neuroimage 2010, 52:32-42.
21. Dudink J, Lequin M, van PC. Fractional anisotropy in white matter tracts of very-low-birth-weight infants. Pediatr Radiol 2007, 37:1216-1223.
22. Erberich SG, Panigrahy A, Friedlich P. Somatosensory lateralization in the newborn brain. Neuroimage 2006, 29:155-161.
23. Feldman R, Eidelman AI. Neonatal state organization, neuromaturation, mother-infant interaction, and cognitive development in small-for-gestational-age premature infants. Pediatrics 2006, 118:e869-e878.
24. Ferrie JC, Barantin L, Saliba E. MR assessment of the brain maturation during the perinatal period: quantitative T2 MR study in premature newborns. Magn Reson Imaging 1999, 17:1275-1288.
25. Fox MD, Snyder AZ, Vincent JL. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 2005, 102:9673-9678.
26. Fransson P, Skiold B, Horsch S. Resting-state networks in the infant brain. Proc Natl Acad Sci USA 2007, 104:15531-15536.
27. Giorgio A, Watkins KE, Douaud G. Changes in white matter microstructure during adolescence. Neuroimage 2008, 39:52-61.
28. Hrbek A, Karlberg P, Olsson T. Development of visual and somatosensory evoked responses in pre-term newborn infants. Electroencephalogr Clin Neurophysiol 1973, 34:225-232.
29. Huang H, Zhang J, Wakana S. White and gray matter development in human fetal, newborn and pediatric brains. Neuroimage 2006, 33:27-38.
30. Huang H, Yamamoto A, Hossain MA. Quantitative cortical mapping of fractional anisotropy in developing rat brains. J Neurosci 2008, 28:1427-1433.
31. Huppi PS. Advances in postnatal neuroimaging: relevance to pathogenesis and treatment of brain injury. Clin Perinatol 2002, 29:827-856.
32. Huppi PS, Schuknecht B, Boesch C. Structural and neurobehavioral delay in postnatal brain development of preterm infants. Pediatr Res 1996, 39:895-901.
33. Huppi PS, Maier SE, Peled S. Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 1998a, 44:584-590.
34. Huppi PS, Warfield S, Kikinis R. Quantitative magnetic resonance imaging of brain development in premature and mature newborns. Ann Neurol 1998b, 43:224-235.
35. Huppi PS, Murphy B, Maier SE. Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics 2001, 107:455-460.
36. Inder TE, Håppi PS, Warfield S. Periventricular white matter injury in the premature infant is associated with a reduction in cerebral cortical gray matter volume at term. Ann Neurol 1999, 46:755-760.
37. Inder TE, Warfield SK, Wang H. Abnormal cerebral structure is present at term in premature infants. Pediatrics 2005, 115:286-294.
38. Kasprian G, Brugger PC, Weber M. In utero tractography of fetal white matter development. Neuroimage 2008, 43:213-224.
39. Kesler SR, Reiss AL, Vohr B. Brain volume reductions within multiple cognitive systems in male preterm children at age twelve. J Pediatr 2008, 152:513-520.
40. Kim JH, Budde MD, Liang HF. Detecting axon damage in spinal cord from a mouse model of multiple sclerosis. Neurobiol Dis 2006, 21:626-632.
41. Kostovic I, Jovanov-Milosevic N. The development of cerebral connections during the first 20-45 weeks' gestation. Semin Fetal Neonatal Med 2006, 11:415-422.
42. Kostovic I, Molliver ME. A new interpretation of the laminar development of the cerebral cortex: synaptogenesis in different layers of neopallium in the human fetus. American Association of Anatomists. Eighty seventh annual session. Anat Rec 1974, 178:395.
43. Kostovic I, Rakic P. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 1990a, 297:441-470.
44. Kostovic I, Rakic P. Developmental history of the transient subplate zone in visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 1990b, 297:441-470.
45. Kostovic I, Vasung L. Insights from in vitro fetal magnetic resonance imaging of cerebral development. Semin Perinatol 2009, 33:220-233.
46. Kostovic I, Judas M, Rados M. Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb Cortex 2002, 12:536-544.
47. Kreher BW, Mader I, Kiselev VG. Gibbs tracking: a novel approach for the reconstruction of neuronal pathways. Magn Reson Med 2008, 60:953-963.
48. Kroenke CD, Bretthorst GL, Inder TE. Diffusion MR imaging characteristics of the developing primate brain. Neuroimage 2005, 25:1205-1213.
49. Limperopoulos C, Soul JS, Gauvreau K. Late gestation cerebellar growth is rapid and impeded by premature birth 1. Pediatrics 2005, 115:688-695.
50. Lodygensky GA, Rademaker K, Zimine S. Structural and functional brain development after hydrocortisone treatment for neonatal chronic lung disease. Pediatrics 2005, 116:1-7.
51. Lodygensky GA, Inder TE, Neil JJ. Application of magnetic resonance imaging in animal models of perinatal hypoxic-ischemic cerebral injury. Int J Dev Neurosci 2008a, 26:13-25.
52. Lodygensky GA, Seghier ML, Warfield SK. Intrauterine growth restriction affects the preterm infant's hippocampus. Pediatr Res 2008b, 63:438-443.
53. Lodygensky G, West T, Stump M. In vivo MRI analysis of an inflammatory injury in the developing brain. Brain Behav Immun 2009, 24:759-767.
54. Martin E, Joeri P, Loenneker T. Visual processing in infants and children studied using functional MRI. Pediatr Res 1999, 46:135-140.
55. McKinstry RC, Mathur A, Miller JP. Radial organization of developing human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. Cereb Cortex 2002a, 12:1237-1243.
56. McKinstry RC, Miller JH, Snyder AZ. A prospective, longitudinal diffusion tensor imaging study of brain injury in newborns. Neurology 2002b, 59:824-833.
57. van Meer MP, van der Marel K, Wang K. Recovery of sensorimotor function after experimental stroke correlates with restoration of resting-state interhemispheric functional connectivity. J Neurosci 2010, 30:3964-3972.
58. Ment LR, Kesler S, Vohr B. Longitudinal brain volume changes in preterm and term control subjects during late childhood and adolescence. Pediatrics 2009, 123:503-511.
59. Mewes AU, Huppi PS, Als H. Regional brain development in serial magnetic resonance imaging of low-risk preterm infants. Pediatrics 2006, 118:23-33.
60. Miller SP, Vigneron DB, Henry RG. Serial quantitative diffusion tensor MRI of the premature brain: development in newborns with and without injury. J Magn Reson Imaging 2002, 16:621-632.
61. Mori S, Crain BJ, Chacko VP. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 1999, 45:265-269.
62. Mukherjee P, Miller JH, Shimony JS. Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. AJNR Am J Neuroradiol 2002, 23:1445-1456.
63. Muramoto S, Yamada H, Sadato N. Age dependent change in metabolic response to photic stimulation of the primary visual cortex in infants: functional magnetic resonance imaging study. J Comput Assist Tomogr 2002, 26:894-901.
64. Murphy BP, Inder TE, Håppi PS. Impaired cerebral cortical gray matter growth following treatment with dexamethasone for neonatal chronic lung disease. Pediatrics 2001, 107:217-221.
65. Narberhaus A, Segarra D, Caldu X. Gestational age at preterm birth in relation to corpus callosum and general cognitive outcome in adolescents. J Child Neurol 2007, 22:761-765.
66. Neil JJ, Shiran SI, McKinstry RC. Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured using diffusion tensor imaging. Radiology 1998, 209:57-66.
67. Nosarti C, Giouroukou E, Healy E. Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome. Brain 2008, 131:205-217.
68. Ogawa SL, Lee TM, Kay AR. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci 1990, 87:9868-9872.
69. Parker GJ, Haroon HA, Wheeler-Kingshott CA. A framework for a streamline-based probabilistic index of connectivity (PICo) using a structural interpretation of MRI diffusion measurements. J Magn Reson Imaging 2003, 18:242-254.
70. Partridge SC, Mukherjee P, Henry RG. Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. Neuroimage 2004, 22:1302-1314.
71. Prayer D, Kasprian G, Krampl E. MRI of normal fetal brain development. Eur J Radiol 2006, 57:199-216.
72. Quairiaux C, Sizonenko SV, Megevand P. Functional deficit and recovery of developing sensorimotor networks following neonatal hypoxic-ischemic injury in the rat. Cereb Cortex 2010, http://dx.doi.org/10.1093/cercor/bhp281, doi:10.1093/cercor/bhp281
73. Rados M, Judas M, Kostovic I. In vitro MRI of brain development. Eur J Radiol 2006, 57:187-198.
74. Ramenghi LA, Fumagalli M, Righini A. Magnetic resonance imaging assessment of brain maturation in preterm neonates with punctate white matter lesions. Neuroradiology 2007, 49:161-167.
75. Rose SE, Hatzigeorgiou X, Strudwick MW. Altered white matter diffusion anisotropy in normal and preterm infants at term-equivalent age. Magn Reson Med 2008, 60:761-767.
76. Rutherford M, Counsell S, Allsop J. Diffusion-weighted magnetic resonance imaging in term perinatal brain injury: a comparison with site of lesion and time from birth. Pediatrics 2004, 114:1004-1014.
77. Schafer RJ, Lacadie C, Vohr B. Alterations in functional connectivity for language in prematurely born adolescents. Brain 2009, 132:661-670.
78. Seghier ML, Huppi PS. The role of functional magnetic resonance imaging in the study of brain development, injury, and recovery in the newborn. Semin Perinatol 2010, 34:79-86.
79. Seghier ML, Lazeyras F, Zimine S. Combination of event-related fMRI and diffusion tensor imaging in an infant with perinatal stroke. Neuroimage 2004, 21:463-472.
80. Seghier ML, Lazeyras F, Zimine S. Visual recovery after perinatal stroke evidenced by functional and diffusion MRI: case report. BMC Neurol 2005, 5:17.
81. Seghier ML, Lazeyras F, Huppi PS. Functional MRI of the newborn. Semin Fetal Neonatal Med 2006, 11:479-488.
82. Sizonenko SV, Kiss JZ, Inder T. Distinctive neuropathologic alterations in the deep layers of the parietal cortex after moderate ischemic-hypoxic injury in the P3 immature rat brain. Pediatr Res 2005, 57:865-872.
83. Sizonenko SV, Bednarek N, Gressens P. Growth factors and plasticity. Semin Fetal Neonatal Med 2007a, 12:241-249.
84. Sizonenko SV, Camm EJ, Garbow JR. Developmental changes and injury induced disruption of the radial organization of the cortex in the immature rat brain revealed by in vivo diffusion tensor MRI. Cereb Cortex 2007b, 17:2609-2617.
85. Smith SM, Jenkinson M, Johansen-Berg H. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006, 31:1487-1505.
86. Smyser CD, Inder TE, Shimony JS. Longitudinal analysis of neural network development in preterm infants. Cereb Cortex 2010, http://dx.doi.org/10.1093/cercor/bhq035, doi:10.1093/cercor/bhq035
87. Song SK, Yoshino J, Le TQ. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 2005, 26:132-140.
88. Srinivasan L, Allsop J, Counsell SJ. Smaller cerebellar volumes in very preterm infants at term-equivalent age are associated with the presence of supratentorial lesions. AJNR Am J Neuroradiol 2006, 27:573-579.
89. Srinivasan L, Dutta R, Counsell SJ. Quantification of deep gray matter in preterm infants at term-equivalent age using manual volumetry of 3-tesla magnetic resonance images. Pediatrics 2007, 119:759-765.
90. Takeuchi H, Sekiguchi A, Taki Y. Training of working memory impacts structural connectivity. J Neurosci 2010, 30:3297-3303.
91. Tavor I, Sagi Y, Hostetter S. Diffusion MRI of Short-Term Spacial Memory Related Brain Plasticity. Proc Intl Soc Mag Reson Med 2010, 18:9.
92. Toft PB, Leth H, Ring PB. Volumetric analysis of the normal infant brain and in intrauterine growth retardation. Early Hum Dev 1995, 43:15-29.
93. Volpe JJ. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 2009, 8:110-124.
94. Weisenfeld NI, Warfield SK. Automatic segmentation of newborn brain MRI. Neuroimage 2009, 47:564-572.
95. West T, Stump M, Lodygensky G. Lack of X-linked inhibitor of apoptosis protein leads to increased apoptosis and tissue loss following neonatal brain injury. ASN NEURO 2009, 1. http://dx.doi.org/10.1042/AN20090005, doi:10.1042/AN20090005
96. Wimberger DM, Roberts TP, Barkovich AJ. Identification of " premyelination" by diffusion-weighted MRI. J Comptr Assisted Tomography 1995, 19:28-33.
97. Woodward LJ, Anderson PJ, Austin NC. Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. N Engl J Med 2006, 355:685-694.
98. Yamada H, Sadato N, Konishi Y. A rapid brain metabolic change in infants detected by fMRI. Neuroreport 1997, 8:3775-3778.
99. Zhang N, Rane P, Huang W. Mapping resting-state brain networks in conscious animals. J Neurosci Methods 2010, 189:186-196.