Emerging cerebral connectivity in the human fetal Brain: An MR tractography study

Cerebral Cortex

Volumn 22, Issue 2, 2012, Pages 455-464

  Takahashi, Emi ^a,b   Folkerth, Rebecca D ^a,c   Galaburda, Albert M ^d   Grant, Patricia E ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Brain; Development; Diffusion imaging; Human fetus; Tractography

Indexed keywords

ARTICLE; AUTOPSY; BRAIN; BRAIN GANGLION; BRAIN REGION; CELL JUNCTION; CEREBELLUM; CONCEPTION; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FETUS; FRONTAL LOBE; HUMAN; HUMAN TISSUE; NEURAL CREST; NEUROIMAGING; PARIETO-OCCIPITAL SULCUS; PRIORITY JOURNAL; TEMPORAL CORTEX;

AGE FACTORS; BRAIN; BRAIN MAPPING; CEREBRAL CORTEX; DIFFUSION TENSOR IMAGING; FETUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; NEURAL PATHWAYS;

EID: 84863001494     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr126     Document Type: Article

References (71)

1. Armstrong E, Schleicher A, Omran H, Curtis M, Silles K. 1995. The ontogeny of human gyrification. Cereb Cortex. 5:56-63.
2. Barbas H, Rempel-Clower N. 1997. Cortical structure predicts the pattern of corticocortical connections. Cereb Cortex. 7:635-646. (Pubitemid 27467975)
3. Barkovich AJ, Rowley H, Bollen A. 1995. Correlation of prenatal events with the development of polymicrogyria. Am J Neuroradiol. 16: 822-827.
4. Barron DH. 1950. An experimental analysis of some factors involved in the development of the fissure pattern of the cerebral cortex. J Exp Zool. 113:553-581.
5. Billiards SS, Pierson CR, Haynes RL, Folkerth RD, Kinney HC. 2006. Is the late preterm infant more vulnerable to gray matter injury than the term infant? Clin Perinatol. 33:915-933. Available from: http://www.ncbi.nlm.nih.gov.ezp- prod1.hul.harvard.edu/pubmed/17148012. (Pubitemid 44834646)
6. Blanton RE, Levitt JG, Thompson PM, Narr KL, Capetillo-Cunliffe L, Nobel A, Singerman JD, McCracken JT, Toga AW, et al. 2001. Mapping cortical asymmetry and complexity patterns in normal children. Psychiatry Res. 107:29-43. (Pubitemid 32706504)
7. Burkhalter A, Bernardo KL, Charles VJ. 1993. Development of local circuits in human visual cortex. J Neurosci. 13:1916-1931. (Pubitemid 23113405)
8. Campbell K, Götz M. 2002. Radial glia: multi-purpose cells for vertebrate brain development. Trends Neurosci. 25:235-238. (Pubitemid 34327796)
9. Caviness VS, Kennedy DN, Bates J, Makris N. 1996. The developmental neuroimaging: mapping the development of brain and behaviour. New York: Academic Press. p. 3-14.
10. Chi JG, Dooling EC, Gilles FH. 1977. Gyral development of the human brain. Ann Neurol. 1:86-93.
11. Connolly C. 1950. External morphology of the primate brain. Springfield (IL): Charles C Thomas.
12. Dubois J, Benders M, Borradori-Tolsa C, Cachia A, Lazeyras F, Ha-Vinh Leuchter R, Sizonenko SV, Warfield SK, Mangin JF, Hüppi PS. 2008. Primary cortical folding in the human newborn: an early marker of later functional development. Brain. 131:2028-2041.
13. Encha-Razavi F, Sonigo P. 2003. Features of the developing brain. Childs Nerv Syst. 19:426-428. (Pubitemid 37161583)
14. Galaburda AM, Sherman GF, Rosen GD, Aboitiz F, Geschwind N. 1985. Developmental dyslexia: four consecutive patients with cortical anomalies. Ann Neurol. 18:222-233. (Pubitemid 15004894)
15. Galaburda AM, Holinger D, Mills D, Reiss A, Korenberg JR, Bellugi U. 2003. Williams syndrome. A summary of cognitive, electrophysiological, anatomofunctional, microanatomical and genetic findings. Rev Neurol. 36(Suppl 1):S132-S137.
16. Goldman-Rakic PS. 1980. Morphological consequences of prenatal injury to the primate brain. Prog Brain Res. 53:1-19.
17. Goldman-Rakic PS, Rakic P. 1984. Experimental modification of gyral patterns. In: Geschwind N, Galaburda A, editors. Cerebral dominance. Cambridge (MA): Harvard University Press. p. 179-192.
18. Haynes RL, Borenstein NS, Desilva TM, Folkerth RD, Liu LG, Volpe JJ, Kinney HC. 2005. Axonal development in the cerebral white matter of the human fetus and infant. J Comp Neurol. 484:156-167. (Pubitemid 40321843)
19. Hevner RF. 2000. Development of connections in the human visual system during fetal mid-gestation: a DiI-tracing study. J Neuropathol Exp Neurol. 59:385-392. (Pubitemid 30257568)
20. Hilgetag CC, Barbas H. 2005. Developmental mechanics of the primate cerebral cortex. Anat Embryol. 210:411-417. (Pubitemid 41752601)
21. Hilgetag CC, Barbas H. 2006. Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Comput Biol. 2(3):e22.
22. His W. 1874. Unsere Korperform und das physiologische Problem ihrer Entstehung. Leipzig (Germany): F.C.W. Vogel.
23. Honig LS, Herrmann K, Shatz CJ. 1996. Developmental changes revealed by immunohistochemical markers in human cerebral cortex. Cereb Cortex. 6:794-806. (Pubitemid 26374304)
24. Huang H, Zhang J, Wakana S, Zhang W, Ren T, Richards LJ, Yarowsky P, Donohue P, Graham E, van Zijl PC, et al. 2006. White and gray matter development in human fetal, newborn and pediatric brains. Neuroimage. 33:27-38. (Pubitemid 44397586)
25. Huang H, Xue R, Zhang J, Ren T, Richards LJ, Yarowsky P, Miller MI, Mori S. 2009. Anatomical characterization of human fetal brain development with diffusion tensor magnetic resonance imaging. J Neurosci. 29:4263-4273.
26. Innocenti GM, Price DJ. 2005. Exuberence in the development of cortical networks. Nat Rev. 6:955-965.
27. Jansen AC, Leonard G, Bastos AC, Esposito-Festen JE, Tampieri D, Watkins K, Andermann F, Andermann E. 2005. Cognitive functioning in bilateral perisylvian polymicrogyria (BPP): clinical and radiological correlations. Epilepsy Behav. 6:393-404. (Pubitemid 40468430)
28. Joyner AH, Rddey CJ, Bloss CS, Bakken TE, Rimol LM, Melle I, Agartz I, Djurovic S, Topol EJ, Schork NJ, et al. 2009. A common MECP2 haplotype associates with reduced cortical surface area in humans in two independent populations. Proc Natl Acad Sci U S A. 106: 15483-15488.
29. Kasprian G, Brugger PC, Weber M, Krssák M, Krampl E, Herold C, Prayer D. 2008. In utero tractography of fetal white matter development. Neuroimage. 43:213-224.
30. Kostovic I, Jovanov-Milosevic N. 2006. The development of cerebral connections during the first 20-45 weeks'gestation. Semin Fetal Neonat Med. 11:415-422. (Pubitemid 44666590)
31. Kostovic I, Judas M. 2010. The development of the subplate and thalamo-cortical connections in the human foetal brain. Acta Paediatr. doi: 10.1111/j.1651-2227.2010.01811.x.
32. Kostovic I, Rakic P. 1984. Development of prestriate visual projections in the monkey and human fetal cerebrum revealed by transient cholinesterase staining. J Neurosci. 4:25-42. (Pubitemid 14198285)
33. Kostovic I, Rakic P. 1990. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol. 297:441-470. (Pubitemid 20222635)
34. Leergaard TB, White NS, de Crespigny A, Bolstad I, D'Arceuil H, Bjaalie JG, Dale AM. 2010. Quantitative histological validation of diffusion MRI fiber orientation distributions in the rat brain. PLoS One. 5:e8595.
35. Letinic K, Zoncu R, Rakic P. 2002. Origin of GABAergic neurons in the human neocortex. Nature. 417:645-649. (Pubitemid 34614822)
36. Levitt JG, Blanton RE, Smalley S, Thompson PM, Guthrie D, McCracken JT, Sadoun T, Heinichen L, Toga AW. 2003. Cortical sulcal maps in autism. Cereb Cortex. 13:728-735. (Pubitemid 36758959)
37. McKinstry RC, Mathur A, Miller JH, Ozcan A, Snyder AZ, Schefft GL, Almli CR, Shiran SI, Conturo TE, Neil JJ. 2002. Radial organization of developing preterm human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. Cereb Cortex. 12:1237-1243. (Pubitemid 35396961)
38. Mori S, Crain BJ, Chacko VP, van Zijl PC. 1999. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol. 45:265-269. (Pubitemid 29072377)
39. Nadarajah B, Alifragis P, Wong ROL, Parnavelas JG. 2003. Neuronal migration in the developing cerebral cortex: observations based on real-time imaging. Cerebral Cortex. 13:607-611. (Pubitemid 36613168)
40. Narr KL, Bilder RM, Kim S, Thompson PM, Szeszko P, Robinson D, Luders E, Toga AW. 2004. Abnormal gyral complexity in firstepisode schizophrenia. Biol Psychiatry. 55:859-867. (Pubitemid 38429878)
41. Noga JT, Bartley AJ, Jones DW, Torrey EF, Weinberger DR. 1996. Cortical gyral anatomy and gross brain dimensions in monozygotic twins discordant for schizophrenia. Schizophr Res. 22:27-40. (Pubitemid 26352772)
42. Nowell MA, Grossman RI, Hackney DB, Zimmerman RA, Goldberg HI, Bilaniuk LT. 1988. MR imaging of white matter disease in children. Am J Radiol. 151:359-365.
43. Rados M, Judas M, Kostovic I. 2006. In vitro MRI of brain development. Eur J Radiol. 57:187-198. (Pubitemid 43183649)
44. Rakic P. 1988. Specification of cerebral cortical areas. Science. 241: 170-176.
45. Rapoport JL, Castellanos FX, Gogate N, Janson K, Kohler S, Nelson P. 2001. Imaging normal and abnormal brain development: new perspectives for child psychiatry. Aust N Z J Psychiatry. 35:272-281. (Pubitemid 32621850)
46. Retzius A. 1891. Ueber den Bau der Oberflachenschicht der Grosshirnrinde beim Menschen und bei den Saugethieren. Biologiska Foreningens Forhandlingar. 3:90-103.
47. Richman DP, Stewart RM, Hutchinson JW, Caviness VS, Jr. 1975. Mechanical model of brain convolutional development. Science. 189:18-21.
48. Sarnat HB. 1992. Regional differentiation of the human fetal ependyma: immunocytochemical markers. J Neuropathol Exp Neurol. 51:58-75.
49. Schmahmann JD, Pandya DN, Wang R, Dai G, D'Arceuil HE, de Crespigny AJ, Wedeen VJ. 2007. Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain. 130:630-653. (Pubitemid 46410733)
50. Schmechel DE, Rakic P. 1979. A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat Embryol (Berl). 1979(156):115-152. (Pubitemid 9213953)
51. Sidman RL, Rakic P. 1973. Neuronal migration, with special reference to developing human brain: a review. Brain Res. 62:1-35.
52. Stagaad M, Mollgard K. 1989. The developing neuroepithelium in human embryonic and fetal brain studied with vimentin immunohistochemistry. Anat Embryol (Berl). 180:17-28. (Pubitemid 19166312)
53. Takahashi E, Dai G, Rosen GD, Wang R, Ohki K, Folkerth RD, Galaburda A, Wedeen VJ, Grant PE. 2011. Developing neocortex organization and connectivity in cats revealed by direct correlation of diffusion tractography and histology. Cereb Cortex. 21:200-211.
54. Takahashi E, Dai G, Wang R, Ohki K, Rosen GD, Galaburda A, Grant PE, Wedeen VJ. 2010. Development of cerebral fiber pathways in cats revealed by diffusion spectrum imaging. Neuroimage. 49: 1231-1240.
55. Takahashi E, Ohki K, Kim DS. 2007. Diffusion tensor studies dissociated two fronto-temporal pathways in the human memory system. Neuroimage. 34:827-838. (Pubitemid 44834475)
56. Takahashi E, Ohki K, Kim DS. 2008. Dissociated pathways for successful memory retrieval from the human parietal cortex: anatomical and functional connectivity analyses. Cereb Cortex. 18:1771-1778. (Pubitemid 352019898)
57. Toro R, Burnod Y. 2005. A morphogenetic model for the development of cortical convolutions. Cereb Cortex. 15:1900-1913. (Pubitemid 41628331)
58. Tuch DS, Reese TG, Wiegell MR, Wedeen VJ. 2003. Diffusion MRI of complex neural architecture. Neuron. 40:885-895. (Pubitemid 37522047)
59. Van Essen D. 1997. A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature. 385:313-318. (Pubitemid 27053095)
60. Van Essen DC, Dierker D, Snyder AZ, Raicle ME, Reiss AL, Korenberg J. 2006. Symmetry of cortical folding abnormalities in Williams syndrome revealed by surface-based analyses. J Neurosci. 26: 5470-5483. (Pubitemid 44318399)
61. Vasung L, Huang H, Jovanov-MiloševićN, Pletikos M, Mori S, KostovićI. 2010. Development of axonal pathways in the human fetal frontolimbic brain: histochemical characterization and diffusion tensor imaging. J Anat. doi: 10.1111/j.1469-7580.2010.01260.x).
62. Vasung L, Jovanov-MiloševićN, Pletikos M, Mori S, JudašM, KostovićI. 2011. Prominent periventricular fiber system related to ganglionic eminence and striatum in the human fetal cerebrum. Brain Struct Funct. 215:237-253.
63. Vishwas M, Chitnis T, Pienaar R, Healy BC, Grant PE. 2010. Tract based analysis of callosal, projection and association pathways in pediatric patients with multiple sclerosis: a preliminary study. Am J Neurodiol. 31:121-128.
64. Volpe JJ. 2008. Neurology of the newborn. 5 ed. Philadelphia (PA): Elsevier Science.
65. Wedeen VJ, Wang RP, Schmahmann JD, Benner T, Tseng WY, Dai G, Pandya DN, Hagmann P, D'Arceuil H, de Crespigny AJ. 2008. Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. Neuroimage. 41:1267-1277.
66. Welker W. 1990. Why does cerebral cortex fissure and fold. In: Jones EG, Peters A, editors. Cerebral cortex. New York: Plenum Press. p. 3-136.
67. Wilkinson M, Hume R, Strange R, Bell JE. 1990. Glial and neuronal differentiation in the human fetal brain 9-23 weeks of gestation. Neuropathol Appl Neurobiol. 16:193-204. (Pubitemid 20222895)
68. White T, Andreasen NC, Nopoulos P, Magnotta V. 2003. Gyrification abnormalities in childhood-and adolescent-onset schizophrenia. Biol Psychiatry. 54:418-426. (Pubitemid 37289448)
69. White T, Su S, Schmidt M, Kao C-Y, Sapio G. 2010. The development of gyrification in childhood and adolescence. Brain Cogn. 72:36-45.
70. Xu G, Knutsen AK, Dikranian K, Kroenke CD, Bayly PV, Taber LA. 2010. Axons pull on the brain, but tension does not drive cortical folding. J Biomech Eng. 132:071013.
71. Zilles K, Schleicher A, Langemann C, Amunts K, Morosan P, Palimero-Gallagher N, Schormann T, Mohlberg H, Bürgel U, Steinmetz H, et al. 1997. Quantitative analysis of sulci in the human cerebral cortex: development, regional heterogeneity, gender difference, asymmetry, intersubject variability, and cortical architecture. Hum Brain Mapp. 5:218-221. (Pubitemid 27375517)