Disrupted developmental organization of the structural connectome in fetuses with corpus callosum agenesis

NeuroImage

Volumn 111, Issue , 2015, Pages 277-288

  Jakab, András ^a   Kasprian, Gregor ^a   Schwartz, Ernst ^a   Gruber, Gerlinde Maria ^b   Mitter, Christian ^a   Prayer, Daniela ^a   Schöpf, Veronika ^a   Langs, Georg ^a,c  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b Medical University of Vienna   (Austria)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Connectome; Corpus callosum agenesis; Corpus callosum hypogenesis; Diffusion tensor imaging; Fetal brain connectivity; Fetal diffusion MRI; Prenatal development

Indexed keywords

ANISOTROPY; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN MALFORMATION; BRAIN REGION; CINGULATE GYRUS; CONNECTOME; CONTROLLED STUDY; CORPUS CALLOSUM AGENESIS; DIFFUSION TENSOR IMAGING; DISEASE ASSOCIATION; FETUS; FETUS DEVELOPMENT; GESTATIONAL AGE; HUMAN; NERVE FIBER; NEUROANATOMY; PARIETAL LOBE; PRIORITY JOURNAL; STREAMLINE TRACTOGRAPHY; SUBCORTEX; TEMPORAL LOBE; THALAMUS; TRACTOGRAPHY; WHITE MATTER; BRAIN; EMBRYOLOGY; FEMALE; FETUS DISEASE; NERVE CELL NETWORK; PATHOLOGY; PREGNANCY; PRENATAL DIAGNOSIS; PROCEDURES;

AGENESIS OF CORPUS CALLOSUM; BRAIN; CONNECTOME; DIFFUSION TENSOR IMAGING; FEMALE; FETAL DEVELOPMENT; FETAL DISEASES; GESTATIONAL AGE; HUMANS; NERVE NET; PREGNANCY; PRENATAL DIAGNOSIS;

EID: 84924189300     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.02.038     Document Type: Article

References (72)

1. Alvarez-hamelin J.I., Barrat A., Vespignani A. Large Scale Networks Fingerprinting and Visualization Using the k-Core Decomposition 2006, 41-50.
2. Barkovich A.J., Guerrini R., Kuzniecky R.I., Jackson G.D., Dobyns W.B. A developmental and genetic classification for malformations of cortical development: update 2012. Brain 2012, 135:1348-1369.
3. Barr M.S., Corballis M.C. The role of the anterior commissure in callosal agenesis. Neuropsychology 2002, 16:459-471.
4. Basser P.J., Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. Ser. B 1996, 111:209-219.
5. Basser P.J., Pajevic S., Pierpaoli C., Duda J., Aldroubi A. In vivo fiber tractography using DT-MRI data. Magn. Reson. Med. 2000, 44:625-632.
6. Beaulieu C. The basis of anisotropic water diffusion in the nervous system? A technical review. NMR Biomed. 2002, 15:435-455.
7. Bedeschi M.F., Bonaglia M.C., Grasso R., Pellegri A., Garghentino R.R., et al. Agenesis of the corpus callosum: clinical and genetic study in 63 young patients. Pediatr. Neurol. 2006, 34:186-193.
8. Behrens T.E.J., Woolrich M.W., Jenkinson M., Johansen-Berg H., Nunes R.G., et al. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn. Reson. Med. 2003, 50:1077-1088.
9. Behrens T.E.J., Berg H.J., Jbabdi S., Rushworth M.F.S., Woolrich M.W. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain?. Neuroimage 2007, 34:144-155.
10. Bloom J., Hynd G. The role of the corpus callosum in interhemispheric transfer of information: excitation or inhibition?. Neuropsychol. Rev. 2005, 15:59-71.
11. Bonneau D., Toutain A., Laquerriere A., Marret S., Saugier-Veber P., et al. X-linked lissencephaly with absent corpus callosum and ambiguous genitalia (XLAG): clinical, magnetic resonance imaging, and neuropathological findings. Ann. Neurol. 2002, 51:340-349.
12. Brown W.S., Jeeves M.A., Dietrich R., Burnison D.S. Bilateral field advantage and evoked potential interhemispheric transmission in commissurotomy and callosal agenesis. Neuropsychologia 1999, 37:1165-1180.
13. Brugger P.C., Stuhr F., Lindner C., Prayer D. Methods of fetal MR: beyond T2-weighted imaging. Eur. J. Radiol. 2006, 57:172-181.
14. Bui T., Daire J.L., Chalard F., Zaccaria I., Alberti C., et al. Microstructural development of human brain assessed in utero by diffusion tensor imaging. Pediatr. Radiol. 2006, 36:1133-1140.
15. Chang L.C., Jones D.K., Pierpaoli C. RESTORE: robust estimation of tensors by outlier rejection. Magn. Reson. Med. 2005, 53:1088-1095.
16. Chung H.W., Chen C.Y., Zimmerman R.A., Lee K.W., Lee C.C., et al. T2-weighted fast MR imaging with true FISP versus HASTE: comparative efficacy in the evaluation of normal fetal brain maturation. AJR Am. J. Roentgenol. 2000, 175:1375-1380.
17. Clarke S., Kraftsik R., Van der Loos H., Innocenti G.M. Forms and measures of adult and developing human corpus callosum: is there sexual dimorphism?. J. Comp. Neurol. 1989, 280:213-230.
18. Comstock C.H., Culp D., Gonzalez J., Boal D.B. Agenesis of the corpus callosum in the fetus: its evolution and significance. J. Ultrasound Med. 1985, 4:613-616.
19. Cook PA, Bai Y, Nedjati-Gilani SK, Seunarine K, Hall MG, et al. (2006).
20. Criminisi A., Sharp T., Blake A. Geos: geodesic image segmentation. Anonymous Computer Vision-ECCV 2008 2008, 99-112. Springer.
21. Dubois J., Dehaene-Lambertz G., Kulikova S., Poupon C., Huppi P.S., et al. The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 2013, 276:48-71.
22. Edwards T.J., Sherr E.H., Barkovich A.J., Richards L.J. Clinical, genetic and imaging findings identify new causes for corpus callosum development syndromes. Brain 2014, 137:1579-1613.
23. Engle E.C. Human genetic disorders of axon guidance. Cold Spring Harb. Perspect. Biol. 2010, 2:a001784.
24. Fields R.D. Myelination: an overlooked mechanism of synaptic plasticity?. Neuroscientist 2005, 11:528-531.
25. Fischer M., Ryan S.B., Dobyns W.B. Mechanisms of interhemispheric transfer and patterns of cognitive function in acallosal patients of normal intelligence. Arch. Neurol. 1992, 49:271-277.
26. Freeman L.C. Centrality in social networks conceptual clarification. Soc. Networks 1979, 1:215-239.
27. Giorgio A., Watkins K.E., Douaud G., James A.C., James S., et al. Changes in white matter microstructure during adolescence. Neuroimage 2008, 39:52-61.
28. Glenn O.A., Barkovich A.J. Magnetic resonance imaging of the fetal brain and spine: an increasingly important tool in prenatal diagnosis, part 1. AJNR Am. J. Neuroradiol. 2006, 27:1604-1611.
29. Gowland P., Fulford J. Initial experiences of performing fetal fMRI. Exp. Neurol. 2004, 190(Supplement 1):22-27.
30. Hagmann P., Cammoun L., Gigandet X., Meuli R., Honey C.J., et al. Mapping the structural core of human cerebral cortex. PLoS Biol. 2008, 6:e159.
31. Harreld J.H., Bhore R., Chason D.P., Twickler D.M. Corpus callosum length by gestational age as evaluated by fetal MR imaging. AJNR Am. J. Neuroradiol. 2011, 32:490-494.
32. Innocenti G.M., Price D.J. Exuberance in the development of cortical networks. Nat. Rev. Neurosci. 2005, 6:955-965.
33. Jenkinson M., Beckmann C.F., Behrens T.E., Woolrich M.W., Smith S.M. Fsl. Neuroimage 2012, 62:782-790.
34. Jeret J.S., Serur D., Wisniewski K., Fisch C. Frequency of agenesis of the corpus callosum in the developmentally disabled population as determined by computerized tomography. Pediatr. Neurosci. 1985, 12:101-103.
35. Jovanov-Milosevic N., Benjak V., Kostovic I. Transient cellular structures in developing corpus callosum of the human brain. Coll. Antropol. 2006, 30:375-381.
36. Kasprian G., Brugger P.C., Weber M., Krssák M., Krampl E., et al. In utero tractography of fetal white matter development. Neuroimage 2008, 43:213-224.
37. Kasprian G., Del Rio M., Prayer D. Fetal diffusion imaging: pearls and solutions. Top. Magn. Reson. Imaging 2010, 21:387-394.
38. Kasprian G., Brugger P.C., Schopf V., Mitter C., Weber M., et al. Assessing prenatal white matter connectivity in commissural agenesis. Brain 2013, 136:168-179.
39. Lefkowitz M., Durand D., Smith G., Silver J. Electrical properties of axons within probst bundles of acallosal mice and callosi that have reformed upon glial-coated polymer implants. Exp. Neurol. 1991, 113:306-313.
40. Lövdén M., Bodammer N.C., Kühn S., Kaufmann J., Schütze H., et al. Experience-dependent plasticity of white-matter microstructure extends into old age. Neuropsychologia 2010, 48:3878-3883.
41. Luders E., Thompson P.M., Toga A.W. The development of the corpus callosum in the healthy human brain. J. Neurosci. 2010, 30:10985-10990.
42. Luttenberg J. Contribution to the fetal ontogenesis of the corpus callosum in man. 3. Myelinization in the corpus callosum. Folia Morphol. (Praha) 1966, 14:192-199.
43. Mailath-Pokorny M., Kasprian G., Mitter C., Schöpf V., Nemec U., et al. Magnetic resonance methods in fetal neurology 2012, 17:278-284.
44. Mitter C., Kasprian G., Brugger P.C., Prayer D. Three-dimensional visualization of fetal white-matter pathways in utero. Ultrasound Obstet. Gynecol. 2011, 37:252-253.
45. Modat M., Ridgway G.R., Taylor Z.A., Lehmann M., Barnes J., et al. Fast free-form deformation using graphics processing units. Comput. Methods Programs Biomed. 2010, 98:278-284.
46. Onnela J., Saramaki J., Kertesz J., Kaski K. Intensity and coherence of motifs in weighted complex networks. Phys. Rev. E 2005, 71:065103.
47. Owen J.P., Li Y.O., Ziv E., Strominger Z., Gold J., et al. The structural connectome of the human brain in agenesis of the corpus callosum. Neuroimage 2013, 70:340-355.
48. Paul L.K., Brown W.S., Adolphs R., Tyszka J.M., Richards L.J., et al. Agenesis of the corpus callosum: genetic, developmental and functional aspects of connectivity. Nat. Rev. Neurosci. 2007, 8:287-299.
49. Prayer D., Kasprian G., Krampl E., Ulm B., Witzani L., et al. MRI of normal fetal brain development. Eur. J. Radiol. 2006, 57:199-216.
50. Prayer D., Brugger P.C., Kasprian G., Witzani L., Helmer H., et al. MRI of fetal acquired brain lesions. Eur. J. Radiol. 2006, 57:233-249.
51. Probst M. Ueber den Bau des vollständig balkenlosen Grosshirnes sowie über Mikrogyrie und Heterotopie der grauen Substanz. Arch. Psychiatr. Nervenkr. 1901, 34:709-777.
52. Pugash D., Brugger P.C., Bettelheim D., Prayer D. Prenatal ultrasound and fetal MRI: the comparative value of each modality in prenatal diagnosis. Eur. J. Radiol. 2008, 68:214-226.
53. Quigley M., Cordes D., Turski P., Moritz C., Haughton V., et al. Role of the corpus callosum in functional connectivity. AJNR Am. J. Neuroradiol. 2003, 24:208-212.
54. Raybaud C. The corpus callosum, the other great forebrain commissures, and the septum pellucidum: anatomy, development, and malformation. Neuroradiology 2010, 52:447-477.
55. Richards L.J., Plachez C., Ren T. Mechanisms regulating the development of the corpus callosum and its agenesis in mouse and human. Clin. Genet. 2004, 66:276-289.
56. Rubinov M., Sporns O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage 2010, 52:1059-1069.
57. Santo S., D'Antonio F., Homfray T., Rich P., Pilu G., et al. Counseling in fetal medicine: agenesis of the corpus callosum. Ultrasound Obstet. Gynecol. 2012, 40:513-521.
58. Sarnat H.B. Embryology and malformations of the forebrain commissures. Handb. Clin. Neurol. 2008, 87:67-87.
59. Scholz J., Klein M.C., Behrens T.E.J., Johansen-Berg H. Training induces changes in white-matter architecture. Nat. Neurosci. 2009, 12:1370-1371.
60. Schöpf V., Kasprian G., Brugger P.C., Prayer D. Watching the fetal brain at 'rest'. Int. J. Dev. Neurosci. 2012, 30:11-17.
61. Sherr E.H., Owen R., Albertson D.G., Pinkel D., Cotter P.D., et al. Genomic microarray analysis identifies candidate loci in patients with corpus callosum anomalies. Neurology 2005, 65:1496-1498.
62. Staudt M. Reorganization after pre- and perinatal brain lesions. J. Anat. 2010, 217:469-474.
63. Tang P.H., Bartha A.I., Norton M.E., Barkovich A.J., Sherr E.H., et al. Agenesis of the corpus callosum: an MR imaging analysis of associated abnormalities in the fetus. AJNR Am. J. Neuroradiol. 2009, 30:257-263.
64. Tomasch J. Size, distribution, and number of fibres in the human corpus callosum. Anat. Rec. 1954, 119:119-135.
65. Tovar-Moll F., Moll J., de Oliveira-Souza R., Bramati I., Andreiuolo P.A., et al. Neuroplasticity in human callosal dysgenesis: a diffusion tensor imaging study. Cereb. Cortex 2007, 17:531-541.
66. Tovar-Moll F., Monteiro M., Andrade J., Bramati I.E., Vianna-Barbosa R., et al. Structural and functional brain rewiring clarifies preserved interhemispheric transfer in humans born without the corpus callosum. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:7843-7848.
67. Utsunomiya H., Yamashita S., Takano K., Okazaki M. Arrangement of fiber tracts forming probst bundle in complete callosal agenesis: report of two cases with an evaluation by diffusion tensor tractography. Acta Radiol. 2006, 47:1063-1066.
68. Vergani P., Ghidini A., Strobelt N., Locatelli A., Mariani S., et al. Prognostic indicators in the prenatal diagnosis of agenesis of corpus callosum. Am. J. Obstet. Gynecol. 1994, 170:753-758.
69. Wahl M., Strominger Z., Jeremy R.J., Barkovich A.J., Wakahiro M., et al. Variability of homotopic and heterotopic callosal connectivity in partial agenesis of the corpus callosum: a 3T diffusion tensor imaging and Q-ball tractography study. AJNR Am. J. Neuroradiol. 2009, 30:282-289.
70. Watts D.J., Strogatz S.H. Collective dynamics of 'small-world' networks. Nature 1998, 393:440-442.
71. Xia M., Wang J., He Y. BrainNet viewer: a network visualization tool for human brain connectomics. PLoS ONE 2013, 8:e68910.
72. Zalesky A., Fornito A., Bullmore E.T. Network-based statistic: identifying differences in brain networks. Neuroimage 2010, 53:1197-1207.