Human cortical connectome reconstruction from diffusion weighted MRI: The effect of tractography algorithm

NeuroImage

Volumn 62, Issue 3, 2012, Pages 1732-1749

  Bastiani, Matteo ^a,b   Shah, Nadim Jon ^a,b,c   Goebel, Rainer ^a   Roebroeck, Alard ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Diffusion weighted magnetic resonance imaging; Human connectome; Quality control; Structural network analysis; Tract specific density coefficient; Tractography

Indexed keywords

ADULT; ALGORITHM; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DIFFUSION WEIGHTED IMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE RECONSTRUCTION; INTERMETHOD COMPARISON; MALE; NERVE CELL NETWORK; NERVE FIBER; NORMAL HUMAN; PRIORITY JOURNAL; PROBABILITY; QUALITY CONTROL; RADIOLOGICAL PARAMETERS; RADIOSENSITIVITY; SENSITIVITY AND SPECIFICITY; STRUCTURE ANALYSIS; TRACTOGRAPHY ALGORITHM; VALIDATION STUDY;

ADULT; ALGORITHMS; CEREBRAL CORTEX; CONNECTOME; DIFFUSION TENSOR IMAGING; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MALE; NEURAL PATHWAYS;

EID: 84863529550     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.06.002     Document Type: Article

References (70)

1. Achard S., Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput. Biol. 2007, 3:e17.
2. Aganj I., Lenglet C., Jahanshad N., Yacoub E., Harel N., Thompson P.M., Sapiro G. A Hough transform global probabilistic approach to multiple-subject diffusion MRI tractography. Med. Image Anal. 2011, 15:414-425.
3. Assaf Y., Basser P.J. Composite hindered and restricted model of diffusion (CHARMED) MR imaging of the human brain. NeuroImage 2005, 27:48-58.
4. Basser P.J., Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. B 1996, 111:209-219.
5. Basser P.J., Mattiello J., LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys. J. 1994, 66:259-267.
6. 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.
7. Bassett D.S., Brown J.A., Deshpande V., Carlson J.M., Grafton S.T. Conserved and variable architecture of human white matter connectivity. NeuroImage 2011, 54:1262-1279.
8. Bassett D.S., Wymbs N.F., Porter M.A., Mucha P.J., Carlson J.M., Grafton S.T. Dynamic reconfiguration of human brain networks during learning. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:7641-7646.
9. Behrens T.E., Woolrich M.W., Jenkinson M., Johansen-Berg H., Nunes R.G., Clare S., Matthews P.M., Brady J.M., Smith S.M. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn. Reson. Med. 2003, 50:1077-1088.
10. Behrens T.E., Berg H.J., Jbabdi S., Rushworth M.F., Woolrich M.W. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain?. NeuroImage 2007, 34:144-155.
11. Cammoun L., Gigandet X., Meskaldji D., Thiran J.P., Sporns O., Do K.Q., Maeder P., Meuli R., Hagmann P. Mapping the human connectome at multiple scales with diffusion spectrum MRI. J. Neurosci. Methods 2012, 203:386-397.
12. Catani M., Thiebaut de Schotten M. A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 2008, 44:1105-1132.
13. Cheng H., Wang Y., Sheng J., Sporns O., Kronenberger W.G., Mathews V.P., Hummer T.A., Saykin A.J. Optimization of seed density in DTI tractography for structural networks. J. Neurosci. Methods 2011, 203(1):264-272.
14. Conturo T.E., Lori N.F., Cull T.S., Akbudak E., Snyder A.Z., Shimony J.S., McKinstry R.C., Burton H., Raichle M.E. Tracking neuronal fiber pathways in the living human brain. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:10422-10427.
15. Cook P.A., Bai Y., Nedjati-Gilani S., Seunarine K.K., Hall M.G., Parker G.J., Alexander D.C. Camino: open-source diffusion-MRI reconstruction and processing. 14th Scientific Meeting of the International Society for Magnetic Resonance in Medicine, Seattle, WA, USA 2006.
16. Du Q., Gunzburger M.D., Ju L.L. Constrained centroidal Voronoi tessellations for surfaces. SIAM J. Sci. Comput. 2003, 24:1488-1506.
17. Feinberg D.A., Moeller S., Smith S.M., Auerbach E., Ramanna S., Gunther M., Glasser M.F., Miller K.L., Ugurbil K., Yacoub E. Multiplexed echo planar imaging for sub-second whole brain FMRI and fast diffusion imaging. PLoS One 2010, 5:e15710.
18. Ffytche D.H., Blom J.D., Catani M. Disorders of visual perception. J. Neurol. Neurosurg. Psychiatry 2010, 81:1280-1287.
19. Fillard P., Descoteaux M., Goh A., Gouttard S., Jeurissen B., Malcolm J., Ramirez-Manzanares A., Reisert M., Sakaie K., Tensaouti F., Yo T., Mangin J.F., Poupon C. Quantitative evaluation of 10 tractography algorithms on a realistic diffusion MR phantom. NeuroImage 2011, 56:220-234.
20. Frank L.R. Anisotropy in high angular resolution diffusion-weighted MRI. Magn. Reson. Med. 2001, 45:935-939.
21. Goebel R., Esposito F., Formisano E. Analysis of functional image analysis contest (FIAC) data with BrainVoyager QX: from single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Hum. Brain Mapp. 2006, 27:392-401.
22. Gong G., Rosa-Neto P., Carbonell F., Chen Z.J., He Y., Evans A.C. Age- and gender-related differences in the cortical anatomical network. J. Neurosci. 2009, 29:15684-15693.
23. Hagmann P., Kurant M., Gigandet X., Thiran P., Wedeen V.J., Meuli R., Thiran J.P. Mapping human whole-brain structural networks with diffusion MRI. PLoS One 2007, 2:e597.
24. Hagmann P., Cammoun L., Gigandet X., Meuli R., Honey C.J., Wedeen V.J., Sporns O. Mapping the structural core of human cerebral cortex. PLoS Biol. 2008, 6:e159.
25. Heidemann R.M., Porter D.A., Anwander A., Feiweier T., Heberlein K., Knosche T.R., Turner R. Diffusion imaging in humans at 7T using readout-segmented EPI and GRAPPA. Magn. Reson. Med. 2010, 64:9-14.
26. Iturria-Medina Y., Canales-Rodriguez E.J., Melie-Garcia L., Valdes-Hernandez P.A., Martinez-Montes E., Aleman-Gomez Y., Sanchez-Bornot J.M. Characterizing brain anatomical connections using diffusion weighted MRI and graph theory. NeuroImage 2007, 36:645-660.
27. Iturria-Medina Y., Perez Fernandez A., Morris D.M., Canales-Rodriguez E.J., Haroon H.A., Garcia Penton L., Augath M., Galan Garcia L., Logothetis N., Parker G.J., Melie-Garcia L. Brain hemispheric structural efficiency and interconnectivity rightward asymmetry in human and nonhuman primates. Cereb. Cortex 2011, 21:56-67.
28. Jarbo K., Verstynen T., Schneider W. In vivo quantification of global connectivity in the human corpus callosum. NeuroImage 2012, 59:1988-1996.
29. Jbabdi S., Johansen-Berg H. Tractography: where do we go from here?. Brain Connect. 2011, 1:169-183.
30. Jbabdi S., Woolrich M.W., Andersson J.L., Behrens T.E. A Bayesian framework for global tractography. NeuroImage 2007, 37:116-129.
31. Jeurissen B., Leemans A., Jones D.K., Tournier J.D., Sijbers J. Probabilistic fiber tracking using the residual bootstrap with constrained spherical deconvolution. Hum. Brain Mapp. 2011, 32:461-479.
32. Jones D.K. Studying connections in the living human brain with diffusion MRI. Cortex 2008, 44:936-952.
33. Jones D.K. Tractography gone wild: probabilistic fibre tracking using the wild bootstrap with diffusion tensor MRI. IEEE Trans. Med. Imaging 2008, 27:1268-1274.
34. Jones D.K. Challenges and limitations of quantifying brain connectivity in vivo with diffusion MRI. Imaging Med. 2010, 2:341-355.
35. Lazar M., Weinstein D.M., Tsuruda J.S., Hasan K.M., Arfanakis K., Meyerand M.E., Badie B., Rowley H.A., Haughton V., Field A., Alexander A.L. White matter tractography using diffusion tensor deflection. Hum. Brain Mapp. 2003, 18:306-321.
36. Leemans A., Jones D.K. The B-matrix must be rotated when correcting for subject motion in DTI data. Magn. Reson. Med. 2009, 61:1336-1349.
37. Li L., Rilling J.K., Preuss T.M., Glasser M.F., Hu X. The effects of connection reconstruction method on the interregional connectivity of brain networks via diffusion tractography. Hum. Brain Mapp. 2011, (Electronic publication ahead of print) http://dx.doi.org/10.1002/hbm.21332.
38. Liu C., Bammer R., Acar B., Moseley M.E. Characterizing non-Gaussian diffusion by using generalized diffusion tensors. Magn. Reson. Med. 2004, 51:924-937.
39. Mori S., Crain B.J., Chacko V.P., van Zijl P.C. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann. Neurol. 1999, 45:265-269.
40. Morris D.M., Embleton K.V., Parker G.J. Probabilistic fibre tracking: differentiation of connections from chance events. NeuroImage 2008, 42:1329-1339.
41. Ozarslan E., Mareci T.H. Generalized diffusion tensor imaging and analytical relationships between diffusion tensor imaging and high angular resolution diffusion imaging. Magn. Reson. Med. 2003, 50:955-965.
42. Ozarslan E., Shepherd T.M., Vemuri B.C., Blackband S.J., Mareci T.H. Resolution of complex tissue microarchitecture using the diffusion orientation transform (DOT). NeuroImage 2006, 31:1086-1103.
43. Parker G.J., Alexander D.C. Probabilistic anatomical connectivity derived from the microscopic persistent angular structure of cerebral tissue. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360:893-902.
44. Parker G.J., Haroon H.A., Wheeler-Kingshott C.A. 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.
45. Ramayya A.G., Glasser M.F., Rilling J.K. A DTI investigation of neural substrates supporting tool use. Cereb. Cortex 2010, 20:507-516.
46. Roebroeck A., Galuske R., Formisano E., Chiry O., Bratzke H., Ronen I., Kim D.S., Goebel R. High-resolution diffusion tensor imaging and tractography of the human optic chiasm at 9.4T. NeuroImage 2008, 39:157-168.
47. Rubinov M., Sporns O. Complex network measures of brain connectivity: uses and interpretations. NeuroImage 2010, 52:1059-1069.
48. Schultz T., Seidel H.P. Estimating crossing fibers: a tensor decomposition approach. IEEE Trans. Vis. Comput. Graph. 2008, 14:1635-1642.
49. Sherbondy A.J., Dougherty R.F., Ben-Shachar M., Napel S., Wandell B.A. ConTrack: finding the most likely pathways between brain regions using diffusion tractography. J. Vis. 2008, 8(15):11-16.
50. Sherbondy A.J., Dougherty R.F., Ananthanarayanan R., Modha D.S., Wandell B.A. Think global, act local; projectome estimation with BlueMatter. Med. Image Comput. Comput. Assist. Interv. 2009, 12:861-868.
51. Sotiropoulos S.N., Bai L., Morgan P.S., Constantinescu C.S., Tench C.R. Brain tractography using Q-ball imaging and graph theory: improved connectivities through fibre crossings via a model-based approach. NeuroImage 2010, 49:2444-2456.
52. Sporns O., Tononi G., Kotter R. The human connectome: a structural description of the human brain. PLoS Comput. Biol. 2005, 1:e42.
53. Thiebaut de Schotten M., Dell'Acqua F., Forkel S.J., Simmons A., Vergani F., Murphy D.G., Catani M. A lateralized brain network for visuospatial attention. Nat. Neurosci. 2011, 14:1245-1246.
54. Tournier J.D., Calamante F., Gadian D.G., Connelly A. Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution. NeuroImage 2004, 23:1176-1185.
55. Tournier J.D., Calamante F., Connelly A. Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. NeuroImage 2007, 35:1459-1472.
56. Tournier J.D., Calamante F., Connelly A. Improved probabilistic streamlines tractography by 2nd order integration over fibre orientation distributions. Proceedings of the Joint Annual Meeting ISMRM-ESMRMB 2010, Stockholm, Sweden 2010.
57. Tuch D.S. Q-ball imaging. Magn. Reson. Med. 2004, 52:1358-1372.
58. Tuch D.S., Reese T.G., Wiegell M.R., Makris N., Belliveau J.W., Wedeen V.J. High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity. Magn. Reson. Med. 2002, 48:577-582.
59. Tuch D.S., Reese T.G., Wiegell M.R., Wedeen V.J. Diffusion MRI of complex neural architecture. Neuron 2003, 40:885-895.
60. van Wijk B.C., Stam C.J., Daffertshofer A. Comparing brain networks of different size and connectivity density using graph theory. PLoS One 2010, 5:e13701.
61. Wakana S., Jiang H., Nagae-Poetscher L.M., van Zijl P.C., Mori S. Fiber tract-based atlas of human white matter anatomy. Radiology 2004, 230:77-87.
62. Watts D.J., Strogatz S.H. Collective dynamics of 'small-world' networks. Nature 1998, 393:440-442.
63. Wedeen V.J., Hagmann P., Tseng W.Y., Reese T.G., Weisskoff R.M. Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn. Reson. Med. 2005, 54:1377-1386.
64. Wedeen V.J., Wang R.P., Schmahmann J.D., Benner T., Tseng W.Y., Dai G., Pandya D.N., Hagmann P., D'Arceuil H., de Crespigny A.J. Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. NeuroImage 2008, 41:1267-1277.
65. Westin C.F., Maier S.E., Mamata H., Nabavi A., Jolesz F.A., Kikinis R. Processing and visualization for diffusion tensor MRI. Med. Image Anal. 2002, 6:93-108.
66. Yeh F.C., Wedeen V.J., Tseng W.Y. Generalized q-sampling imaging. IEEE Trans. Med. Imaging 2010, 29:1626-1635.
67. Zalesky A. DT-MRI fiber tracking: a shortest paths approach. IEEE Trans. Med. Imaging 2008, 27:1458-1471.
68. Zalesky A., Fornito A. A DTI-derived measure of cortico-cortical connectivity. IEEE Trans. Med. Imaging 2009, 28:1023-1036.
69. Zalesky A., Fornito A., Harding I.H., Cocchi L., Yucel M., Pantelis C., Bullmore E.T. Whole-brain anatomical networks: does the choice of nodes matter?. NeuroImage 2010, 50:970-983.
70. Zhang Y., Brady M., Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imaging 2001, 20:45-57.