Unraveling the multiscale structural organization and connectivity of the human brain: The role of diffusion MRI

Frontiers in Neuroanatomy

Volumn 9, Issue June, 2015, Pages

  Bastiani, Matteo ^a   Roebroeck, Alard ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Cortical layers and areas; Cytoarchitecture; Diffusion MRI; Myeloachtecture; Structural connectivity

Indexed keywords

ANATOMICAL CONCEPTS; APPARENT DIFFUSION COEFFICIENT; ARTICLE; BRAIN; CYTOARCHITECTURE; DIFFUSION TENSOR IMAGING; DIFFUSION WEIGHTED IMAGING; HUMAN; NEUROANATOMY; NEUROIMAGING; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; RADIOLOGICAL PARAMETERS; STRUCTURAL ARCHITECTURE; TRACTOGRAPHY;

EID: 84935883412     PISSN: None     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2015.00077     Document Type: Article

References (135)

1. Aboitiz, F., Scheibel, A. B., Fisher, R. S., and Zaidel, E. (1992). Fiber composition of the human corpus callosum. Brain Res. 598, 143-153. doi: 10.1016/0006-8993(92)90178-C
2. Alexander, D. C., Barker, G. J., and Arridge, S. R. (2002). Detection and modeling of non-Gaussian apparent diffusion coefficient profiles in human brain data. Magn. Reson. Med. 48, 331-340. doi: 10.1002/mrm.10209
3. Alexander, D. C., Hubbard, P. L., Hall, M. G., Moore, E. A., Ptito, M., Parker, G. J., et al. (2010). Orientationally invariant indices of axon diameter and density from diffusion MRI. Neuroimage 52, 1374-1389. doi: 10.1016/j.neuroimage.2010.05.043
4. Amunts, K., Lenzen, M., Friederici, A. D., Schleicher, A., Morosan, P., Palomero-Gallagher, N., et al. (2010). Broca’s region: novel organizational principles and multiple receptor mapping. PLoS Biol. 8:e1000489. doi: 10.1371/journal.pbio.1000489
5. Amunts, K., Lepage, C., Borgeat, L., Mohlberg, H., Dickscheid, T., Rousseau, M. E., et al. (2013). BigBrain: an ultrahigh-resolution 3D human brain model. Science 340, 1472-1475. doi: 10.1126/science.1235381
6. Assaf, Y., and Basser, P. J. (2005). Composite hindered and restricted model of diffusion (CHARMED) MR imaging of the human brain. Neuroimage 27, 48-58. doi: 10.1016/j.neuroimage.2005.03.042
7. Assaf, Y., Blumenfeld-Katzir, T., Yovel, Y., and Basser, P. J. (2008). AxCaliber: a method for measuring axon diameter distribution from diffusion MRI. Magn. Reson. Med. 59, 1347-1354. doi: 10.1002/mrm.21577
8. Axer, H., Axer, M., Krings, T., and Keyserlingk, D. G. (2001). Quantitative estimation of 3-D fiber course in gross histological sections of the human brain using polarized light. J. Neurosci. Methods 105, 121-131. doi: 10.1016/S0165-0270(00)00349-6
9. Axer, H., Beck, S., Schuchardt, F., Heepe, J., Flücken, A., Axer, M., et al. (2011a). Microstructural analysis of human white matter architecture using polarized light imaging: views from neuroanatomy. Front. Neuroinform. 5:28. doi: 10.3389/fninf.2011.00028
10. Axer, M., Grassel, D., Kleiner, M., Dammers, J., Dickscheid, T., Reckfort, J., et al. (2011b). High-resolution fiber tract reconstruction in the human brain by means of three-dimensional polarized light imaging. Front. Neuroinform. 5:34. doi: 10.3389/fninf.2011.00034
11. Axer, H., and Keyserlingk, D. G. (2000). Mapping of fiber orientation in human internal capsule by means of polarized light and confocal scanning laser microscopy. J. Neurosci. Methods 94, 165-175. doi: 10.1016/S0165-0270(99)00132-6
12. Bakker, R., Wachtler, T., and Diesmann, M. (2012). CoCoMac 2.0 and the future of tract-tracing databases. Front. Neuroinform. 6:30. doi: 10.3389/fninf.2012.00030
13. Barazany, D., Basser, P. J., and Assaf, Y. (2009). In vivo measurement of axon diameter distribution in the corpus callosum of rat brain. Brain 132, 1210-1220. doi: 10.1093/brain/awp042
14. Basser, P. J., Mattiello, J., and Lebihan, D. (1994). MR diffusion tensor spectroscopy and imaging. Biophys. J. 66, 259-267. doi: 10.1016/S0006-3495(94)80775-1
15. Basser, P. J., Pajevic, S., Pierpaoli, C., Duda, J., and Aldroubi, A. (2000). In vivo fiber tractography using DT-MRI data. Magn. Reson. Med. 44, 625-632. doi: 10.1002/1522-2594(200010)44:4<625::AID-MRM17>3.0.CO;2-O
16. Basser, P. J., and Pierpaoli, C. (1996). Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. B 111, 209-219. doi: 10.1006/jmrb.1996.0086
17. Bastiani, M., Shah, N. J., Goebel, R., and Roebroeck, A. (2012). Human cortical connectome reconstruction from diffusion weighted MRI: the effect of tractography algorithm. Neuroimage 62, 1732-1749. doi: 10.1016/j.neuroimage.2012.06.002
18. Behrens, T. E., Berg, H. J., Jbabdi, S., Rushworth, M. F., and Woolrich, M. W. (2007). Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34, 144-155. doi: 10.1016/j.neuroimage.2006.09.018
19. Behrens, T. E., Johansen-Berg, H., Woolrich, M. W., Smith, S. M., Wheeler-Kingshott, C. A., Boulby, P. A., et al. (2003a). Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat. Neurosci. 6, 750-757. doi: 10.1038/nn1075
20. Behrens, T. E., Woolrich, M. W., Jenkinson, M., Johansen-Berg, H., Nunes, R. G., Clare, S., et al. (2003b). Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn. Reson. Med. 50, 1077-1088. doi: 10.1002/mrm.10609
21. Bells, S., Cercignani, M., Deoni, S., Assaf, Y., Pasternak, O., Evans, C. J., et al. (2011). "Tractometry: comprehensive multi-modal quantitative assessment of white matter along specific tracts," in Proceedings of the 19th Annual Meeting of International Society for Magnetic Resonance in Medicine, Montreal, QC.
22. Bezgin, G., Vakorin, V. A., Van Opstal, A. J., Mcintosh, A. R., and Bakker, R. (2012). Hundreds of brain maps in one atlas: registering coordinate-independent primate neuro-anatomical data to a standard brain. Neuroimage 62, 67-76. doi: 10.1016/j.neuroimage.2012.04.013
23. Bonin, G. V., and Bailey, P. (1947). The Neocortex of Macaca Mulatta. Urbana: University of Illinois Press.
24. Bressler, S. L., and Menon, V. (2010). Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn. Sci. 14, 277-290. doi: 10.1016/j.tics.2010.04.004
25. Brodmann, K. (1909). Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: Johann Ambrosius Barth.
26. Callaghan, P. T., Eccles, C. D., and Xia, Y. (1988). NMR microscopy of dynamic displacements: k-space and q-space imaging. J. Phys. E Sci. Instrum. 21, 820. doi: 10.1088/0022-3735/21/8/017
27. Campbell, J. S., Momayyezsiahkal, P., Savadjiev, P., Leppert, I. R., Siddiqi, K., and Pike, G. B. (2014). Beyond crossing fibers: bootstrap probabilistic tractography using complex subvoxel fiber geometries. Front. Neurol. 5:216. doi: 10.3389/fneur.2014.00216
28. Caspers, S., Axer, M., Caspers, J., Jockwitz, C., Jütten, K., Reckfort, J., et al. (2015). Target sites for transcallosal fibers in human visual cortex - a combined diffusion and polarized light imaging study. Cortex doi: 10.1016/j.cortex.2015.01.009 [Epub ahead of print].
29. Catani, M., Dell’acqua, F., Vergani, F., Malik, F., Hodge, H., Roy, P., et al. (2012). Short frontal lobe connections of the human brain. Cortex 48, 273-291. doi: 10.1016/j.cortex.2011.12.001
30. Catani, M., Howard, R. J., Pajevic, S., and Jones, D. K. (2002). Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17, 77-94. doi: 10.1006/nimg.2002.1136
31. Catani, M., and Thiebaut de Schotten, M. (2008). A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44, 1105-1132. doi: 10.1016/j.cortex.2008.05.004
32. Catani, M., Thiebaut De Schotten, M., Slater, D., and Dell’acqua, F. (2013). Connectomic approaches before the connectome. Neuroimage 80, 2-13. doi: 10.1016/j.neuroimage.2013.05.109
33. Chomiak, T., and Hu, B. (2009). What is the optimal value of the g-Ratio for myelinated fibers in the rat CNS? A theoretical approach. PLoS ONE 4:e7754. doi: 10.1371/journal.pone.0007754
34. Chung, K., and Deisseroth, K. (2013). CLARITY for mapping the nervous system. Nat. Methods 10, 508-513. doi: 10.1038/nmeth.2481
35. Conturo, T. E., Lori, N. F., Cull, T. S., Akbudak, E., Snyder, A. Z., Shimony, J. S., et al. (1999). Tracking neuronal fiber pathways in the living human brain. Proc. Natl. Acad. Sci. U.S.A. 96, 10422-10427. doi: 10.1073/pnas.96.18.10422
36. Craddock, R. C., Jbabdi, S., Yan, C. G., Vogelstein, J. T., Castellanos, F. X., Di Martino, A., et al. (2013). Imaging human connectomes at the macroscale. Nat. Methods 10, 524-539. doi: 10.1038/nmeth.2482
37. D’Arceuil, H., and de Crespigny, A. (2007). The effects of brain tissue decomposition on diffusion tensor imaging and tractography. Neuroimage 36, 64-68. doi: 10.1016/j.neuroimage.2007.02.039
38. D’Arceuil, H. E., Westmoreland, S., and De Crespigny, A. J. (2007). An approach to high resolution diffusion tensor imaging in fixed primate brain. Neuroimage 35, 553-565. doi: 10.1016/j.neuroimage.2006.12.028
39. da Costa, N. M., and Martin, K. A. (2010). Whose cortical column would that be? Front. Neuroanat. 4:16. doi: 10.3389/fnana.2010.00016
40. Dammers, J., Axer, M., Grassel, D., Palm, C., Zilles, K., Amunts, K., et al. (2010). Signal enhancement in polarized light imaging by means of independent component analysis. Neuroimage 49, 1241-1248. doi: 10.1016/j.neuroimage.2009.08.059
41. Dammers, J., Breuer, L., Axer, M., Kleiner, M., Eiben, B., Grassel, D., et al. (2012). Automatic identification of gray and white matter components in polarized light imaging. Neuroimage 59, 1338-1347. doi: 10.1016/j.neuroimage.2011.08.030
42. Dong, Q., Welsh, R. C., Chenevert, T. L., Carlos, R. C., Maly-Sundgren, P., Gomez-Hassan, D. M., et al. (2004). Clinical applications of diffusion tensor imaging. J. Magn. Reson. Imaging 19, 6-18. doi: 10.1002/jmri.10424
43. Eickhoff, S. B., Rottschy, C., Kujovic, M., Palomero-Gallagher, N., and Zilles, K. (2008). Organizational principles of human visual cortex revealed by receptor mapping. Cereb. Cortex 18, 2637-2645. doi: 10.1093/cercor/bhn024
44. Einstein, A. (1905). Über die von der molekularkinetischen theorie der wärme geforderte bewegung von in ruhenden flüssigkeiten suspendierten teilchen. Ann. Phys. 322, 549-560. doi: 10.1002/andp.19053220806
45. Felleman, D. J., and Van Essen, D. C. (1991). Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1-47. doi: 10.1093/cercor/1.1.1
46. Frank, L. R. (2002). Characterization of anisotropy in high angular resolution diffusion-weighted MRI. Magn. Reson. Med. 47, 1083-1099. doi: 10.1002/mrm.10156
47. Fuster, J. M. (2005). "Neurobiology of cortical networks," in Cortex and Mind (New York, NY: Oxford University Press). doi: 10.1093/acprof:oso/9780195300840.001.0001
48. Geyer, S., Matelli, M., Luppino, G., Schleicher, A., Jansen, Y., Palomero-Gallagher, N., et al. (1998). Receptor autoradiographic mapping of the mesial motor and premotor cortex of the macaque monkey. J. Comp. Neurol. 397, 231-250. doi: 10.1002/(SICI)1096-9861(19980727)397:2<231::AID-CNE6>3.0.CO;2-1
49. Gorbach, N. S., Schutte, C., Melzer, C., Goldau, M., Sujazow, O., Jitsev, J., et al. (2011). Hierarchical information-based clustering for connectivity-based cortex parcellation. Front. Neuroinform. 5:18. doi: 10.3389/fninf.2011.00018
50. Goulas, A., Bastiani, M., Bezgin, G., Uylings, H. B., Roebroeck, A., and Stiers, P. (2014). Comparative analysis of the macroscale structural connectivity in the macaque and human brain. PLoS Comput. Biol. 10:e1003529. doi: 10.1371/journal.pcbi.1003529
51. Hagmann, P., Cammoun, L., Gigandet, X., Meuli, R., Honey, C. J., Wedeen, V. J., et al. (2008). Mapping the structural core of human cerebral cortex. PLoS Biol. 6:e159. doi: 10.1371/journal.pbio.0060159
52. Hagmann, P., Jonasson, L., Maeder, P., Thiran, J. P., Wedeen, V. J., and Meuli, R. (2006). Understanding diffusion MR imaging techniques: from scalar diffusion- weighted imaging to diffusion tensor imaging and beyond. Radiographics 26(Suppl. 1), S205-S223. doi: 10.1148/rg.26si065510
53. Hellwig, B. (1993). How the myelin picture of the human cerebral cortex can be computed from cytoarchitectural data. a bridge between von economo and vogt. J. Hirnforsch. 34, 387-402.
54. Horton, J. C., and Adams, D. L. (2005). The cortical column: a structure without a function. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 837-862. doi: 10.1098/rstb.2005.1623
55. Huang, D., Swanson, E. A., Lin, C. P., Schuman, J. S., Stinson, W. G., Chang, W., et al. (1991). Optical coherence tomography. Science 254, 1178-1181. doi: 10.1126/science.1957169
56. Hubel, D. H., and Wiesel, T. N. (1962). Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J. Physiol. 160, 106-154. doi: 10.1113/jphysiol.1962.sp006837
57. Hubel, D. H., and Wiesel, T. N. (1968). Receptive fields and functional architecture of monkey striate cortex. J. Physiol. 195, 215-243. doi: 10.1113/jphysiol.1968.sp008455
58. Iturria-Medina, Y., Canales-Rodriguez, E. J., Melie-Garcia, L., Valdes-Hernandez, P. A., Martinez-Montes, E., Aleman-Gomez, Y., et al. (2007). Characterizing brain anatomical connections using diffusion weighted MRI and graph theory. Neuroimage 36, 645-660. doi: 10.1016/j.neuroimage.2007.02.012
59. Jansons, K. M., and Alexander, D. C. (2003). Persistent Angular Structure: new insights from diffusion MRI data. Dummy version. Inf. Process. Med. Imaging 18, 672-683. doi: 10.1007/978-3-540-45087-0_56
60. Jbabdi, S., and Johansen-Berg, H. (2011). Tractography: where do we go from here? Brain Connect. 1, 169-183. doi: 10.1089/brain.2011.0033
61. Jbabdi, S., Woolrich, M. W., Andersson, J. L., and Behrens, T. E. (2007). A Bayesian framework for global tractography. Neuroimage 37, 116-129. doi: 10.1016/j.neuroimage.2007.04.039
62. Jeurissen, B., Leemans, A., Tournier, J. D., Jones, D. K., and Sijbers, J. (2013). Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Hum. Brain Mapp. 34, 2747-2766. doi: 10.1002/hbm.22099
63. Jones, D. K. (2003). Determining and visualizing uncertainty in estimates of fiber orientation from diffusion tensor MRI. Magn. Reson. Med. 49, 7-12. doi: 10.1002/mrm.10331
64. Jones, D. K. (2010). Challenges and limitations of quantifying brain connectivity in vivo with diffusion MRI. Imaging Med. 2, 341-355. doi: 10.2217/iim.10.21
65. Jones, E. G. (1981). "Anatomy of cerebral cortex: columnar input-output organization," in The Organization of the Cerebral Cortex, eds F. O. Schmitt, F. G. Worden, G. Adelman, and S. G. Dennis (Cambridge, MA: MIT Press).
66. Khayal, I. S., Vandenberg, S. R., Smith, K. J., Cloyd, C. P., Chang, S. M., Cha, S., et al. (2011). MRI apparent diffusion coefficient reflects histopathologic subtype, axonal disruption, and tumor fraction in diffuse-type grade II gliomas. Neuro Oncol. 13, 1192-1201. doi: 10.1093/neuonc/nor122
67. Kleiner, M., Axer, M., Grassell, D., Reckfort, J., Pietrzyk, U., Amunts, K., et al. (2012). Classification of ambiguous nerve fiber orientations in 3D polarized light imaging. Med. Image Comput. Comput. Assist. Interv. 15, 206-213. doi: 10.1007/978-3-642-33415-3_26
68. Kleinnijenhuis, M., Zerbi, V., Kusters, B., Slump, C. H., Barth, M., and Van Cappellen Van Walsum, A. M. (2013). Layer-specific diffusion weighted imaging in human primary visual cortex in vitro. Cortex 49, 2569-2582. doi: 10.1016/j.cortex.2012.11.015
69. Kotter, R., and Wanke, E. (2005). Mapping brains without coordinates. Philos. Trans. R. Soc. B Biol. Sci. 360, 751-766. doi: 10.1098/rstb.2005.1625
70. Kreher, B. W., Mader, I., and Kiselev, V. G. (2008). Gibbs tracking: a novel approach for the reconstruction of neuronal pathways. Magn. Reson. Med. 60, 953-963. doi: 10.1002/mrm.21749
71. Lamantia, A. S., and Rakic, P. (1990). Cytological and quantitative characteristics of four cerebral commissures in the rhesus monkey. J. Comp. Neurol. 291, 520-537. doi: 10.1002/cne.902910404
72. Larsen, L., Griffin, L. D., Grassel, D., Witte, O. W., and Axer, H. (2007). Polarized light imaging of white matter architecture. Microsc. Res. Tech. 70, 851-863. doi: 10.1002/jemt.20488
73. Leuze, C. W., Anwander, A., Bazin, P. L., Dhital, B., Stuber, C., Reimann, K., et al. (2014). Layer-specific intracortical connectivity revealed with diffusion MRI. Cereb. Cortex 24, 328-339. doi: 10.1093/cercor/bhs311
74. Li, L., Rilling, J. K., Preuss, T. M., Glasser, M. F., and Hu, X. (2012). The effects of connection reconstruction method on the interregional connectivity of brain networks via diffusion tractography. Hum. Brain Mapp. 33, 1894-1913. doi: 10.1002/hbm.21332
75. Magnain, C., Augustinack, J. C., Reuter, M., Wachinger, C., Frosch, M. P., Ragan, T., et al. (2014). Blockface histology with optical coherence tomography: a comparison with Nissl staining. Neuroimage 84, 524-533. doi: 10.1016/j.neuroimage.2013.08.072
76. Markov, N. T., and Kennedy, H. (2013). The importance of being hierarchical. Curr. Opin. Neurobiol. 23, 187-194. doi: 10.1016/j.conb.2012.12.008
77. Markov, N. T., Misery, P., Falchier, A., Lamy, C., Vezoli, J., Quilodran, R., et al. (2011). Weight consistency specifies regularities of macaque cortical networks. Cereb. Cortex 21, 1254-1272. doi: 10.1093/cercor/bhq201
78. Mars, R. B., Jbabdi, S., Sallet, J., O’Reilly, J. X., Croxson, P. L., Olivier, E., et al. (2011). Diffusion-weighted imaging tractography-based parcellation of the human parietal cortex and comparison with human and macaque resting-state functional connectivity. J. Neurosci. 31, 4087-4100. doi: 10.1523/JNEUROSCI.5102-10.2011
79. McKinstry, R. C., Mathur, A., Miller, J. H., Ozcan, A., Snyder, A. Z., Schefft, G. L., et al. (2002). Radial organization of developing preterm human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. Cereb. Cortex 12, 1237-1243. doi: 10.1093/cercor/12.12.1237
80. Miller, K. L., Stagg, C. J., Douaud, G., Jbabdi, S., Smith, S. M., Behrens, T. E., et al. (2011). Diffusion imaging of whole, post-mortem human brains on a clinical MRI scanner. Neuroimage 57, 167-181. doi: 10.1016/j.neuroimage.2011.03.070
81. Morell, P. (1984). Myelin. New York: Plenum Press. doi: 10.1007/978-1-4757-1830-0
82. Mori, S., Crain, B. J., Chacko, V. P., and Van Zijl, P. C. (1999). Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann. Neurol. 45, 265-269. doi: 10.1002/1531-8249(199902)45:2<265::AID-ANA21>3.0.CO;2-3
83. Mori, S., and van Zijl, P. C. (2002). Fiber tracking: principles and strategies – a technical review. NMR Biomed. 15, 468-480. doi: 10.1002/nbm.781
84. Mountcastle, V. B. (1997). The columnar organization of the neocortex. Brain 120 (Pt 4), 701-722. doi: 10.1093/brain/120.4.701
85. Nieuwenhuys, R. (2013). The myeloarchitectonic studies on the human cerebral cortex of the Vogt-Vogt school, and their significance for the interpretation of functional neuroimaging data. Brain Struct. Funct. 218, 303-352. doi: 10.1007/s00429-012-0460-z
86. Ozarslan, E., Shepherd, T. M., Vemuri, B. C., Blackband, S. J., and Mareci, T. H. (2006). Resolution of complex tissue microarchitecture using the diffusion orientation transform (DOT). Neuroimage 31, 1086-1103. doi: 10.1016/j.neuroimage.2006.01.024
87. Panagiotaki, E., Schneider, T., Siow, B., Hall, M. G., Lythgoe, M. F., and Alexander, D. C. (2012). Compartment models of the diffusion MR signal in brain white matter: a taxonomy and comparison. Neuroimage 59, 2241-2254. doi: 10.1016/j.neuroimage.2011.09.081
88. Parker, G. J., and Alexander, D. C. (2005). Probabilistic anatomical connectivity derived from the microscopic persistent angular structure of cerebral tissue. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 893-902. doi: 10.1098/rstb.2005.1639
89. Parker, G. J., Haroon, H. A., and Wheeler-Kingshott, C. A. (2003). A framework for a streamline-based probabilistic index of connectivity (PICo) using a structural interpretation of MRI diffusion measurements. J. Magn. Reson. Imaging 18, 242-254. doi: 10.1002/jmri.10350
90. Patterson, D. M., Padhani, A. R., and Collins, D. J. (2008). Technology insight: water diffusion MRI-a potential new biomarker of response to cancer therapy. Nat. Clin. Pract. Oncol. 5, 220-233. doi: 10.1038/ncponc1073
91. Perrin, M., Cointepas, Y., Cachia, A., Poupon, C., Thirion, B., Riviere, D., et al. (2008). Connectivity-based parcellation of the cortical mantle using q-ball diffusion imaging. Int. J. Biomed. Imaging 2008, 368406. doi: 10.1155/2008/368406
92. Pestilli, F., Yeatman, J. D., Rokem, A., Kay, K. N., and Wandell, B. A. (2014). Evaluation and statistical inference for human connectomes. Nat. Methods 11, 1058-1063. doi: 10.1038/nmeth.3098
93. Rakic, P. (2008). Confusing cortical columns. Proc. Natl. Acad. Sci. U.S.A. 105, 12099-12100. doi: 10.1073/pnas.0807271105
94. Reisert, M., Kellner, E., and Kiselev, V. G. (2012). About the geometry of asymmetric fiber orientation distributions. IEEE Trans. Med. Imaging 31, 1240-1249. doi: 10.1109/TMI.2012.2187916
95. Reisert, M., and Kiselev, V. G. (2011). Fiber continuity: an anisotropic prior for ODF estimation. IEEE Trans. Med. Imaging 30, 1274-1283. doi: 10.1109/TMI.2011.2112769
96. Reisert, M., Mader, I., Anastasopoulos, C., Weigel, M., Schnell, S., and Kiselev, V. (2011). Global fiber reconstruction becomes practical. Neuroimage 54, 955-962. doi: 10.1016/j.neuroimage.2010.09.016
97. Rubinov, M., and Sporns, O. (2010). Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52, 1059-1069. doi: 10.1016/j.neuroimage.2009.10.003
98. Rushton, W. A. (1951). A theory of the effects of fibre size in medullated nerve. J. Physiol. 115, 101-122. doi: 10.1113/jphysiol.1951.sp004655
99. Sanides, F. (1962). [Architectonics of the human frontal lobe of the brain. With a demonstration of the principles of its formation as a reflection of phylogenetic differentiation of the cerebral cortex]. Monogr. Gesamtgeb. Neurol. Psychiatr. 98, 1-201.
100. Savadjiev, P., Campbell, J. S., Descoteaux, M., Deriche, R., Pike, G. B., and Siddiqi, K. (2008). Labeling of ambiguous subvoxel fibre bundle configurations in high angular resolution diffusion MRI. Neuroimage 41, 58-68. doi: 10.1016/j.neuroimage.2008.01.028
101. Savadjiev, P., Campbell, J. S., Pike, G. B., and Siddiqi, K. (2006). 3D curve inference for diffusion MRI regularization and fibre tractography. Med. Image Anal. 10, 799-813. doi: 10.1016/j.media.2006.06.009
102. Schleicher, A., Amunts, K., Geyer, S., Morosan, P., and Zilles, K. (1999). Observer- independent method for microstructural parcellation of cerebral cortex: a quantitative approach to cytoarchitectonics. Neuroimage 9, 165-177. doi: 10.1006/nimg.1998.0385
103. Seehaus, A. K., Roebroeck, A., Chiry, O., Kim, D. S., Ronen, I., Bratzke, H., et al. (2013). Histological validation of DW-MRI tractography in human postmortem tissue. Cereb. Cortex 23, 442-450. doi: 10.1093/cercor/bhs036
104. Sherbondy, A. J., Dougherty, R. F., Ananthanarayanan, R., Modha, D. S., and Wandell, B. A. (2009). Think global, act local; projectome estimation with BlueMatter. Med. Image Comput. Comput. Assist. Interv. 12, 861-868. doi: 10.1007/978-3-642-04268-3_106
105. Sherbondy, A. J., Dougherty, R. F., Ben-Shachar, M., Napel, S., and Wandell, B. A. (2008). ConTrack: finding the most likely pathways between brain regions using diffusion tractography. J. Vis. 8, 15.1-16. doi: 10.1167/8.9.15
106. Sotiropoulos, S. N., Bai, L., Morgan, P. S., Constantinescu, C. S., and Tench, C. R. (2010). Brain tractography using Q-ball imaging and graph theory: improved connectivities through fibre crossings via a model-based approach. Neuroimage 49, 2444-2456. doi: 10.1016/j.neuroimage.2009.10.001
107. Sotiropoulos, S. N., Jbabdi, S., Xu, J., Andersson, J. L., Moeller, S., Auerbach, E. J., et al. (2013). Advances in diffusion MRI acquisition and processing in the Human Connectome Project. Neuroimage 80, 125-143. doi: 10.1016/j.neuroimage.2013.05.057
108. Sporns, O., Tononi, G., and Kotter, R. (2005). The human connectome: a structural description of the human brain. PLoS Comput. Biol. 1:e42. doi: 10.1371/journal.pcbi.0010042
109. Stanisz, G. J., Szafer, A., Wright, G. A., and Henkelman, R. M. (1997). An analytical model of restricted diffusion in bovine optic nerve. Magn. Reson. Med. 37, 103-111. doi: 10.1002/mrm.1910370115
110. Stejskal, E. O., and Tanner, J. E. (1965). Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient. J. Chem. Phys. 42, 288-292. doi: 10.1063/1.1695690
111. Stephan, K. E., Zilles, K., and Kotter, R. (2000). Coordinate-independent mapping of structural and functional data by objective relational transformation (ORT). Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 37-54. doi: 10.1098/rstb.2000.0548
112. Stikov, N., Campbell, J., Boudreau, M., Narayanan, S., Stroh, T., Nuara, S., et al. (2014). "In vivo histology of the myelin g-ratio," in Proceedings of the 2014 Organization for Human Brain Mapping Annual Meeting, Hamburg, 2249.
113. Talairach, J., and Tournoux, P. (1988). Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging. Stuttgart: Georg Thieme.
114. Thomas, C., Ye, F. Q., Irfanoglu, M. O., Modi, P., Saleem, K. S., Leopold, D. A., et al. (2014). Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc. Natl. Acad. Sci. U.S.A. 111, 16574-16579. doi: 10.1073/pnas.1405672111
115. Tomassini, V., Jbabdi, S., Klein, J. C., Behrens, T. E., Pozzilli, C., Matthews, P. M., et al. (2007). Diffusion-weighted imaging tractography-based parcellation of the human lateral premotor cortex identifies dorsal and ventral subregions with anatomical and functional specializations. J. Neurosci. 27, 10259-10269. doi: 10.1523/JNEUROSCI.2144-07.2007
116. Tournier, J. D., Calamante, F., and Connelly, A. (2007). Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage 35, 1459-1472. doi: 10.1016/j.neuroimage.2007.02.016
117. Tournier, J. D., Calamante, F., and Connelly, A. (2010). "Improved probabilistic streamlines tractography by 2nd order integration over fibre orientation distributions," in Proceedings of the Joint Annual Meeting ISMRM-ESMRMB 2010, Stockholm.
118. Tournier, J. D., Calamante, F., Gadian, D. G., and Connelly, A. (2004). Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution. Neuroimage 23, 1176-1185. doi: 10.1016/j.neuroimage.2004.07.037
119. Tuch, D. S. (2004). Q-ball imaging. Magn. Reson. Med. 52, 1358-1372. doi: 10.1002/mrm.20279
120. Tuch, D. S., Reese, T. G., Wiegell, M. R., Makris, N., Belliveau, J. W., and Wedeen, V. J. (2002). High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity. Magn. Reson. Med. 48, 577-582. doi: 10.1002/mrm.10268
121. van den Heuvel, M. P., Mandl, R. C., Stam, C. J., Kahn, R. S., and Hulshoff Pol, H. E. (2010). Aberrant frontal and temporal complex network structure in schizophrenia: a graph theoretical analysis. J. Neurosci. 30, 15915-15926. doi: 10.1523/JNEUROSCI.2874-10.2010
122. van den Heuvel, M. P., and Sporns, O. (2011). Rich-club organization of the human connectome. J. Neurosci. 31, 15775-15786. doi: 10.1523/JNEUROSCI.3539-11.2011
123. Van Essen, D. C., and Ugurbil, K. (2012). The future of the human connectome. Neuroimage 62, 1299-1310. doi: 10.1016/j.neuroimage.2012.01.032
124. Vogt, O. (1910). Die myeloarchitektonische felderung des menschlichen stirnhirns. J. Psychol. Neurol. 15, 221-232.
125. von Economo, C., and Koskinas, G. N. (1925). Die Cytoarchitektonik der Hirnrinde des Erwachsenen Menschen. Vienna: Julius Springer.
126. Wakana, S., Jiang, H., Nagae-Poetscher, L. M., Van Zijl, P. C., and Mori, S. (2004). Fiber tract-based atlas of human white matter anatomy. Radiology 230, 77-87. doi: 10.1148/radiol.2301021640
127. Wang, H., Black, A. J., Zhu, J., Stigen, T. W., Al-Qaisi, M. K., Netoff, T. I., et al. (2011). Reconstructing micrometer-scale fiber pathways in the brain: multi-contrast optical coherence tomography based tractography. Neuroimage 58, 984-992. doi: 10.1016/j.neuroimage.2011.07.005
128. Wedeen, V. J., Hagmann, P., Tseng, W. Y., Reese, T. G., and Weisskoff, R. M. (2005). Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn. Reson. Med. 54, 1377-1386. doi: 10.1002/mrm.20642
129. Yeh, F. C., Wedeen, V. J., and Tseng, W. Y. (2010). Generalized q-sampling imaging. IEEE Trans. Med. Imaging 29, 1626-1635. doi: 10.1109/TMI.2010.2045126
130. Zalesky, A., and Fornito, A. (2009). A DTI-derived measure of cortico- cortical connectivity. IEEE Trans. Med. Imaging 28, 1023-1036. doi: 10.1109/TMI.2008.2012113
131. Zatorre, R. J., Fields, R. D., and Johansen-Berg, H. (2012). Plasticity in gray and white: neuroimaging changes in brain structure during learning. Nat. Neurosci. 15, 528-536. doi: 10.1038/nn.3045
132. Zhang, H., Schneider, T., Wheeler-Kingshott, C. A., and Alexander, D. C. (2012). NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage 61, 1000-1016. doi: 10.1016/j.neuroimage.2012.03.072
133. Zikopoulos, B., and Barbas, H. (2011). "Comparable organization of frontal white matter in human and non-human primates," in Proceedings of the 2011 Society for Neuroscience Annual Meeting, Washington, DC: Society for Neuroscience.
134. Zilles, K., and Amunts, K. (2009). Receptor mapping: architecture of the human cerebral cortex. Curr. Opin. Neurol. 22, 331-339. doi: 10.1097/WCO.0b013e32832d95db
135. Zilles, K., and Amunts, K. (2010). TIMELINE centenary of Brodmann’s map - conception and fate. Nat. Rev. Neurosci. 11, 139-145. doi: 10.1038/nrn2776