Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 46, 2014, Pages 16574-16579

  Thomas, Cibu ^a,b   Ye, Frank Q ^c,d   Irfanoglu, M Okan ^a,b   Modi, Pooja ^a   Saleem, Kadharbatcha S ^c   Leopold, David A ^c,d   Pierpaoli, Carlo ^a,b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^d Section on Cognitive Neurophysiology and Imaging   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; ADULT; ALGORITHM; ANIMAL EXPERIMENT; ARTICLE; BRAIN TISSUE; CONNECTOME; DIFFUSION WEIGHTED IMAGING; EX VIVO STUDY; IMAGE ANALYSIS; IMAGE QUALITY; MALE; NEUROANATOMY; NEUROIMAGING; NONHUMAN; RECEIVER OPERATING CHARACTERISTIC; RHESUS MONKEY; SENSITIVITY AND SPECIFICITY; TRACTOGRAPHY; WHITE MATTER; ANATOMY AND HISTOLOGY; ANIMAL; BIOLOGICAL MODEL; BODY WATER; COMPARATIVE STUDY; DIFFUSION; DIFFUSION TENSOR IMAGING; METHODOLOGY; MOTOR CORTEX; NERVE FIBER; NERVE FIBER TRANSPORT; OCCIPITAL LOBE; PROCEDURES; STATISTICS AND NUMERICAL DATA; ULTRASTRUCTURE;

CONTRAST MEDIUM; GADOLINIUM PENTETATE; LEUCINE; PROLINE; TRITIUM;

ALGORITHMS; ANIMALS; AXONAL TRANSPORT; AXONS; BODY WATER; CONNECTOME; CONTRAST MEDIA; DIFFUSION; DIFFUSION MAGNETIC RESONANCE IMAGING; DIFFUSION TENSOR IMAGING; GADOLINIUM DTPA; LEUCINE; MACACA MULATTA; MALE; MODELS, NEUROLOGICAL; MOTOR CORTEX; OCCIPITAL LOBE; PROLINE; RESEARCH DESIGN; ROC CURVE; SENSITIVITY AND SPECIFICITY; TRITIUM; WHITE MATTER;

EID: 84915758306     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1405672111     Document Type: Article

References (63)

1. Schmahmann JD, Pandya DN (2007) Cerebral white matter-historical evolution of facts and notions concerning the organization of the fiber pathways of the brain. J Hist Neurosci 16(3):237-267.
2. Le Bihan D, et al. (1986) MR imaging of intravoxel incoherent motions: Application to diffusion and perfusion in neurologic disorders. Radiology 161(2):401-407.
3. Merboldt K-D, Hanicke W, Frahm J (1985) Self-diffusion NMR imaging using stimulated echoes. J Magn Reson (1969) 64(3):479-486.
4. Taylor DG, Bushell MC (1985) The spatial mapping of translational diffusion coefficients by the NMR imaging technique. Phys Med Biol 30(4):345-349.
5. Basser PJ, Mattiello J, Le Bihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103(3):247-254.
6. Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G (1996) Diffusion tensor MR imaging of the human brain. Radiology 201(3):637-648.
7. Sundgren PC, et al. (2004) Diffusion tensor imaging of the brain: Review of clinical applications. Neuroradiology 46(5):339-350.
8. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44(4):625-632.
9. Conturo TE, et al. (1999) Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci USA 96(18):10422-10427.
10. Jones DK, Simmons A, Williams SC, Horsfield MA (1999) Non-invasive assessment of axonal fiber connectivity in the human brain via diffusion tensor MRI. Magn Reson Med 42(1):37-41.
11. 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(2):265-269.
12. Poupon C, et al. (2000) Regularization of diffusion-based direction maps for the tracking of brain white matter fascicles. Neuroimage 12(2):184-195.
13. Jbabdi S, Johansen-Berg H (2011) Tractography: Where do we go from here? Brain Connect 1(3):169-183.
14. Jones DK (2008) Studying connections in the living human brain with diffusion MRI. Cortex 44(8):936-952.
15. Catani M, de Schotten MT (2012) Atlas of Human Brain Connections (Oxford Univ Press, New York).
16. Johansen-Berg H, Behrens TE (2006) Just pretty pictures? What diffusion tractography can add in clinical neuroscience. Curr Opin Neurol 19(4):379-385.
17. Schmahmann JD, Pandya D (2009) Fiber Pathways of the Brain (Oxford Univ Press, New York).
18. Pierpaoli C, et al. (2001) Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage 13(6 Pt 1):1174-1185.
19. Farquharson S, et al. (2013) White matter fiber tractography: Why we need to move beyond DTI. J Neurosurg 118(6):1367-1377.
20. Cook P, et al. (2006) Camino: Open-source diffusion-MRI reconstruction and processing. 14th Scientific Meeting of the International Society for Magnetic Resonance in Medicine, p 2759.
21. Dell'Acqua F, et al. (2007) A model-based deconvolution approach to solve fiber crossing in diffusion-weighted MR imaging. Biomedical Engineering. IEEE Transactions on 54(3):462-472.
22. Tournier JD, Calamante F, Connelly A (2007) Robust determination of the fibre orientation distribution in diffusion MRI: Non-negativity constrained super-resolved spherical deconvolution. Neuroimage 35(4):1459-1472.
23. Tuch DS, et al. (2002) High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity. Magn Reson Med 48(4):577-582.
24. Wedeen VJ, Hagmann P, Tseng W-YI, Reese TG, Weisskoff RM (2005) Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med 54(6):1377-1386.
25. Pierpaoli C (2011) Artifacts in Diffusion MRI. Diffusion MRI: Theory, Methods and Application, ed Jones D (Oxford Publications, New York), pp 303-318.
26. Irfanoʇlu MO, Walker L, Sarlls J, Marenco S, Pierpaoli C (2012) Effects of image distortions originating from susceptibility variations and concomitant fields on diffusion MRI tractography results. Neuroimage 61(1):275-288.
27. Uʇurbil K, et al.; WU-Minn HCP Consortium (2013) Pushing spatial and temporal resolution for functional and diffusion MRI in the Human Connectome Project. Neuroimage 80:80-104.
28. Setsompop K, et al. (2013) Pushing the limits of in vivo diffusion MRI for the Human Connectome Project. Neuroimage 80:220-233.
29. Van Essen DC, et al.; WU-Minn HCP Consortium (2012) The Human Connectome Project: A data acquisition perspective. Neuroimage 62(4):2222-2231.
30. Seehaus AK, et al. (2012) Histological validation of DW-MRI tractography in human postmortem tissue. Cereb Cortex 23(2):442-450.
31. Iturria-Medina Y, et al. (2011) Brain hemispheric structural efficiency and interconnectivity rightward asymmetry in human and nonhuman primates. Cereb Cortex 21(1):56-67.
32. Youden WJ (1950) Index for rating diagnostic tests. Cancer 3(1):32-35.
33. Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? Neuroimage 34(1):144-155.
34. Jbabdi S, Lehman JF, Haber SN, Behrens TE (2013) Human and monkey ventral prefrontal fibers use the same organizational principles to reach their targets: Tracing versus tractography. J Neurosci 33(7):3190-3201.
35. Sotiropoulos SN, et al.; WU-Minn HCP Consortium (2013) Advances in diffusion MRI acquisition and processing in the Human Connectome Project. Neuroimage 80: 125-143.
36. Gschwind M, Pourtois G, Schwartz S, Van De Ville D, Vuilleumier P (2012) Whitematter connectivity between face-responsive regions in the human brain. Cereb Cortex 22(7):1564-1576.
37. Behrens TE, et al. (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6(7):750-757.
38. Schmahmann JD, et al. (2007) Association fibre pathways of the brain: Parallel observations from diffusion spectrum imaging and autoradiography. Brain 130(Pt 3): 630-653.
39. Dyrby TB, et al. (2007) Validation of in vitro probabilistic tractography. Neuroimage 37(4):1267-1277.
40. Dauguet J, et al. (2007) Comparison of fiber tracts derived from in-vivo DTI tractography with 3D histological neural tract tracer reconstruction on a macaque brain. Neuroimage 37(2):530-538.
41. Roebroeck A, et al. (2008) High-resolution diffusion tensor imaging and tractography of the human optic chiasm at 9.4 T. Neuroimage 39(1):157-168.
42. Mangin J-F, et al. (2013) Toward global tractography. Neuroimage 80:290-296.
43. Bürgel U, et al. (2006) White matter fiber tracts of the human brain: Threedimensional mapping at microscopic resolution, topography and intersubject variability. Neuroimage 29(4):1092-1105.
44. Lawes IN, et al. (2008) Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. Neuroimage 39(1):62-79.
45. Tsao DY, Moeller S, Freiwald WA (2008) Comparing face patch systems in macaques and humans. Proc Natl Acad Sci USA 105(49):19514-19519.
46. Saleem KS, Price JL, Hashikawa T (2007) Cytoarchitectonic and chemoarchitectonic subdivisions of the perirhinal and parahippocampal cortices in macaque monkeys. J Comp Neurol 500(6):973-1006.
47. Margulies DS, et al. (2009) Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci USA 106(47):20069-20074.
48. Saleem KS, Miller B, Price JL (2014) Subdivisions and connectional networks of the lateral prefrontal cortex in the macaque monkey. J Comp Neurol 522(7):1641-1690.
49. Leuze CW, et al. (2014) Layer-specific intracortical connectivity revealed with diffusion MRI. Cereb Cortex 24(2):328-339.
50. McNab JA, et al. (2013) Surface based analysis of diffusion orientation for identifying architectonic domains in the in vivo human cortex. Neuroimage 69:87-100.
51. Ungerleider LG, Galkin TW, Desimone R, Gattass R (2008) Cortical connections of area V4 in the macaque. Cereb Cortex 18(3):477-499.
52. Stepniewska I, Preuss TM, Kaas JH (1994) Thalamic connections of the primary motor cortex (M1) of owl monkeys. J Comp Neurol 349(4):558-582.
53. Burman KJ, Bakola S, Richardson KE, Reser DH, Rosa MG (2014) Patterns of cortical input to the primary motor area in the marmoset monkey. J Comp Neurol 522(4): 811-843.
54. Webster MJ, Bachevalier J, Ungerleider LG (1994) Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cereb Cortex 4(5):470-483.
55. Dyrby TB, et al. (2011) An ex vivo imaging pipeline for producing high-quality and high-resolution diffusion-weighted imaging datasets. Hum Brain Mapp 32(4): 544-563.
56. Tournier J, Calamante F, Connelly A (2012) MRtrix: Diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol 22(1):53-66.
57. Budde MD, Frank JA (2010) Neurite beading is sufficient to decrease the apparent diffusion coefficient after ischemic stroke. Proc Natl Acad Sci USA 107(32): 14472-14477.
58. Callaghan PT (1993) Principles of Nuclear Magnetic Resonance Microscopy (Oxford Univ Press, New York).
59. Stejskal E (1965) Use of spin echoes in a pulsed magnetic-field gradient to study anisotropic, restricted diffusion and flow. J Chem Phys 43:3597.
60. Özarslan E, et al. (2013) Mean apparent propagator (MAP) MRI: A novel diffusion imaging method for mapping tissue microstructure. Neuroimage 78:16-32.
61. Yang QX, Posse S, Le Bihan D, Smith MB (1996) Double-sampled echo-planar imaging at 3 tesla. J Magn Reson B 113(2):145-150.
62. Committee on Care and Use of Laboratory Animals (1996) Guide for the Care and Use of Laboratory Animals (National Academies Press, Washington, DC).
63. Pierpaoli C, et al. (2010) TORTOISE: An integrated software package for processing of diffusion MRI data. 18th Scientific Meeting of the International Society for Magnetic Resonance in Medicine, p. 1597.