Connectivity-based fixel enhancement: Whole-brain statistical analysis of diffusion MRI measures in the presence of crossing fibres

NeuroImage

Volumn 117, Issue , 2015, Pages 40-55

  Raffelt, David A ^a   Smith, Robert E ^a   Ridgway, Gerard R ^b,c   Tournier, J Donald ^d   Vaughan, David N ^a,e,f   Rose, Stephen ^g   Henderson, Robert ^g   Connelly, Alan ^a,e,f  

^a FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f UNIVERSITY OF MELBOURNE   (Australia)

^g ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

Author keywords

Analysis; Connectivity; Diffusion; Fixel; MRI; Statistics

Indexed keywords

ARTICLE; BRAIN RADIOGRAPHY; BRAIN REGION; CLINICAL ARTICLE; CONNECTOME; CONTROLLED STUDY; DIFFUSION WEIGHTED IMAGING; FRACTIONAL ANISOTROPY; GRAY MATTER; HUMAN; MOTOR NEURON DISEASE; NEUROANATOMY; NEUROIMAGING; PRIORITY JOURNAL; PROBABILITY; SENSITIVITY AND SPECIFICITY; SIGNAL NOISE RATIO; STATISTICAL ANALYSIS; TRACTOGRAPHY; WHITE MATTER; ANATOMY AND HISTOLOGY; BRAIN; IMAGE ENHANCEMENT; PATHOLOGY; PROCEDURES; THREE DIMENSIONAL IMAGING;

BRAIN; DATA INTERPRETATION, STATISTICAL; DIFFUSION MAGNETIC RESONANCE IMAGING; HUMANS; IMAGE ENHANCEMENT; IMAGING, THREE-DIMENSIONAL; MOTOR NEURON DISEASE; WHITE MATTER;

EID: 84930652853     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.05.039     Document Type: Article

References (63)

1. Ashburner J. Computational Neuroanatomy 2000, University College London, London, United Kingdom.
2. Ashburner J., Friston K.J. Voxel-based morphometry-the methods. NeuroImage 2000, 11:805-821. 10.1006/nimg.2000.0582.
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. 10.1016/j.neuroimage.2005.03.042.
4. Bach M., Laun F.B., Leemans A., Tax C.M.W., Biessels G.J., Stieltjes B., Maier-Hein K.H. Methodological considerations on tract-based spatial statistics (TBSS). NeuroImage 2014, 100:358-369. 10.1016/j.neuroimage.2014.06.021.
5. 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.
6. 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. 10.1016/j.neuroimage.2006.09.018.
7. Brooks B.R., Miller R.G., Swash M., Munsat T.L., World Federation of Neurology Research Group on Motor Neuron Diseases El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 2000, 1:293-299.
8. Chakraborty D.P., Winter L.H. Free-response methodology: alternate analysis and a new observer-performance experiment. Radiology 1990, 174:873-881. 10.1148/radiology.174.3.2305073.
9. Core R Team R: A Language and Environment for Statistical Computing. Vienna, Austria 2013.
10. Daducci A., Dal Palu A., Alia L., Thiran J.-P. COMMIT: convex optimization modeling for micro-structure informed tractography. IEEE Trans. Med. Imaging 2014, 10.1109/TMI.2014.2352414.
11. De Groot M., Vernooij M.W., Klein S., Ikram M.A., Vos F.M., Smith S.M., Niessen W.J., Andersson J.L.R. Improving alignment in tract-based spatial statistics: evaluation and optimization of image registration. NeuroImage 2013, 76:400-411. 10.1016/j.neuroimage.2013.03.015.
12. Dell'Acqua F., Simmons A., Williams S.C.R., Catani M. Can spherical deconvolution provide more information than fiber orientations? Hindrance modulated orientational anisotropy, a true-tract specific index to characterize white matter diffusion. Hum. Brain Mapp. 2013, 34:2464-2483. 10.1002/hbm.22080.
13. Edden R.A., Jones D.K. Spatial and orientational heterogeneity in the statistical sensitivity of skeleton-based analyses of diffusion tensor MR imaging data. J. Neurosci. Methods 2011, 201:213-219. 10.1016/j.jneumeth.2011.07.025.
14. Farquharson S., Raffelt D., Sadeghian F., Tournier J.-D., Mandelstam S., Schneider-Kolsky M., Berkovic, Scheffer I.E., Jackson G.D., Connelly A. Apparent Fibre Density (AFD) Analysis Reveals Decreases in Axonal Density in the White Matter Pathways of Patients with Grey Matter Heterotopia. Proceedings of the International Society for Magnetic Resonance in Medicine. Milan, Italy 2014.
15. Foerster B.R., Dwamena B.A., Petrou M., Carlos R.C., Callaghan B.C., Pomper M.G. Diagnostic accuracy using diffusion tensor imaging in the diagnosis of ALS: a meta-analysis. Academic Radiology 2012, 10.1016/j.acra.2012.04.012.
16. Foerster B.R., Welsh R.C., Feldman E.L. 25years of neuroimaging in amyotrophic lateral sclerosis. Nat. Rev. Neurol. 2013, 10.1038/nrneurol.2013.153.
17. Freedman D., Lane D. A nonstochastic interpretation of reported significance levels. J Bus Econ. Stat. 1983, 1:292-298. 10.1080/07350015.1983.10509354.
18. Friston K.J., Frith C.D., Liddle P.F., Frackowiak R.S.J. Comparing functional (PET) images: the assessment of significant change. J. Cereb. Blood Flow Metab. 1991, 11:690-699. 10.1038/jcbfm.1991.122.
19. Friston K.J., Worsley K.J., Frackowiak R.S.J., Mazziotta J.C., Evans A.C. Assessing the significance of focal activations using their spatial extent. Hum. Brain Mapp. 1994, 1:210-220. 10.1002/hbm.460010306.
20. Friston K.J., Holmes A.P., Poline J.B., Grasby P.J., Williams S.C., Frackowiak R.S., Turner R. Analysis of fMRI time-series revisited. NeuroImage 1995, 2:45-53. 10.1006/nimg.1995.1007.
21. Friston K.J., Holmes A., Poline J.B., Price C.J., Frith C.D. Detecting activations in PET and fMRI: levels of inference and power. NeuroImage 1996, 4:223-235. 10.1006/nimg.1996.0074.
22. Gee J.C. On matching brain volumes. Pattern Recogn. 1999, 32:99-111. 10.1016/S0031-3203(98)00093-4.
23. Hayasaka S., Phan K.L., Liberzon I., Worsley K.J., Nichols T.E. Nonstationary cluster-size inference with random field and permutation methods. NeuroImage 2004, 22:676-687. 10.1016/j.neuroimage.2004.01.041.
24. Holmes A.P., Blair R.C., Watson J.D., Ford I. Nonparametric analysis of statistic images from functional mapping experiments. J. Cereb. Blood Flow Metab. 1996, 16:7-22. 10.1097/00004647-199601000-00002.
25. Hornberger M., Wong S., Tan R., Irish M., Piguet O., Kril J., Hodges J.R., Halliday G. In vivo and post-mortem memory circuit integrity in frontotemporal dementia and Alzheimer's disease. Brain 2012, 135:3015-3025. 10.1093/brain/aws239.
26. Hughes J.T. Pathology of amyotrophic lateral sclerosis. Adv. Neurol. 1982, 36:61-74.
27. Jbabdi S., Behrens T.E., Smith S.M. Crossing fibres in tract-based spatial statistics. NeuroImage 2010, 49:249-256. 10.1016/j.neuroimage.2009.08.039.
28. Jenkinson M. Fast, automated, N-dimensional phase-unwrapping algorithm. Magn. Reson. Med. 2003, 49:193-197. 10.1002/mrm.10354.
29. Jeurissen B., Leemans A., Tournier J.-D., Jones D.K., Sijbers J. Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Hum. Brain Mapp. 2012, 10.1002/hbm.22099.
30. Jones D.K., Horsfield M.A., Simmons A. Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magn. Reson. Med. 1999, 42:515-525.
31. Maddah M., Miller J.V., Sullivan E.V., Pfefferbaum A., Rohlfing T. Sheet-like white matter fiber tracts: representation, clustering, and quantitative analysis. Med. Image Comput. Comput. Assist. Interv. 2011, 14:191-199.
32. Nichols T., Hayasaka S. Controlling the familywise error rate in functional neuroimaging: a comparative review. Stat. Methods Med. Res. 2003, 12:419-446.
33. Nichols T.E., Holmes A.P. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 2002, 15:1-25.
34. Poline J.B., Mazoyer B.M. Analysis of individual positron emission tomography activation maps by detection of high signal-to-noise-ratio pixel clusters. J. Cereb. Blood Flow Metab. 1993, 13:425-437. 10.1038/jcbfm.1993.57.
35. Raffelt D., Tournier J.-D., Fripp J., Crozier S., Connelly A., Salvado O. Symmetric diffeomorphic registration of fibre orientation distributions. NeuroImage 2011, 56:1171-1180.
36. Raffelt D., Tournier J.-D., Crozier S., Connelly A., Salvado O. Reorientation of fiber orientation distributions using apodized point spread functions. Magn. Reson. Med. 2012, 67:844-855.
37. Raffelt D., Tournier J.-D., Rose S., Ridgway G.R., Henderson R., Crozier S., Salvado O., Connelly A. Apparent fibre density: a novel measure for the analysis of diffusion-weighted magnetic resonance images. NeuroImage 2012, 59:3976-3994.
38. Raffelt D., Tournier J.-D., Salvado O., Connelly A. Mask-based motion and eddy-current correction of high b-value diffusion-weighted images. Proceedings of the International Society for Magnetic Resonance in Medicine. Melbourne, Australia, USA 2012.
39. Raffelt D., Smith R.E., Tournier J.-D., Ridgway G.R., Villemagne V.L., Rowe C.C., Salvado O., Connelly A. Tractographic threshold-free cluster enhancement: whole-brain statistical analysis of diffusion MRI measures in the presence of crossing fibres. Proceedings of the International Society for Magnetic Resonance in Medicine. Salt Lake City, Utah, USA 2013.
40. Raffelt D., Cheong J.L., Sadeghian F., Thompson D.K., Anderson P.J., Doyle L.W., Connelly A. Apparent fibre density abnormalities in adolescents born extremely preterm: moving beyond the diffusion tensor. Proceedings of the International Society for Magnetic Resonance in Medicine. Milan, Italy 2014.
41. Raffelt D., Parker D., McMahon J.M., Scheffer I.E., Connelly A. Decreased apparent fibre density in Dravet syndrome. Proceedings of the International Society for Magnetic Resonance in Medicine. Milan, Italy 2014.
42. Raffelt D., Smith R.E., Tournier J.-D., Vaughan D., Jackson G.D., Connelly A. Fixel-based morphometry: whole-brain white matter morphometry in the presence of crossing fibres. Proceedings of the International Society for Magnetic Resonance in Medicine. Milan, Italy 2014.
43. Raffelt D., Sadeghian F., Connor H., Connelly A. Decreased apparent fibre density in the optic pathways correlates with glaucoma disease severity. Proceedings of the International Society for Magnetic Resonance in Medicine. Toronto, Canada 2015.
44. Ridgway G.R., Omar R., Ourselin S., Hill D.L.G., Warren J.D., Fox N.C. Issues with threshold masking in voxel-based morphometry of atrophied brains. NeuroImage 2009, 44:99-111. 10.1016/j.neuroimage.2008.08.045.
45. Rohlfing T., Zahr N.M., Sullivan E.V., Pfefferbaum A. The SRI24 multichannel atlas of normal adult human brain structure. Hum. Brain Mapp. 2010, 31:798-819. 10.1002/hbm.20906.
46. Salimi-Khorshidi G., Smith S.M., Nichols T.E. Adjusting the effect of nonstationarity in cluster-based and TFCE inference. NeuroImage 2011, 54:2006-2019. 10.1016/j.neuroimage.2010.09.088.
47. Scherrer B., Warfield S.K. Parametric representation of multiple white matter fascicles from cube and sphere diffusion MRI. PLoS One 2012, 7(11):e48232. 10.1371/journal.pone.0048232.
48. Schwarz C.G., Reid R.I., Gunter J.L., Senjem M.L., Przybelski S.A., Zuk S.M., Whitwell J.L., Vemuri P., Josephs K.A., Kantarci K., Thompson P.M., Petersen R.C., Jack C.R., for the Alzheimer's Disease Neuroimaging Initiative Improved DTI registration allows voxel-based analysis that outperforms Tract-Based Spatial Statistics. NeuroImage 2014, 10.1016/j.neuroimage.2014.03.026.
49. Smith S.M., Nichols T.E. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 2009, 44:83-98. 10.1016/j.neuroimage.2008.03.061.
50. Smith S.M., Jenkinson M., Johansen-Berg H., Rueckert D., Nichols T.E., Mackay C.E., Watkins K.E., Ciccarelli O., Cader M.Z., Matthews P.M., Behrens T.E.J. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 2006, 31:1487-1505. 10.1016/j.neuroimage.2006.02.024.
51. Smith R.E., Tournier J.-D., Calamante F., Connelly A. SIFT: spherical-deconvolution informed filtering of tractograms. NeuroImage 2013, 67:298-312. 10.1016/j.neuroimage.2012.11.049.
52. Tournier J.-D., Calamante F., Connelly A. Improved probabilistic streamlines tractography by 2nd order integration over fibre orientation distributions. Proceedings of the International Society for Magnetic Resonance in Medicine. Stockholm, Sweden 2010.
53. Tournier J.-D., Calamante F., Connelly A. MRtrix: diffusion tractography in crossing fiber regions. Int. J. Imaging Syst. Technol. 2012, 22:53-66. 10.1002/ima.22005.
54. Tournier J.-D., Calamante F., Connelly A. A robust spherical deconvolution method for the analysis of low SNR or low angular resolution diffusion data. Proceedings of the International Society for Magnetic Resonance in Medicine. Salt Lake City, Utah, USA 2013.
55. Tuch D.S. Q-ball imaging. Magn. Reson. Med. 2004, 52:1358-1372. 10.1002/mrm.20279.
56. Tustison N.J., Avants B.B., Cook P.A., Zheng Y., Egan A., Yushkevich P.A., Gee J.C. N4ITK: improved N3 bias correction. IEEE Trans. Med. Imaging 2010, 29:1310-1320. 10.1109/TMI.2010.2046908.
57. Van Hecke W., Leemans A., Sage C.A., Emsell L., Veraart J., Sijbers J., Sunaert S., Parizel P.M. The effect of template selection on diffusion tensor voxel-based analysis results. NeuroImage 2011, 55:566-573. 10.1016/j.neuroimage.2010.12.005.
58. Wedeen V.J., Hagmann P., Tseng W.-Y.I., Reese T.G., Weisskoff R.M. Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn. Reson. Med. 2005, 54:1377-1386. 10.1002/mrm.20642.
59. Winkler A.M., Ridgway G.R., Webster M.A., Smith S.M., Nichols T.E. Permutation inference for the general linear model. NeuroImage 2014, 92:381-397. 10.1016/j.neuroimage.2014.01.060.
60. Worsley K.J., Evans A.C., Marrett S., Neelin P. A three-dimensional statistical analysis for CBF activation studies in human brain. J. Cereb. Blood Flow Metab. 1992, 12:900-918. 10.1038/jcbfm.1992.127.
61. Worsley K.J., Andermann M., Koulis T., MacDonald D., Evans A.C. Detecting changes in nonisotropic images. Hum. Brain Mapp. 1999, 8:98-101.
62. Yushkevich P.A., Zhang H., Simon T.J., Gee J.C. Structure-specific statistical mapping of white matter tracts. NeuroImage 2008, 41:448-461. 10.1016/j.neuroimage.2008.01.013.
63. Zhang H., Awatea S.P., Das S.R., Woo J.H., Melhem E.R., Gee J.C., Yushkevich P.A. A tract-specific framework for white matter morphometry combining macroscopic and microscopic tract features. Med. Image Anal. 2010, 14:666-673. 10.1016/j.media.2010.05.002.