Quantitative DTI Measures

  • Kathleen M. Curran
  • Louise Emsell
  • Alexander Leemans

Abstract

Diffusion tensor imaging (DTI) has revolutionized the visualization of white matter in vivo. However, it is far more than a qualitative tool and can also be used to generate quantitative measures related to diffusion magnitude and its degree of anisotropy, which indirectly reflect microstructural organisation. Although highly sensitive to microstructural change, DTI measures lack specificity and are influenced by a wide range of biological and methodological factors. This makes the interpretation of DTI metric changes extremely challenging.

This chapter introduces the most common DTI measures and how they relate to tissue microstructure. Important confounds are addressed, including how DTI metrics are influenced by biological factors such as ageing and pathology, and by methodological factors such as data acquisition, modeling, and analysis.

Keywords

Diffusion parameters Visualization Axial and radial diffusivity Relationship to neurobiology 

Notes

Acknowledgements

The authors would like to thank Dr. Niall Colgan, University College London for producing and analysing the synthetic data using the Camino: Open-source diffusion-MRI reconstruction and processing tool [89] and Dr. Karla Miller and FMRIB Centre, University of Oxford for supplying the 1.5 and 7 T data.

References

  1. 1.
    Sotak CH. The role of diffusion tensor imaging in the evaluation of ischemic brain injury - a review. NMR Biomed. 2002;15(7-8):561–9 [Review].CrossRefPubMedGoogle Scholar
  2. 2.
    Norris DG, Niendorf T, Leibfritz D. Health and infarcted brain tissues studied at short diffusion times: the origins of apparent restriction and the reduction in apparent diffusion coefficient. NMR Biomed. 1994;7(7):304–10.CrossRefPubMedGoogle Scholar
  3. 3.
    Concha L. A macroscopic view of microstructure: using diffusion-weighted images to infer damage, repair, and plasticity of white matter. Neuroscience. 2014;276:14–28.CrossRefPubMedGoogle Scholar
  4. 4.
    Basser PJ, Mattiello J, LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B. 1994;103(3):247–54.CrossRefPubMedGoogle Scholar
  5. 5.
    Beaulieu C, Allen PS. Determinants of anisotropic water diffusion in nerves. Magn Reson Med. 1994;31(4):394–400 [Research Support, Non-U.S. Gov’t].CrossRefPubMedGoogle Scholar
  6. 6.
    Basser PJ, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B. 1996;111(3):209–19.CrossRefPubMedGoogle Scholar
  7. 7.
    Moseley ME, Cohen Y, Kucharczyk J, Mintorovitch J, Asgari HS, Wendland MF, et al. Diffusion-weighted MR imaging of anisotropic water diffusion in cat central nervous system. Radiology. 1990;176(2):439–45 [Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, Non-P.H.S. Research Support, U.S. Gov’t, P.H.S.].CrossRefPubMedGoogle Scholar
  8. 8.
    van Gelderen P, de Vleeschouwer MHM, DesPres D, Pekar J, van Zijl P, Moonen CTW. Water diffusion and acute stroke. Magn Reson Med. 1994;31(2):154–63.CrossRefPubMedGoogle Scholar
  9. 9.
    Basser PJ. New histological and physiological stains derived from diffusion-tensor MR images. Ann N Y Acad Sci. 1997;820:123–38.CrossRefPubMedGoogle Scholar
  10. 10.
    Le Bihan D. Diffusion, perfusion and functional magnetic resonance imaging. J Mal Vasc. 1995;20(3):203–14.PubMedGoogle Scholar
  11. 11.
    Westin CF, Maier SE, Mamata H, Nabavi A, Jolesz FA, Kikinis R. Processing and visualization for diffusion tensor MRI. Med Image Anal. 2002;6(2):93–108.CrossRefPubMedGoogle Scholar
  12. 12.
    Vos SB, Jones DK, Jeurissen B, Viergever MA, Leemans A. The influence of complex white matter architecture on the mean diffusivity in diffusion tensor MRI of the human brain. Neuroimage. 2012;59(3):2208–16.CrossRefPubMedGoogle Scholar
  13. 13.
    Douaud G, Behrens TE, Poupon C, Cointepas Y, Jbabdi S, Gaura V, et al. In vivo evidence for the selective subcortical degeneration in Huntington’s disease. Neuroimage. 2009;46(4):958–66.CrossRefPubMedGoogle Scholar
  14. 14.
    Ennis DB, Kindlmann G. Orthogonal tensor invariants and the analysis of diffusion tensor magnetic resonance images. Magn Reson Med. 2006;55(1):136–46.CrossRefPubMedGoogle Scholar
  15. 15.
    Jensen JH, Helpern JA. MRI quantification of non-Gaussian water diffusion by kurtosis analysis. NMR Biomed. 2010;23(7):698–710 [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t Review].PubMedCentralCrossRefPubMedGoogle Scholar
  16. 16.
    Van Cauter S, De Keyzer F, Sima DM, Croitor Sava A, D’Arco F, Veraart J, et al. Integrating diffusion kurtosis imaging, dynamic susceptibility-weighted contrast-enhanced MRI, and short echo time chemical shift imaging for grading gliomas. Neuro Oncol. 2014;16:1010.PubMedCentralCrossRefPubMedGoogle Scholar
  17. 17.
    Gooijers J, Leemans A, Van Cauter S, Sunaert S, Swinnen SP, Caeyenberghs K. White matter organization in relation to upper limb motor control in healthy subjects: exploring the added value of diffusion kurtosis imaging. Brain Struct Funct. 2014;219:1627.CrossRefPubMedGoogle Scholar
  18. 18.
    Billiet T, Maedler B, D’Arco F, Peeters R, Plasschaert E, Leemans A, et al. Characterizing the microstructure of “unidentified bright objects” in neurofibromatosis type 1: a combined in vivo multi-exponential T2 relaxation and multi-shell diffusion MRI analysis. Neuroimage Clin. 2014;4:649–58.PubMedCentralCrossRefPubMedGoogle Scholar
  19. 19.
    Van Cauter S, Veraart J, Sijbers J, Peeters RR, Himmelreich U, De Keyzer F, et al. Gliomas: diffusion kurtosis MR imaging in grading. Radiology. 2012;263(2):492–501.CrossRefPubMedGoogle Scholar
  20. 20.
    Veraart J, Poot DH, Van Hecke W, Blockx I, Van der Linden A, Verhoye M, et al. More accurate estimation of diffusion tensor parameters using diffusion Kurtosis imaging. Magn Reson Med. 2011;65(1):138–45 [Research Support, Non-U.S. Gov’t].CrossRefPubMedGoogle Scholar
  21. 21.
    Panagiotaki E, Schneider T, Siow B, Hall MG, Lythgoe MF, Alexander DC. Compartment models of the diffusion MR signal in brain white matter: a taxonomy and comparison. Neuroimage. 2012;59(3):2241–54 [Comparative Study Research Support, Non-U.S. Gov’t].CrossRefPubMedGoogle Scholar
  22. 22.
    Assaf Y, Basser PJ. Composite hindered and restricted model of diffusion (CHARMED) MR imaging of the human brain. Neuroimage. 2005;27(1):48–58.CrossRefPubMedGoogle Scholar
  23. 23.
    Assaf Y, Blumenfeld‐Katzir T, Yovel Y, Basser PJ. AxCaliber: a method for measuring axon diameter distribution from diffusion MRI. Magn Reson Med. 2008;59(6):1347–54.PubMedCentralCrossRefPubMedGoogle Scholar
  24. 24.
    Alexander DC, Hubbard PL, Hall MG, Moore EA, Ptito M, Parker GJM, et al. Orientationally invariant indices of axon diameter and density from diffusion MRI. Neuroimage. 2010;52(4):1374–89.CrossRefPubMedGoogle Scholar
  25. 25.
    Assaf Y, Alexander DC, Jones DK, Bizzi A, Behrens TEJ, Clark CA, et al. The CONNECT project: combining macro-and micro-structure. Neuroimage. 2013;80:273.CrossRefPubMedGoogle Scholar
  26. 26.
    Zhang H, Schneider T, Wheeler-Kingshott CA, Alexander DC. NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage. 2012;61(4):1000–16 [Research Support, Non-U.S. Gov’t].CrossRefPubMedGoogle Scholar
  27. 27.
    Polders DL, Leemans A, Hendrikse J, Donahue MJ, Luijten PR, Hoogduin JM. Signal to noise ratio and uncertainty in diffusion tensor imaging at 1.5, 3.0, and 7.0 Tesla. J Magn Reson Imaging. 2011;33(6):1456–63.CrossRefPubMedGoogle Scholar
  28. 28.
    Basser PJ, Pierpaoli C. A simplified method to measure the diffusion tensor from seven MR images. Magn Reson Med. 1998;39(6):928–34.CrossRefPubMedGoogle Scholar
  29. 29.
    Jones DK. The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: a Monte Carlo study. Magn Reson Med. 2004;51(4):807–15.CrossRefPubMedGoogle Scholar
  30. 30.
    Jones DK, Cercignani M. Twenty‐five pitfalls in the analysis of diffusion MRI data. NMR Biomed. 2010;23(7):803–20.CrossRefPubMedGoogle Scholar
  31. 31.
    Jones DK, Williams SC, Gasston D, Horsfield MA, Simmons A, Howard R. Isotropic resolution diffusion tensor imaging with whole brain acquisition in a clinically acceptable time. Hum Brain Mapp. 2002;15(4):216–30.CrossRefPubMedGoogle Scholar
  32. 32.
    Tournier JD, Mori S, Leemans A. Diffusion tensor imaging and beyond. Magn Reson Med. 2011;65(6):1532–56.PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Froeling M, Tax CMW, Vos SB, Luijten PR, Leemans A, editors. MASSIVE: multiple acquisitions for standardization of structural imaging validation and evaluation. International Society for Magnetic Resonance Imaging in Medicine Annual Scientific Meeting & Exhibition; 2014; Milan, Italy.Google Scholar
  34. 34.
    Jeurissen B, Leemans A, Tournier JD, Jones DK, Sijbers J. Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Hum Brain Mapp. 2013;34(11):2747–66.CrossRefPubMedGoogle Scholar
  35. 35.
    Pierpaoli C, Basser PJ. Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med. 1996;36(6):893–906.CrossRefPubMedGoogle Scholar
  36. 36.
    Jones DK, Knösche TR, Turner R. White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage. 2013;73:239–54.CrossRefPubMedGoogle Scholar
  37. 37.
    Jones DK, Basser PJ. “Squashing peanuts and smashing pumpkins”: how noise distorts diffusion-weighted MR data. Magn Reson Med. 2004;52(5):979–93.CrossRefPubMedGoogle Scholar
  38. 38.
    Descoteaux M, Deriche R, Le Bihan D, Mangin JF, Poupon C. Diffusion propagator imaging: using Laplace’s equation and multiple shell acquisitions to reconstruct the diffusion propagator. Inf Process Med Imaging. 2009;21:1–13.CrossRefPubMedGoogle Scholar
  39. 39.
    Veraart J, Sijbers J, Sunaert S, Leemans A, Jeurissen B. Weighted linear least squares estimation of diffusion MRI parameters: strengths, limitations, and pitfalls. Neuroimage. 2013;81:335–46 [Research Support, Non-U.S. Gov’t].CrossRefPubMedGoogle Scholar
  40. 40.
    Jones DK, Leemans A. Diffusion tensor imaging. Methods Mol Biol. 2011;711:127–44.CrossRefPubMedGoogle Scholar
  41. 41.
    Metzler-Baddeley C, O’Sullivan MJ, Bells S, Pasternak O, Jones DK. How and how not to correct for CSF-contamination in diffusion MRI. Neuroimage. 2012;59(2):1394–403.CrossRefPubMedGoogle Scholar
  42. 42.
    Leemans A, Jones DK. The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med. 2009;61(6):1336–49.CrossRefPubMedGoogle Scholar
  43. 43.
    Beaulieu C. What makes diffusion anisotropic in the nervous system? In: Jones DK, editor. Diffusion MRI: theory, methods and applications. New York, NY: Oxford University Press; 2011. p. 92–109.Google Scholar
  44. 44.
    Assaf Y, Pasternak O. Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci. 2008;34(1):51–61.CrossRefPubMedGoogle Scholar
  45. 45.
    Budde MD, Kim JH, Liang HF, Schmidt RE, Russell JH, Cross AH, et al. Toward accurate diagnosis of white matter pathology using diffusion tensor imaging. Magn Reson Med. 2007;57(4):688–95.CrossRefPubMedGoogle Scholar
  46. 46.
    Filley CM. White matter and behavioral neurology. Ann N Y Acad Sci. 2005;1064:162–83.CrossRefPubMedGoogle Scholar
  47. 47.
    Horsfield MA, Jones DK. Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases – a review. NMR Biomed. 2002;15(7-8):570–7.CrossRefPubMedGoogle Scholar
  48. 48.
    Werring DJ, Clark CA, Barker GJ, Thompson AJ, Miller DH. Diffusion tensor imaging of lesions and normal-appearing white matter in multiple sclerosis. Neurology. 1999;52(8):1626–32.CrossRefPubMedGoogle Scholar
  49. 49.
    Cascio CJ, Gerig G, Piven J. Diffusion tensor imaging: application to the study of the developing brain. J Am Acad Child Adolesc Psychiatry. 2007;46(2):213–23.CrossRefPubMedGoogle Scholar
  50. 50.
    Hüppi PS, Maier SE, Peled S, Zientara GP, Barnes PD, Jolesz FA, et al. Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res. 1998;44(4):584–90.CrossRefPubMedGoogle Scholar
  51. 51.
    Lebel C, Walker L, Leemans A, Phillips L, Beaulieu C. Microstructural maturation of the human brain from childhood to adulthood. Neuroimage. 2008;40(3):1044–55.CrossRefPubMedGoogle Scholar
  52. 52.
    Partridge SC, Mukherjee P, Henry RG, Miller SP, Berman JI, Jin H, et al. Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. Neuroimage. 2004;22(3):1302–14.CrossRefPubMedGoogle Scholar
  53. 53.
    Wozniak JR, Lim KO. Advances in white matter imaging: a review of in vivo magnetic resonance methodologies and their applicability to the study of development and aging. Neurosci Biobehav Rev. 2006;30(6):762–74.PubMedCentralCrossRefPubMedGoogle Scholar
  54. 54.
    Mabbott DJ, Noseworthy M, Bouffet E, Laughlin S, Rockel C. White matter growth as a mechanism of cognitive development in children. Neuroimage. 2006;33(3):936–46.CrossRefPubMedGoogle Scholar
  55. 55.
    Nagy Z, Westerberg H, Klingberg T. Maturation of white matter is associated with the development of cognitive functions during childhood. J Cogn Neurosci. 2004;16(7):1227–33.CrossRefPubMedGoogle Scholar
  56. 56.
    Schmithorst VJ, Wilke M, Dardzinski BJ, Holland SK. Cognitive functions correlate with white matter architecture in a normal pediatric population: a diffusion tensor MRI study. Hum Brain Mapp. 2005;26(2):139–47.PubMedCentralCrossRefPubMedGoogle Scholar
  57. 57.
    Hüppi PS, Dubois J. Diffusion tensor imaging of brain development. Semin Fetal Neonatal Med. 2006;11(6):489–97.CrossRefPubMedGoogle Scholar
  58. 58.
    Zhai G, Lin W, Wilber KP, Gerig G, Gilmore JH. Comparisons of Regional White Matter Diffusion in Healthy Neonates and Adults Performed with a 3.0-T Head-only MR Imaging Unit. Radiology. 2003;229(3):673–81.CrossRefPubMedGoogle Scholar
  59. 59.
    Sullivan EV, Pfefferbaum A. DTI in aging and age-related neurodegenerative disorders. In: Jones DK, editor. Diffusion MRI: theory, methods and applications. New York, NY: Oxford University Press; 2011.Google Scholar
  60. 60.
    Huang H, Zhang J, Wakana S, Zhang W, Ren T, Richards LJ, et al. White and gray matter development in human fetal, newborn and pediatric brains. Neuroimage. 2006;33(1):27–38 [Research Support, N.I.H., Extramural].CrossRefPubMedGoogle Scholar
  61. 61.
    Maas LC, Mukherjee P, Carballido-Gamio J, Veeraraghavan S, Miller SP, Partridge SC, et al. Early laminar organization of the human cerebrum demonstrated with diffusion tensor imaging in extremely premature infants. Neuroimage. 2004;22(3):1134–40.CrossRefPubMedGoogle Scholar
  62. 62.
    Ulug AM, Beauchamp Jr N, Bryan RN, van Zijl PC. Absolute quantitation of diffusion constants in human stroke. Stroke. 1997;28(3):483–90.CrossRefPubMedGoogle Scholar
  63. 63.
    Engelbrecht V, Scherer A, Rassek M, Witsack HJ, Mödder U. Diffusion-weighted MR imaging in the brain in children: findings in the normal brain and in the brain with white matter diseases. Radiology. 2002;222(2):410–8.CrossRefPubMedGoogle Scholar
  64. 64.
    Oishi K, Mori S, Donohue PK, Ernst T, Anderson L, Buchthal S, et al. Multi-contrast human neonatal brain atlas: application to normal neonate development analysis. Neuroimage. 2011;56(1):8–20.PubMedCentralCrossRefPubMedGoogle Scholar
  65. 65.
    Xu D, Mukherjee P, Barkovich AJ. Pediatric brain injury: can DTI scalars predict functional outcome? Pediatr Radiol. 2013;43(1):55–9.PubMedCentralCrossRefPubMedGoogle Scholar
  66. 66.
    Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage. 2002;17(3):1429–36 [Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, P.H.S.].CrossRefPubMedGoogle Scholar
  67. 67.
    Field AS, Alexander AL, Wu Y-C, Hasan KM, Witwer B, Badie B. Diffusion tensor eigenvector directional color imaging patterns in the evaluation of cerebral white matter tracts altered by tumor. J Magn Reson Imaging. 2004;20(4):555–62.CrossRefPubMedGoogle Scholar
  68. 68.
    Wheeler-Kingshott CAM, Cercignani M. About “axial” and “radial” diffusivities. Magn Reson Med. 2009;61(5):1255–60.CrossRefPubMedGoogle Scholar
  69. 69.
    Cercignani M, Alexander DC. Optimal acquisition schemes for in vivo quantitative magnetization transfer MRI. Magn Reson Med. 2006;56(4):803–10.CrossRefPubMedGoogle Scholar
  70. 70.
    Sled JG, Pike GB. Quantitative imaging of magnetization transfer exchange and relaxation properties in vivo using MRI. Magn Reson Med. 2001;46(5):923–31.CrossRefPubMedGoogle Scholar
  71. 71.
    Kolind SH, Deoni SC. Rapid three-dimensional multicomponent relaxation imaging of the cervical spinal cord. Magn Reson Med. 2011;65(2):551–6 [Research Support, Non-U.S. Gov’t].CrossRefPubMedGoogle Scholar
  72. 72.
    MacKay A, Laule C, Vavasour I, Bjarnason T, Kolind S, Madler B. Insights into brain microstructure from the T2 distribution. Magn Reson Imaging. 2006;24(4):515–25.CrossRefPubMedGoogle Scholar
  73. 73.
    Leemans A. Visualisation of diffusion MRI data. In: Jones DK, editor. Diffusion MRI: theory, methods and applications. New York, NY: Oxford University Press; 2011. p. 354–79.Google Scholar
  74. 74.
    Dubois J, Dehaene-Lambertz G, Perrin M, Mangin J-F, Cointepas Y, Duchesnay E, et al. Asynchrony of the early maturation of white matter bundles in healthy infants: quantitative landmarks revealed noninvasively by diffusion tensor imaging. Hum Brain Mapp. 2008;29(1):14–27.CrossRefPubMedGoogle Scholar
  75. 75.
    Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, et al. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci. 1999;2(10):861–3.CrossRefPubMedGoogle Scholar
  76. 76.
    Hulkower MB, Poliak DB, Rosenbaum SB, Zimmerman ME, Lipton ML. A decade of DTI in traumatic brain injury: 10 years and 100 articles later. AJNR Am J Neuroradiol. 2013;34:2064.CrossRefPubMedGoogle Scholar
  77. 77.
    Douaud G, Jbabdi S, Behrens TE, Menke RA, Gass A, Monsch AU, et al. DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer’s disease. Neuroimage. 2011;55(3):880–90.CrossRefPubMedGoogle Scholar
  78. 78.
    Pierpaoli C, Barnett A, Pajevic S, Chen R, Penix L, Virta A, et al. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage. 2001;13(6):1174–85.CrossRefPubMedGoogle Scholar
  79. 79.
    Leemans A, Sijbers J, Verhoye M, Van der Linden A, Van Dyck D. Mathematical framework for simulating diffusion tensor MR neural fiber bundles. Magn Reson Med. 2005;53(4):944–53.CrossRefPubMedGoogle Scholar
  80. 80.
    Wheeler-Kingshott CA, Ciccarelli O, Schneider T, Alexander DC, Cercignani M. A new approach to structural integrity assessment based on axial and radial diffusivities. Funct Neurol. 2012;27(2):85–90 [Research Support, Non-U.S. Gov’t].PubMedCentralPubMedGoogle Scholar
  81. 81.
    Szczepankiewicz F, Latt J, Wirestam R, Leemans A, Sundgren P, van Westen D, et al. Variability in diffusion kurtosis imaging: impact on study design, statistical power and interpretation. Neuroimage. 2013;76:145–54 [Research Support, Non-U.S. Gov’t].CrossRefPubMedGoogle Scholar
  82. 82.
    Vos SB, Jones DK, Viergever MA, Leemans A. Partial volume effect as a hidden covariate in DTI analyses. Neuroimage. 2011;55(4):1566–76.CrossRefPubMedGoogle Scholar
  83. 83.
    Concha L, Gross DW, Beaulieu C. Diffusion tensor tractography of the limbic system. AJNR Am J Neuroradiol. 2005;26(9):2267–74.PubMedGoogle Scholar
  84. 84.
    Chou MC, Lin YR, Huang TY, Wang CY, Chung HW, Juan CJ, et al. FLAIR diffusion-tensor MR tractography: comparison of fiber tracking with conventional imaging. AJNR Am J Neuroradiol. 2005;26(3):591–7.PubMedGoogle Scholar
  85. 85.
    Pasternak O, Sochen N, Gur Y, Intrator N, Assaf Y. Free water elimination and mapping from diffusion MRI. Magn Reson Med. 2009;62(3):717–30.CrossRefPubMedGoogle Scholar
  86. 86.
    Pierpaoli C, Jones D, editors. Removing CSF contamination in brain DT-MRIs by using a two-compartment tensor model. Proceedings of the International Society for Magnetic Resonance in Medicine. 12th Scientific meeting ISMRM04; 2004. p. 1215Google Scholar
  87. 87.
    Chaddock CA, Barker GJ, Marshall N, Schulze K, Hall MH, Fern A, et al. White matter microstructural impairments and genetic liability to familial bipolar I disorder. Br J Psychiatry. 2009;194(6):527–34.CrossRefPubMedGoogle Scholar
  88. 88.
    Emsell L, Chaddock C, Forde N, Van Hecke W, Barker GJ, Leemans A, et al. White matter microstructural abnormalities in families multiply affected with bipolar I disorder: a diffusion tensor tractography study. Psychol Med. 2013;27:1–12.Google Scholar
  89. 89.
    Cook PA, Bai Y, Nedjati-Gilani S, Seunarine KK, Hall MG, Parker GJ, et al., editors. Camino: open-source diffusion-MRI reconstruction and processing 2006. Proceedings of the International Society for Magnetic Resonance in Medicine. 14th Scientific Meeting, Seattle, WA, May 2006; p. 2759Google Scholar

Suggested Reading

  1. 90.
    Jones DK, Cercignani M. Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed. 2010;23(7):803–20.CrossRefPubMedGoogle Scholar
  2. 91.
    Jones DK, Knösche TR, Turner R. White matter integrity, fibre count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage. 2013;73:239–54.CrossRefPubMedGoogle Scholar
  3. 92.
    Tournier JD, Mori S, Leemans A. Diffusion tensor imaging and beyond. Magn Reson Med. 2011;65(6):1532–56.PubMedCentralCrossRefPubMedGoogle Scholar
  4. 93.
    Wheeler-Kingshott CAM, Cercignani M. About “axial” and “radial” diffusivities. Magn Reson Med. 2009;61(5):1255–60.CrossRefPubMedGoogle Scholar
  5. 94.
    Concha L. A macroscopic view of microstructure: using diffusion-weighted images to infer damage, repair, and plasticity of white matter. Neuroscience. 2014;276:14–28.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Kathleen M. Curran
    • 1
  • Louise Emsell
    • 2
    • 3
  • Alexander Leemans
    • 4
  1. 1.Complex & Adaptive Systems Laboratory, School of Medicine & Medical SciencesUniversity College DublinDublinIreland
  2. 2.Translational MRI, Department of Imaging and Pathology, KU Leuven and RadiologyUniversity Hospitals LeuvenLeuvenBelgium
  3. 3.Universitair Psychiatrisch Centrum (UPC), KU LeuvenLeuvenBelgium
  4. 4.PROVIDI Lab, Image Sciences InstituteUniversity Medical Center UtrechtUtrechtThe Netherlands

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