Advertisement

Functional MR and Diffusion MR Imaging in Diffuse Low-Grade Gliomas

  • Alberto BizziEmail author
Chapter

Abstract

In the last decade, functional MR imaging and MR tractography with diffusion tensor imaging have changed the way to evaluate patients with glioma before surgery, in particular when the tumor is infiltrating eloquent brain structures. Mapping of cortical sites and white matter pathways may improve presurgical planning and surgical targeting with neuronavigational devices, and it may reduce intraoperative time. Clinical use of these advanced MR imaging tools is growing in importance, and exams in patients are increasingly being requested by neurosurgeons worldwide. Applications and current limitations of fMRI and MR diffusion tractography are discussed focusing on the sensorimotor, speech, and visuospatial networks.

Keywords

Functional MR imaging MR tractography Diffusion MR imaging Low-grade glioma Language network Visuospatial network 

Notes

Acknowledgments

Part of this work was supported by a grant of the Consortium of Neuroimagers for the Noninvasive Assessment of Brain Connectivity and Tracts (CONNECT) team, funded by the European Commission under Framework Package 7 and a grant provided by family and friends in memory of Mr. Luca Dresti.

Tortoise software v. 1.3.0 (https://science.nichd.nih.gov/confluence/display/nihpd/TORTOISE) and Trackvis software v. 0.5.2.1 (www.trackvis.org) were used to ­process DTI datasets and generate virtual dissections of the white matter tracts displayed on Figs. 20.1, 20.2, 20.3, 20.4, 20.5, and 20.6.

References

  1. 1.
    Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA. 1990;87(24):9868–72.PubMedCrossRefGoogle Scholar
  2. 2.
    Basser PJ, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys J. 1994;66(1):259–67.PubMedCrossRefGoogle Scholar
  3. 3.
    Belliveau JW, Kennedy Jr DN, McKinstry RC, Buchbinder BR, Weisskoff RM, Cohen MS, et al. Functional mapping of the human visual cortex by magnetic resonance imaging. Science. 1991;254(5032):716–9.PubMedCrossRefGoogle Scholar
  4. 4.
    Clark CA, Barrick TR, Murphy MM, Bell BA. White matter fiber tracking in patients with space-occupying lesions of the brain: a new technique for neurosurgical planning? Neuroimage. 2003;20(3):1601–8.PubMedCrossRefGoogle Scholar
  5. 5.
    Conturo TE, Lori NF, Cull TS, Akbudak E, Snyder AZ, Shimony JS, et al. Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci USA. 1999;96(18):10422–7.PubMedCrossRefGoogle Scholar
  6. 6.
    Mori S, Crain BJ, Chacko VP, van Zijl PC. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol. 1999;45(2):265–9.PubMedCrossRefGoogle Scholar
  7. 7.
    Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, et al. Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol. 2008;26(8):1338–45.PubMedCrossRefGoogle Scholar
  8. 8.
    Duffau H. Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol. 2005;4(8):476–86.PubMedCrossRefGoogle Scholar
  9. 9.
    Petrella JR, Shah LM, Harris KM, Friedman AH, George TM, Sampson JH, et al. Preoperative functional MR imaging localization of language and motor areas: effect on therapeutic decision making in patients with potentially resectable brain tumors. Radiology. 2006;240(3):793–802.PubMedCrossRefGoogle Scholar
  10. 10.
    Bobholz JA, Rao SM, Saykin AJ, Pliskin N. Clinical use of functional magnetic resonance imaging: reflections on the new CPT codes. Neuropsychol Rev. 2007;17(2):189–91.PubMedCrossRefGoogle Scholar
  11. 11.
    Logothetis NK. The underpinnings of the BOLD functional magnetic resonance imaging signal. J Neurosci. 2003;23(10):3963–71.PubMedGoogle Scholar
  12. 12.
    Logothetis NK. What we can do and what we cannot do with fMRI. Nature. 2008;453(7197):869–78.PubMedCrossRefGoogle Scholar
  13. 13.
    Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. 2001;412(6843):150–7.PubMedCrossRefGoogle Scholar
  14. 14.
    Logothetis NK, Wandell BA. Interpreting the BOLD signal. Annu Rev Physiol. 2004;66:735–69.PubMedCrossRefGoogle Scholar
  15. 15.
    Zhang D, Johnston JM, Fox MD, Leuthardt EC, Grubb RL, Chicoine MR, et al. Preoperative sensorimotor mapping in brain tumor patients using spontaneous fluctuations in neuronal activity imaged with functional magnetic resonance imaging: initial experience. Neurosurgery. 2009;65(6 Suppl):226–36.PubMedGoogle Scholar
  16. 16.
    Briganti C, Sestieri C, Mattei PA, Esposito R, Galzio RJ, Tartaro A, et al. Reorganization of functional connectivity of the language network in patients with brain gliomas. AJNR Am J Neuroradiol. 2012;33(10):1983–90.Google Scholar
  17. 17.
    Esposito R, Mattei PA, Briganti C, Romani GL, Tartaro A, Caulo M. Modifications of default-mode network connectivity in patients with cerebral glioma. PLoS One. 2012;7(7):e40231.PubMedCrossRefGoogle Scholar
  18. 18.
    Smits M, Visch-Brink E, Schraa-Tam CK, Koudstaal PJ, van der Lugt A. Functional MR imaging of language processing: an overview of easy-to-implement paradigms for patient care and clinical research. Radiographics. 2006;26 Suppl 1:S145–58. Review.PubMedCrossRefGoogle Scholar
  19. 19.
    Simoes-Franklin C, Whitaker TA, Newell FN. Active and passive touch differentially activate somatosensory cortex in texture perception. Hum Brain Mapp. 2011;32(7):1067–80.PubMedCrossRefGoogle Scholar
  20. 20.
    Schweisfurth MA, Schweizer R, Frahm J. Functional MRI indicates consistent intra-digit topographic maps in the little but not the index finger within the human primary somatosensory cortex. Neuroimage. 2011;56(4):2138–43.PubMedCrossRefGoogle Scholar
  21. 21.
    Wedeen VJ, Rosene DL, Wang R, Dai G, Mortazavi F, Hagmann P, et al. The geometric structure of the brain fiber pathways. Science. 2012;335(6076):1628–34.PubMedCrossRefGoogle Scholar
  22. 22.
    Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G. Diffusion tensor MR imaging of the human brain. Radiology. 1996;201(3):637–48.PubMedGoogle Scholar
  23. 23.
    Catani M, Thiebaut de Schotten M. A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex. 2008;44(8):1105–32.PubMedCrossRefGoogle Scholar
  24. 24.
    Oishi K, Zilles K, Amunts K, Faria A, Jiang H, Li X, et al. Human brain white matter atlas: identification and assignment of common anatomical structures in super­ficial white matter. Neuroimage. 2008;43(3):447–57.PubMedCrossRefGoogle Scholar
  25. 25.
    Dell’acqua F, Catani M. Structural human brain networks: hot topics in diffusion tractography. Curr Opin Neurol. 2012;25(4):375–83.PubMedGoogle Scholar
  26. 26.
    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. 2012. Accessed on 19 May 2012. doi:  10.1002/hbm.22099. [Epub ahead of print]
  27. 27.
    Ohue S, Kohno S, Inoue A, Yamashita D, Harada H, Kumon Y, et al. Accuracy of diffusion tensor magnetic resonance imaging-based tractography for surgery of gliomas near the pyramidal tract: a significant correlation between subcortical electrical stimulation and postoperative tractography. Neurosurgery. 2012;70(2):283–93; discussion 94.PubMedCrossRefGoogle Scholar
  28. 28.
    Berman JI, Berger MS, Chung SW, Nagarajan SS, Henry RG. Accuracy of diffusion tensor magnetic resonance imaging tractography assessed using intraoperative subcortical stimulation mapping and magnetic source imaging. J Neurosurg. 2007;107(3):488–94.PubMedCrossRefGoogle Scholar
  29. 29.
    Bello L, Gambini A, Castellano A, Carrabba G, Acerbi F, Fava E, et al. Motor and language DTI Fiber Tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage. 2008;39(1):369–82.PubMedCrossRefGoogle Scholar
  30. 30.
    Mesulam MM. Defining neurocognitive networks in the BOLD new world of computed connectivity. Neuron. 2009;62:1–3.PubMedCrossRefGoogle Scholar
  31. 31.
    Hickok G, Poeppel D. Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language. Cognition. 2004;92(1–2):67–99.PubMedCrossRefGoogle Scholar
  32. 32.
    Hickok G, Poeppel D. The cortical organization of speech processing. Nat Rev Neurosci. 2007;8(5):393–402.PubMedCrossRefGoogle Scholar
  33. 33.
    Weiller C, Bormann T, Saur D, Musso M, Rijntjes M. How the ventral pathway got lost: and what its recovery might mean. Brain Lang. 2011;118(1–2):29–39.PubMedCrossRefGoogle Scholar
  34. 34.
    Catani M, Jones DK, Ffytche DH. Perisylvian language networks of the human brain. Ann Neurol. 2005;57(1):8–16.PubMedCrossRefGoogle Scholar
  35. 35.
    Lawes IN, Barrick TR, Murugam V, Spierings N, Evans DR, Song M, et al. Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. Neuroimage. 2008;39(1):62–79.PubMedCrossRefGoogle Scholar
  36. 36.
    Petrides M, Pandya DN. Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey. J Comp Neurol. 1988;273:52–66.PubMedCrossRefGoogle Scholar
  37. 37.
    Thiebaut de Schotten M, Dell’Acqua F, Forkel SJ, Simmons A, Vergani F, Murphy DG, et al. A lateralized brain network for visuospatial attention. Nat Neurosci. 2011;14(10):1245–6.PubMedCrossRefGoogle Scholar
  38. 38.
    Catani M, Mesulam M. The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. Cortex. 2008;44(8):953–61.PubMedCrossRefGoogle Scholar
  39. 39.
    Weiller C, Musso M, Rijntjes M, Saur D. Please don’t underestimate the ventral pathway in language. Trends Cogn Sci. 2009;13(9):369–70; 70–1.PubMedCrossRefGoogle Scholar
  40. 40.
    Saur D, Kreher BW, Schnell S, Kummerer D, Kellmeyer P, Vry MS, et al. Ventral and dorsal pathways for language. Proc Natl Acad Sci USA. 2008;105(46):18035–40.PubMedCrossRefGoogle Scholar
  41. 41.
    Kier EL, Staib LH, Davis LM, Bronen RA. MR imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer’s loop of the optic radiation. AJNR Am J Neuroradiol. 2004;25(5):677–91.PubMedGoogle Scholar
  42. 42.
    Bizzi A. Presurgical mapping of verbal language in brain tumors with functional MR imaging and MR tractography. In: Pia Sundgren M, editor. Advanced imaging techniques in brain tumors. Elsevier, Canada; 2009. p. 573–96.Google Scholar
  43. 43.
    de Schotten MT, Ffytche DH, Bizzi A, Dell’Acqua F, Allin M, Walshe M, et al. Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. Neuroimage. 2011;54(1):49–59.CrossRefGoogle Scholar
  44. 44.
    Catani M, Howard RJ, Pajevic S, Jones DK. Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage. 2002;17(1):77–94.PubMedCrossRefGoogle Scholar
  45. 45.
    Bizzi A, Nava S, Ferre F, Castelli G, Aquino D, Ciaraffa F, et al. Aphasia induced by gliomas growing in the ventrolateral frontal region: assessment with diffusion MR tractography, functional MR imaging and neuropsychology. Cortex. 2012;48(2):255–72.PubMedCrossRefGoogle Scholar
  46. 46.
    Dejerine J, Dejerine-Klumpke A. Anatomies des centres nerveux. Paris: Rueff et Cie; 1895.Google Scholar
  47. 47.
    Catani M, Dell’acqua F, Vergani F, Malik F, Hodge H, Roy P, et al. Short frontal lobe connections of the human brain. Cortex. 2012;48(2):273–91.PubMedCrossRefGoogle Scholar
  48. 48.
    Ford A, McGregor KM, Case K, Crosson B, White KD. Structural connectivity of Broca’s area and medial frontal cortex. Neuroimage. 2010;52(4):1230–7.PubMedCrossRefGoogle Scholar
  49. 49.
    Petrides M, Pandya DN. Distinct parietal and temporal pathways to the homologues of Broca’s area in the monkey. PLoS Biol. 2009;7(8):e1000170.PubMedCrossRefGoogle Scholar
  50. 50.
    Frey S, Campbell JS, Pike GB, Petrides M. Dissociating the human language pathways with high angular resolution diffusion fiber tractography. J Neurosci. 2008;28(45):11435–44.PubMedCrossRefGoogle Scholar
  51. 51.
    Martino J, De Witt Hamer PC, Vergani F, Brogna C, de Lucas EM, Vazquez-Barquero A, et al. Cortex-sparing fiber dissection: an improved method for the study of white matter anatomy in the human brain. J Anat. 2011;219(4):531–41.PubMedCrossRefGoogle Scholar
  52. 52.
    Dronkers NF, Plaisant O, Iba-Zizen MT, Cabanis EA. Paul Broca’s historic cases: high resolution MR imaging of the brains of Leborgne and Lelong. Brain. 2007;130(Pt 5):1432–41.PubMedCrossRefGoogle Scholar
  53. 53.
    Dronkers NF. A new brain region for coordinating speech articulation. Nature. 1996;384(6605):159–61.PubMedCrossRefGoogle Scholar
  54. 54.
    Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Sichez JP, et al. Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain. 2002;125(Pt 1):199–214.PubMedCrossRefGoogle Scholar
  55. 55.
    Duffau H, Gatignol P, Denvil D, Lopes M, Capelle L. The articulatory loop: study of the subcortical connectivity by electrostimulation. Neuroreport. 2003;14(15):2005–8.PubMedCrossRefGoogle Scholar
  56. 56.
    Bello L, Gallucci M, Fava M, Carrabba G, Giussani C, Acerbi F, et al. Intraoperative subcortical language tract mapping guides surgical removal of gliomas involving speech areas. Neurosurgery. 2007;60(1):67–82.PubMedCrossRefGoogle Scholar
  57. 57.
    Duffau H, Gatignol P, Mandonnet E, Peruzzi P, Tzourio-Mazoyer N, Capelle L. New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. Brain. 2005;128(Pt 4):797–810.PubMedCrossRefGoogle Scholar
  58. 58.
    Mandonnet E, Nouet A, Gatignol P, Capelle L, Duffau H. Does the left inferior longitudinal fasciculus play a role in language? A brain stimulation study. Brain. 2007;130(Pt 3):623–9.PubMedCrossRefGoogle Scholar
  59. 59.
    Shinoura N, Suzuki Y, Tsukada M, Yoshida M, Yamada R, Tabei Y, et al. Deficits in the left inferior longitudinal fasciculus results in impairments in object naming. Neurocase. 2010;16(2):135–9.PubMedCrossRefGoogle Scholar
  60. 60.
    Papagno C, Miracapillo C, Casarotti A, Romero Lauro LJ, Castellano A, Falini A, et al. What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. Brain. 2011;134(2):405–14.PubMedCrossRefGoogle Scholar
  61. 61.
    Corbetta M, Shulman GL. Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci. 2002;3(3):201–15.PubMedCrossRefGoogle Scholar
  62. 62.
    Thiebaut de Schotten M, Urbanski M, Duffau H, Volle E, Levy R, Dubois B, et al. Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science. 2005;309:2226.PubMedCrossRefGoogle Scholar
  63. 63.
    Vallar G, Perani D. The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man. Neuropsychologia. 1986;24(5):609–22.PubMedCrossRefGoogle Scholar
  64. 64.
    Stone SP, Wilson B, Wroot A, Halligan PW, Lange LS, Marshall JC, et al. The assessment of visuo-spatial neglect after acute stroke. J Neurol Neurosurg Psychiatry. 1991;54(4):345–50.PubMedCrossRefGoogle Scholar
  65. 65.
    Ciaraffa F, Castelli G, Parati EA, Bartolomeo P, Bizzi A. Visual neglect as a disconnection syndrome? A confirmatory case report. Neurocase. 2012. Accessed on 2 May 2012. [Epub ahead of print]Google Scholar
  66. 66.
    Urbanski M, Thiebaut de Schotten M, Rodrigo S, Catani M, Oppenheim C, Touze E, et al. Brain networks of spatial awareness: evidence from diffusion tensor imaging tractography. J Neurol Neurosurg Psychiatry. 2008;79(5):598–601.PubMedCrossRefGoogle Scholar
  67. 67.
    Urbanski M, Thiebaut de Schotten M, Rodrigo S, Oppenheim C, Touze E, Meder JF, et al. DTI-MR tractography of white matter damage in stroke patients with neglect. Exp Brain Res. 2011;208(4):491–505.PubMedCrossRefGoogle Scholar
  68. 68.
    Dell’acqua F, Simmons A, Williams SC, 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. 2012. Accessed on 5 Apr 2012. doi:  10.1002/hbm.22080. [Epub ahead of print]
  69. 69.
    Jellison BJ, Field AS, Medow J, Lazar M, Salamat MS, Alexander AL. Diffusion tensor imaging of ­cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. AJNR Am J Neuroradiol. 2004;25(3):356–69.PubMedGoogle Scholar
  70. 70.
    Schonberg T, Pianka P, Hendler T, Pasternak O, Assaf Y. Characterization of displaced white matter by brain tumors using combined DTI and fMRI. Neuroimage. 2006;30(4):1100–11.PubMedCrossRefGoogle Scholar
  71. 71.
    Berman JI, Berger MS, Mukherjee P, Henry RG. Diffusion-tensor imaging-guided tracking of fibers of the pyramidal tract combined with intraoperative cortical stimulation mapping in patients with gliomas. J Neurosurg. 2004;101(1):66–72.PubMedCrossRefGoogle Scholar
  72. 72.
    Ducreux D, Lepeintre JF, Fillard P, Loureiro C, Tadie M, Lasjaunias P. MR diffusion tensor imaging and fiber tracking in 5 spinal cord astrocytomas. AJNR Am J Neuroradiol. 2006;27(1):214–6.PubMedGoogle Scholar
  73. 73.
    Berman JI, Chung S, Mukherjee P, Hess CP, Han ET, Henry RG. Probabilistic streamline q-ball tractography using the residual bootstrap. Neuroimage. 2008;39(1):215–22.PubMedCrossRefGoogle Scholar
  74. 74.
    Tournier JD, Calamante F, Connelly A. Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage. 2007;35(4):1459–72.PubMedCrossRefGoogle Scholar
  75. 75.
    Assaf Y, Basser PJ. Composite hindered and restricted model of diffusion (CHARMED) MR imaging of the human brain. Neuroimage. 2005;27(1):48–58.PubMedCrossRefGoogle Scholar
  76. 76.
    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.PubMedCrossRefGoogle Scholar
  77. 77.
    Zhang H, Hubbard PL, Parker GJ, Alexander DC. Axon diameter mapping in the presence of orientation dispersion with diffusion MRI. Neuroimage. 2011;56(3):1301–15.PubMedCrossRefGoogle Scholar
  78. 78.
    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.PubMedCrossRefGoogle Scholar
  79. 79.
    Chang EF, Clark A, Smith JS, Polley MY, Chang SM, Barbaro NM, et al. Functional mapping-guided resection of low-grade gliomas in eloquent areas of the brain: improvement of long-term survival. J Neurosurg. 2011;114(3):566–73.PubMedCrossRefGoogle Scholar
  80. 80.
    Bandettini PA, Wong EC, Hinks RS, Tikofsky RS, Hyde JS. Time course EPI of human brain function during task activation. Magn Reson Med. 1992;25(2):390–7.PubMedCrossRefGoogle Scholar
  81. 81.
    Quiñones-Hinojosa A, Ojemann SG, Sanai N, Dillon WP, Berger MS. Preoperative correlation of intraoperative cortical mapping with magnetic resonance imaging landmarks to predict localization of the Broca area. J Neurosurg. 2003;99(2):311–8.PubMedCrossRefGoogle Scholar
  82. 82.
    Field AS, Alexander AL, Wu YC, 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.PubMedCrossRefGoogle Scholar
  83. 83.
    Mori S, Frederiksen K, van Zijl PC, Stieltjes B, Kraut MA, Solaiyappan M, et al. Brain white matter anatomy of tumor patients evaluated with diffusion tensor imaging. Ann Neurol. 2002;51(3):377–80.PubMedCrossRefGoogle Scholar
  84. 84.
    Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen AG, et al. Intraoperative diffusion-tensor MR imaging: shifting of white matter tracts during neurosurgical procedures – initial experience. Radiology. 2005;234(1):218–25.PubMedCrossRefGoogle Scholar
  85. 85.
    Nimsky C, Ganslandt O, Fahlbusch R. Implementation of fiber tract navigation. Neurosurgery. 2006;58(ONS Suppl 2):ONS-292–304.Google Scholar
  86. 86.
    Turner R. How much cortex can a vein drain? Downstream dilution of activation-related cerebral blood oxygenation changes. Neuroimage. 2002;16(4):1062–7.PubMedCrossRefGoogle Scholar
  87. 87.
    Seunarine KK, Alexander DC. Multiple fibers: beyond the diffusion tensor. In: Johansen-Berg H, Behrens TE, editors. Diffusion MRI: from quantitative measurement to in vivo neuroanatomy. Oxford: Elsevier; 2009. p. 55–72.CrossRefGoogle Scholar
  88. 88.
    Jones DK. Studying connections in the living human brain with diffusion MRI. Cortex. 2008;44(8):936–52.PubMedCrossRefGoogle Scholar
  89. 89.
    Jones DK, Cercignani M. Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed. 2010;23(7):803–20.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag London 2013

Authors and Affiliations

  1. 1.Department of NeuroradiologyIstituto Clinico Humanitas IRCCSRozzano, MilanoItaly

Personalised recommendations