Imaging white matter diffusion changes with development and recovery from brain injury

Developmental Neurorehabilitation

Volumn 11, Issue 3, 2008, Pages 174-186

  Bosnell, Rose ^a   Giorgio, Antonio ^a,b   Johansen Berg, Heidi ^a  

^a JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^b UNIVERSITY OF SIENA   (Italy)

Author keywords

Anatomy; Development; Diffusion tensor imaging; Imaging; Recovery; Tractography

Indexed keywords

BRAIN DEVELOPMENT; BRAIN INJURY; DIFFUSION TENSOR IMAGING; DISEASE COURSE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEAD INJURY; HUMAN; MULTIPLE SCLEROSIS; PRIORITY JOURNAL; REVIEW; STROKE; WHITE MATTER; BRAIN CORTEX; BRAIN DISEASE; CHILD; COMPARATIVE STUDY; CONVALESCENCE; DIFFUSION WEIGHTED IMAGING; FEMALE; FOLLOW UP; GESTATIONAL AGE; IMAGE PROCESSING; INFANT; MALE; METHODOLOGY; MONITORING; NERVOUS SYSTEM MALFORMATION; NEWBORN; PATHOLOGY; PREGNANCY; PRENATAL DEVELOPMENT; PRENATAL DIAGNOSIS; PRESCHOOL CHILD; REFERENCE VALUE; SENSITIVITY AND SPECIFICITY;

BRAIN DISEASES; BRAIN INJURIES; CEREBRAL CORTEX; CHILD; CHILD, PRESCHOOL; DIFFUSION MAGNETIC RESONANCE IMAGING; DISEASE PROGRESSION; FEMALE; FOLLOW-UP STUDIES; GESTATIONAL AGE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INFANT; INFANT, NEWBORN; MALE; MONITORING, PHYSIOLOGIC; NERVOUS SYSTEM MALFORMATIONS; PREGNANCY; PRENATAL DIAGNOSIS; RECOVERY OF FUNCTION; REFERENCE VALUES; SENSITIVITY AND SPECIFICITY;

EID: 58149311207     PISSN: 17518423     EISSN: 17518431     Source Type: Journal    
DOI: 10.1080/17518420802289065     Document Type: Review

References (136)

1. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomedicine 2002;15:435-455.
2. Basser PJ, Mattiello J, LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. Journal of Magnetic Resonance B 1994;103:247-254.
3. Pierpaoli C, Basser PJ. Toward a quantitative assessment of diffusion anisotropy. Magnetic Resonance Medicine 1996; 36:893-906.
4. Alexander AL, Lee JE, Lazar M, Boudos R, DuBray MB, Oakes TR, Miller JN, Lu J, Jeong EK, McMahon WM, et al. Diffusion tensor imaging of the corpus callosum in Autism. Neuroimage 2007;34:61-73.
5. Budde MD, Kim JH, Liang HF, Russell JH, Cross AH, Song SK. Axonal injury detected by in vivo diffusion tensor imaging correlates with neurological disability in a mouse model of multiple sclerosis. NMR Biomedicine 2008;21: 589-597.
6. Deo AA, Grill RJ, Hasan KM, Narayana PA. In vivo serial diffusion tensor imaging of experimental spinal cord injury. Journal of Neuroscience Research 2006;83: 801-810.
7. Kim JH, Loy DN, Liang HF, Trinkaus K, Schmidt RE, Song SK. Noninvasive diffusion tensor imaging of evolving white matter pathology in a mouse model of acute spinal cord injury. Magnetic Resonance Medicine 2007;58: 253-260.
8. Makki MI, Chugani DC, Janisse J, Chugani HT. Characteristics of abnormal diffusivity in normal-appearing white matter investigated with diffusion tensor MR imaging in tuberous sclerosis complex. AJNR: American Journal of Neuroradiology 2007;28:1662-1667.
9. Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 2003;20:1714-1722.
10. 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;17:1429-1436.
11. Sun SW, Liang HF, Schmidt RE, Cross AH, Song SK. Selective vulnerability of cerebral white matter in a murine model of multiple sclerosis detected using diffusion tensor imaging. Neurobiological Diseases 2007;28:30-38.
12. Thomalla G, Glauche V, Weiller C, Rother J. Time course of Wallerian degeneration after ischaemic stroke revealed by diffusion tensor imaging. Journal of Neurology, Neurosurgery and Psychiatry 2005;76:266-268.
13. Wu Q, Butzkueven H, Gresle M, Kirchhoff F, Friedhuber A, Yang Q, Wang H, Fang K, Lei H, Egan GF, et al. MR diffusion changes correlate with ultra-structurally defined axonal degeneration in murine optic nerve. Neuroimage 2007;37:1138-1147.
14. Jones DK, Symms MR, Cercignani M, Howard RJ. The effect of filter size on VBM analyses of DT-MRI data. Neuroimage 2005;26:546-554.
15. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, et al. Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. Neuroimage 2006;31:1487-1505.
16. Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady PM, Smith SM. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magnetic Resonance Medicine 2003;50:1077-1088.
17. Jones DK, Simmons A, Williams SC, Horsfield MA. Non-invasive assessment of axonal fiber connectivity in the human brain via diffusion tensor MRI. Magnetic Resonance Medicine 1999;42:37-41.
18. Mori S, Crain BJ, Chacko VP, van Zijl PC. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Annals of Neurology 1999; 45:265-269.
19. Catani M, Jones DK, ffytche DH. Perisylvian language networks of the human brain. Annals of Neurology 2005; 57:8-16.
20. Johansen-Berg H, Behrens TE. Just pretty pictures? What diffusion tractography can add in clinical neuroscience. Current Opinion in Neurology 2006;19:379-385.
21. Mori S, Itoh R, Zhang J, Kaufmann WE, van Zijl PC, Solaiyappan M, Yarowski P. Diffusion tensor imaging of the developing mouse brain. Magnetic Resonance Medicine 2001;46:18-23.
22. Gupta RK, Hasan KM, Trivedi R, Pradhan M, Das V, Parikh NA, Narayana PA. Diffusion tensor imaging of the developing human cerebrum. Journal of Neuroscience Research 2005;81:172-178.
23. Deipolyi AR, Mukherjee P, Gill K, Henry RG, Partridge SC, Veeraraghavan S, et al. Comparing microstructural and macrostructural development of the cerebral cortex in premature newborns: Diffusion tensor imaging versus cortical gyration. Neuroimage 2005;27:579-586.
24. McKinstry RC, Mathur A, Miller JH, Ozcan A, Snyder AZ, Schefft GL, et al. Radial organization of developing preterm human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. Cerebral Cortex 2002; 12:1237-1243.
25. Bockhorst KH, Narayana PA, Liu R, Ahobila-Vijjula P, Ramu J, Kamel M, et al. Early postnatal development of rat brain: In vivo diffusion tensor imaging. Journal of Neuroscience Research 2008.
26. Sizonenko SV, Camm EJ, Garbow JR, Maier SE, Inder TE, Williams CE, Neil JJ, Huppi PS. Developmental changes and injury induced disruption of the radial organization of the cortex in the immature rat brain revealed by in vivo diffusion tensor MRI. Cerebral Cortex 2007;17:2609-2617.
27. Chahboune H, Ment LR, Stewart WB, Ma X, Rothman DL, Hyder F. Neurodevelopment of C57B/L6 mouse brain assessed by in vivo diffusion tensor imaging. NMR Biomedicine 2007;20:375-382.
28. 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;33:27-38.
29. Huppi 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. Pediatric Research 1998;44:584-590.
30. Partridge SC, Mukherjee P, Henry RG, Miller SP, Berman JI, Jin H, Lu Y, Glenn OA, Ferriero DM, Barkovich AJ, et al. Diffusion tensor imaging: Serial quantitation of white matter tract maturity in premature newborns. Neuroimage 2004;22:1302-1314.
31. Drobyshevsky A, Song SK, Gamkrelidze G, Wyrwicz AM, Derrick M, Meng F, Li L, Ji X, Trommer B, Beardsley DJ, et al. Developmental changes in diffusion anisotropy coincide with immature oligodendrocyte progression and maturation of compound action potential. Journal of Neuroscience 2005;25:5988-5997.
32. Larvaron P, Boespflug-Tanguy O, Renou JP, Bonny JM. In vivo analysis of the post-natal development of normal mouse brain by DTI. NMR Biomedicine 2007;20:413-421.
33. Hermoye L, Saint-Martin C, Cosnard G, Lee SK, Kim J, Nassogne MC, Menten R, Clapuyt P, Donohue PK, Hua K, et al. Pediatric diffusion tensor imaging: Normal database and observation of the white matter maturation in early childhood. Neuroimage 2006;29:493-504.
34. Schneider JF, Il'yasov KA, Hennig J, Martin E. Fast quantitative diffusion-tensor imaging of cerebral white matter from the neonatal period to adolescence. Neuroradiology 2004;46:258-266.
35. Ben Bashat D, Ben Sira L, Graif M, Pianka P, Hendler T, Cohen Y, Assaf Y. Normal white matter development from infancy to adulthood: Comparing diffusion tensor and high b value diffusion weighted MR images. Journal of Magnetic Resonance Imaging 2005;21:503-511.
36. Eluvathingal TJ, Hasan KM, Kramer L, Fletcher JM, Ewing-Cobbs L. Quantitative diffusion tensor tractography of association and projection fibers in normally developing children and adolescents. Cerebral Cortex 2007; 17:2760-2768.
37. 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. Human Brain Mapping 2005;26:139-147.
38. Olesen PJ, Nagy Z, Westerberg H, Klingberg T. Combined analysis of DTI and fMRI data reveals a joint maturation of white and grey matter in a fronto-parietal network. Brain Research: Cognitive Brain Research 2003;18:48-57.
39. Barnea-Goraly N, Menon V, Eckert M, Tamm L, Bammer R, Karchemskiy A, Dant CC, Reiss AL. White matter development during childhood and adolescence: A cross-sectional diffusion tensor imaging study. Cerebral Cortex 2005;15:1848-1854.
40. Giorgio A, Watkins KE, Douaud G, James AC, James S, De Stefano N, Matthews PM, Smith SM, Johansen-Berg H. Changes in white matter microstructure during adolescence. Neuroimage 2008;39:52-61.
41. Muetzel RL, Collins PF, Mueller BA, A MS, Lim KO, Luciana M. The development of corpus callosum micro-structure and associations with bimanual task performance in healthy adolescents. Neuroimage 2008;39:1918-1925.
42. Snook L, Paulson LA, Roy D, Phillips L, Beaulieu C. Diffusion tensor imaging of neurodevelopment in children and young adults. Neuroimage 2005;26:1164-1173.
43. Johansen-Berg H, Della-Maggiore V, Behrens TE, Smith SM, Paus T. Integrity of white matter in the corpus callosum correlates with bimanual co-ordination skills. Neuroimage 2007;36(Suppl 2):T16-T21.
44. Paus T, Zijdenbos A, Worsley K, Collins DL, Blumenthal J, Giedd JN, Rapoport JL, Evans AC. Structural maturation of neural pathways in children and adolescents: In vivo study. Science 1999;283:1908-1911.
45. Huttenlocher PR, Dabholkar AS. Regional differences in synaptogenesis in human cerebral cortex. Journal of Computational Neurology 1997;387:167-178.
46. Cruz Junior LC, Sorensen AG. Diffusion tensor magnetic resonance imaging of brain tumors. Neurosurgical Clinics of North America 2005;16:115-134.
47. Ge Y, Law M, Grossman RI. Applications of diffusion tensor MR imaging in multiple sclerosis. Annals of the New York Academy of Sciences 2005;1064:202-219.
48. Kim MJ, Provenzale JM, Law M. Magnetic resonance and diffusion tensor imaging in pediatric white matter diseases. Topics in Magnetic Resonance Imaging 2006;17:265-274.
49. Lee SK, Kim DI, Kim J, Kim DJ, Kim HD, Kim DS, Mori S. Diffusion-tensor MR imaging and fiber tractography: A new method of describing aberrant fiber connections in developmental CNS anomalies. Radiographics 2005;25:53-65, discussion 66-68.
50. Luat AF, Chugani HT. Molecular and diffusion tensor imaging of epileptic networks. Epilepsia 2008;49(Suppl 3): 15-22.
51. Mukherjee P. Diffusion tensor imaging and fiber tractography in acute stroke. Neuroimaging Clinics of North America 2005;15:655-665, xii.
52. Sundgren PC, Dong Q, Gomez-Hassan D, Mukherji SK, Maly P, Welsh R. Diffusion tensor imaging of the brain: Review of clinical applications. Neuroradiology 2004; 46:339-350.
53. Wang S, Melhem ER. Amyotrophic lateral sclerosis and primary lateral sclerosis: The role of diffusion tensor imaging and other advanced MR-based techniques as objective upper motor neuron markers. Annals of the New York Academy of Sciences 2005;1064:61-77.
54. Copen WA, Schwamm LH, Gonzalez RG, Wu O, Harmath CB, Schaefer PW, Koroshetz WJ, Sorensen AG. Ischemic stroke: Effects of etiology and patient age on the time course of the core apparent diffusion coefficient. Radiology 2001;221:27-34.
55. Lansberg MG, Thijs VN, O'Brien MW, Ali JO, de Crespigny AJ, Tong DC, Moseley ME, Albers GW. Evolution of apparent diffusion coefficient, diffusion-weighted, and T2-weighted signal intensity of acute stroke. AJNR: American Journal of Neuroradiology 2001;22: 637-644.
56. Schlaug G, Siewert B, Benfield A, Edelman RR, Warach S. Time course of the apparent diffusion coefficient (ADC) abnormality in human stroke. Neurology 1997;49:113-119.
57. Munoz Maniega S, Bastin ME, Armitage PA, Farrall AJ, Carpenter TK, Hand PJ, Cvoro V, Rivers CS, Wardlaw JM. Temporal evolution of water diffusion parameters is different in grey and white matter in human ischaemic stroke. Journal of Neurology, Neurosurgery and Psychiatry 2004;75: 1714-1718.
58. Zelaya F, Flood N, Chalk JB, Wang D, Doddrell DM, Strugnell W, Benson M, Ostergaard L, Semple J, Eagle S. An evaluation of the time dependence of the anisotropy of the water diffusion tensor in acute human ischemia. Magnetic Resonance Imaging 1999;17:331-348.
59. Armitage PA, Bastin ME, Marshall I, Wardlaw JM, Cannon J. Diffusion anisotropy measurements in ischaemic stroke of the human brain. Magma 1998;6:28-36.
60. Yang Q, Tress BM, Barber PA, Desmond PM, Darby DG, Gerraty RP, Li T, Davis SM. Serial study of apparent diffusion coefficient and anisotropy in patients with acute stroke. Stroke 1999;30:2382-2390.
61. Sotak CH. The role of diffusion tensor imaging in the evaluation of ischemic brain injury - a review. NMR Biomedicine 2002;15:561-569.
62. Ward NS, Newton JM, Swayne OB, Lee L, Thompson AJ, Greenwood RJ, et al. Motor system activation after sub-cortical stroke depends on corticospinal system integrity. Brain 2006;129:809-819.
63. Fraidakis M, Klason T, Cheng H, Olson L, Spenger C. High-resolution MRI of intact and transected rat spinal cord. Experimental Neurology 1998;153:299-312.
64. Werring DJ, Toosy AT, Clark CA, Parker GJ, Barker GJ, Miller DH, et al. Diffusion tensor imaging can detect and quantify corticospinal tract degeneration after stroke. Journal of Neurology, Neurosurgery and Psychiatry 2000; 69:269-272.
65. Pierpaoli C, Barnett A, Pajevic S, Chen R, Penix LR, Virta A, et al. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage 2001;13:1174-1185.
66. Konishi J, Yamada K, Kizu O, Ito H, Sugimura K, Yoshikawa K, et al. MR tractography for the evaluation of functional recovery from lenticulostriate infarcts. Neurology 2005;64:108-113.
67. Kunimatsu A, Aoki S, Masutani Y, Abe O, Mori H, Ohtomo K. Three-dimensional white matter tractography by diffusion tensor imaging in ischaemic stroke involving the corticospinal tract. Neuroradiology 2003;45:532-535.
68. Liang Z, Zeng J, Liu S, Ling X, Xu A, Yu J, et al. A prospective study of secondary degeneration following subcortical infarction using diffusion tensor imaging. Journal of Neurology, Neurosurgery and Psychiatry 2007;78: 581-586.
69. Moller M, Frandsen J, Andersen G, Gjedde A, Vestergaard-Poulsen P, Ostergaard L. Dynamic changes in corticospinal tracts after stroke detected by fibretracking. Journal of Neurology, Neurosurgery and Psychiatry 2007;78: 587-592.
70. Thomalla G, Glauche V, Koch MA, Beaulieu C, Weiller C, Rother J. Diffusion tensor imaging detects early Wallerian degeneration of the pyramidal tract after ischemic stroke. Neuroimage 2004;22:1767-1774.
71. Gupta RK, Saksena S, Hasan KM, Agarwal A, Haris M, Pandey CM, et al. Focal Wallerian degeneration of the corpus callosum in large middle cerebral artery stroke: Serial diffusion tensor imaging. Journal of Magnetic Resonance Imaging 2006;24:549-555.
72. Wang C, Stebbins GT, Nyenhuis DL, deToledo-Morrell L, Freels S, Gencheva E, et al. Longitudinal changes in white matter following ischemic stroke: A three-year follow-up study. Neurobiology and Aging 2006;27: 1827-1833.
73. Stinear CM, Barber PA, Smale PR, Coxon JP, Fleming MK, Byblow WD. Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain 2007; 130:170-180.
74. Cramer SC, Nelles G, Benson RR, Kaplan JD, Parker RA, Kwong KK, et al. A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 1997; 28:2518-2527.
75. Ward NS, Newton JM, Swayne OB, Lee L, Frackowiak RS, Thompson AJ, et al. The relationship between brain activity and peak grip force is modulated by corticospinal system integrity after subcortical stroke. European Journal of Neuroscience 2007;25:1865-1873.
76. Turton A, Wroe S, Trepte N, Fraser C, Lemon RN. Contralateral and ipsilateral EMG responses to transcranial magnetic stimulation during recovery of arm and hand function after stroke. Electroencephalography Clinics on Neurophysiology 1996;101:316-328.
77. Newton JM, Ward NS, Parker GJ, Deichmann R, Alexander DC, Friston KJ, et al. Non-invasive mapping of corticofugal fibres from multiple motor areas - relevance to stroke recovery. Brain 2006;129:1844-1858.
78. Schaechter JD, Perdue KL, Wang RM. Structural damage to the corticospinal tract correlates with bilateral sensorimo-tor cortex reorganization in stroke patients. Neuroimage 2007.
79. Frost SB, Barbay S, Friel KM, Plautz EJ, Nudo RJ. Reorganization of remote cortical regions after ischemic brain injury: A potential substrate for stroke recovery. Journal of Neurophysiology 2003;89:3205-3214.
80. Johansen-Berg H, Rushworth MF, Bogdanovic MD, Kischka U, Wimalaratna S, Matthews PM. The role of ipsilateral premotor cortex in hand movement after stroke. Proceedings of the National Academy of Sciences (USA) 2002;99:14518-14523.
81. Lotze M, Markert J, Sauseng P, Hoppe J, Plewnia C, Gerloff C. The role of multiple contralesional motor areas for complex hand movements after internal capsular lesion. Journal of Neuroscience 2006;26:6096-6102.
82. Schmahmann JD, Pandya DN. Fiber pathways of the brain. 2006.
83. Behrens TE, Johansen-Berg H. Relating connectional architecture to grey matter function using diffusion imaging. Philosophical Transactions of the Royal Society of London B: Biological Science 2005;360:903-911.
84. ffytche DH, Catani M. Beyond localization: From hodology to function. Philosophical Transactions of the Royal Society of London B: Biological Science 2005;360:767-779.
85. Bammer R, Augustin M, Strasser-Fuchs S, Seifert T, Kapeller P, Stollberger R, et al. Magnetic resonance diffusion tensor imaging for characterizing diffuse and focal white matter abnormalities in multiple sclerosis. Magnetic Resonance Medicine 2000;44:583-591.
86. Filippi M, Cercignani M, Inglese M, Horsfield MA, Comi G. Diffusion tensor magnetic resonance imaging in multiple sclerosis. Neurology 2001;56:304-311.
87. 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; 52:1626-1632.
88. Filippi M, Iannucci G, Cercignani M, Assunta Rocca M, Pratesi A, Comi G. A quantitative study of water diffusion in multiple sclerosis lesions and normal-appearing white matter using echo-planar imaging. Archives of Neurology 2000; 57:1017-1021.
89. Filippi M, Inglese M. Overview of diffusion-weighted magnetic resonance studies in multiple sclerosis. Journal of Neurological Science 2001;186(Suppl. 1):S37-S43.
90. Nusbaum AO, Lu D, Tang CY, Atlas SW. Quantitative diffusion measurements in focal multiple sclerosis lesions: Correlations with appearance on TI-weighted MR images. AJR: American Journal of Roentgenology 2000;175:821-825.
91. Rovaris M, Gallo A, Valsasina P, Benedetti B, Caputo D, Ghezzi A, et al. Short-term accrual of gray matter pathology in patients with progressive multiple sclerosis: An in vivo study using diffusion tensor MRI. Neuroimage 2005; 24:1139-1146.
92. Oreja-Guevara C, Rovaris M, Iannucci G, Valsasina P, Caputo D, Cavarretta R, et al. Progressive gray matter damage in patients with relapsing-remitting multiple sclerosis: A longitudinal diffusion tensor magnetic resonance imaging study. Archives of Neurology 2005;62:578-584.
93. Ciccarelli O, Werring DJ, Wheeler-Kingshott CA, Barker GJ, Parker GJ, Thompson AJ, et al. Investigation of MS normal-appearing brain using diffusion tensor MRI with clinical correlations. Neurology 2001;56:926-933.
94. Terajima K, Matsuzawa H, Tanaka K, Nishizawa M, Nakada T. Cell-oriented analysis in vivo using diffusion tensor imaging for normal-appearing brain tissue in multiple sclerosis. Neuroimage 2007;37:1278-1285.
95. Vrenken H, Pouwels PJ, Geurts JJ, Knol DL, Polman CH, Barkhof F, et al. Altered diffusion tensor in multiple sclerosis normal-appearing brain tissue: Cortical diffusion changes seem related to clinical deterioration. Journal of Magnetic Resonance Imaging 2006;23:628-636.
96. Tortorella P, Rocca MA, Mezzapesa DM, Ghezzi A, Lamantia L, Comi G, et al. MRI quantification of gray and white matter damage in patients with early-onset multiple sclerosis. Journal of Neurology 2006;253:903-907.
97. Gallo A, Rovaris M, Riva R, Ghezzi A, Benedetti B, Martinelli V, et al. Diffusion-tensor magnetic resonance imaging detects normal-appearing white matter damage unrelated to short-term disease activity in patients at the earliest clinical stage of multiple sclerosis. Archives of Neurology 2005;62:803-808.
98. Griffin CM, Chard DT, Ciccarelli O, Kapoor B, Barker GJ, Thompson AI, et al. Diffusion tensor imaging in early relapsing-remitting multiple sclerosis. Multiple Sclerosis 2001;7:290-297.
99. Henry RG, Oh J, Nelson SJ, Pelletier D. Directional diffusion in relapsing-remitting multiple sclerosis: A possible in vivo signature of Wallerian degeneration. Journal of Magnetic Resonance Imaging 2003;18:420-426.
100. Ge Y, Law M, Johnson G, Herbert J, Babb JS, Mannon LJ, et al. Preferential occult injury of corpus callosum in multiple sclerosis measured by diffusion tensor imaging. Journal of Magnetic Resonance Imaging 2004;20:1-7.
101. Lin X, Tench CR, Morgan PS, Constantinescu CS. Use of combined conventional and quantitative MRI to quantify pathology related to cognitive impairment in multiple sclerosis. Journal of Neurology, Neurosurgery and Psychiatry 2008;79:437-441.
102. Lin X, Tench CR, Morgan PS, Niepel G, Constantinescu CS. 'Importance sampling' in MS: Use of diffusion tensor tractography to quantify pathology related to specific impairment. Journal of Neurological Science 2005;237:13-19.
103. Warlop NP, Achten E, Debruyne J, Vingerhoets G. Diffusion weighted callosal integrity reflects interhemi-spheric communication efficiency in multiple sclerosis. Neuropsychologia 2008;46:2258-2264.
104. Hasan KM, Gupta RK, Santos RM, Wolinsky JS, Narayana PA. Diffusion tensor fractional anisotropy of the normal-appearing seven segments of the corpus callosum in healthy adults and relapsing-remitting multiple sclerosis patients. Journal of Magnetic Resonance Imaging 2005;21:735-743.
105. Lenzi D, Conte A, Mainero C, Frasca V, Fubelli F, Totaro P, et al. Effect of corpus callosum damage on ipsilateral motor activation in patients with multiple sclerosis: A functional and anatomical study. Human Brain Mapping 2007;28:636-644.
106. Lin F, Yu C, Jiang T, Li K, Chan P. Diffusion tensor tractography-based group mapping of the pyramidal tract in relapsing-remitting multiple sclerosis patients. AJNR: American Journal of Neuroradiology 2007; 28:278-282.
107. Wilson M, Tench CR, Morgan PS, Blumhardt LD. Pyramidal tract mapping by diffusion tensor magnetic resonance imaging in multiple sclerosis: Improving correlations with disability. Journal of Neurology, Neurosurgery and Psychiatry 2003;74:203-207.
108. Ciccarelli O, Werring DJ, Barker GJ, Griffin CM, Wheeler-Kingshott CA, Miller DH, et al. A study of the mechanisms of normal-appearing white matter damage in multiple sclerosis using diffusion tensor imaging - evidence of Wallerian degeneration. Journal of Neurology 2003; 250:287-292.
109. Mezzapesa DM, Rocca MA, Falini A, Rodegher ME, Ghezzi A, Comi G, et al. A preliminary diffusion tensor and magnetization transfer magnetic resonance imaging study of early-onset multiple sclerosis. Archives of Neurology 2004;61:366-368.
110. Rocca MA, Iannucci G, Rovaris M, Comi G, Filippi M. Occult tissue damage in patients with primary progressive multiple sclerosis is independent of T2-visible lesions - a diffusion tensor MR study. Journal of Neurology 2003; 250:456-460.
111. Saindane AM, Law M, Ge Y, Johnson G, Babb JS, Grossman RI. Correlation of diffusion tensor and dynamic perfusion MR imaging metrics in normal-appearing corpus callosum: Support for primary hypoperfusion in multiple sclerosis. AJNR: American Journal of Neuroradiology 2007;28:767-772.
112. Caramia F, Pantano P, Di Legge S, Piattella MC, Lenzi D, Paolillo A, et al. A longitudinal study of MR diffusion changes in normal appearing white matter of patients with early multiple sclerosis. Magnetic Resonance Imaging 2002;20:383-388.
113. Schmierer K, Altmann DR, Kassim N, Kitzler H, Kerskens CM, Doege CA, et al. Progressive change in primary progressive multiple sclerosis normal-appearing white matter: A serial diffusion magnetic resonance imaging study. Multiple Sclerosis 2004;10:182-187.
114. Rashid W, Hadjiprocopis A, Davies G, Griffin C, Chard D, Tiberio M, et al. Longitudinal evaluation of clinically early relapsing-remitting multiple sclerosis with diffusion tensor imaging. Journal of Neurology 2008;255: 390-397.
115. Rovaris M, Judica E, Gallo A, Benedetti B, Sormani MP, Caputo D, et al. Grey matter damage predicts the evolution of primary progressive multiple sclerosis at 5 years. Brain 2006;129:2628-2634.
116. Rocca MA, Cercignani M, Iannucci G, Comi G, Filippi M. Weekly diffusion-weighted imaging of normal-appearing white matter in MS. Neurology 2000;55:882-884.
117. Werring DJ, Brassat D, Droogan AG, Clark CA, Symms MR, Barker GJ, et al. The pathogenesis of lesions and normal-appearing white matter changes in multiple sclerosis: A serial diffusion MRI study. Brain 2000; 123(Pt 8):1667-1676.
118. Cader S, Johansen-Berg H, Wylezinska M, Palace J, Behrens TE, Smith S, et al. Discordant white matter N-acetylasparate and diffusion MRI measures suggest that chronic metabolic dysfunction contributes to axonal pathology in multiple sclerosis. Neuroimage 2007;36:19-27.
119. Bozzali M, Cercignani M, Sormani MP, Comi G, Filippi M. Quantification of brain gray matter damage in different MS phenotypes by use of diffusion tensor MR imaging. AJNR: American Journal of Neuroradiology 2002;23:985-988.
120. Lowe MJ, Beall EB, Sakaie KE, Koenig KA, Stone L, Marrie RA, et al. Resting state sensorimotor functional connectivity in multiple sclerosis inversely correlates with transcallosal motor pathway transverse diffusivity. Human Brain Mapping 2008;29:818-827.
121. Simon JH, Zhang S, Laidlaw DH, Miller DE, Brown M, Corboy J, et al. Identification of fibers at risk for degeneration by diffusion tractography in patients at high risk for MS after a clinically isolated syndrome. Journal of Magnetic Resonance Imaging 2006;24:983-988.
122. Pagani E, Filippi M, Rocca MA, Horsfield MA. A method for obtaining tract-specific diffusion tensor MRI measurements in the presence of disease: Application to patients with clinically isolated syndromes suggestive of multiple sclerosis. Neuroimage 2005;26:258-265.
123. Rocca MA, Pagani E, Absinta M, Valsasina P, Falini A, Scotti G, Comi G, Filippi M. Altered functional and structural connectivities in patients with MS: A 3-T study. Neurology 2007;69:2136-2145.
124. Audoin B, Guye M, Reuter F, Au Duong MV, Confort-Gouny S, Malikova I, Soulier E, Viout P, Cherif AA, Cozzone PJ, et al. Structure of WM bundles constituting the working memory system in early multiple sclerosis: A quantitative DTI tractogra-phy study. Neuroimage 2007;36:1324-1330.
125. Rocca MA, Valsasina P, Ceccarelli A, Absinta M, Ghezzi A, Riccitelli G, Pagani E, Falini A, Comi G, Scotti G, et al. Structural and functional MRI correlates of Stroop control in benign MS. Human Brain Mapping 2007.
126. Huisman TA, Schwamm LH, Schaefer PW, Koroshetz WJ, Shetty-Alva N, Ozsunar Y, Wu O, Sorensen AG. Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. AJNR: American Journal of Neuroradiology 2004;25:370-376.
127. Ahn YH, Kim SH, Han BS, Kim OL, Ahn SH, Cho YW, Kwon YH, Jang SH. Focal lesions of the corticospinal tract demonstrated by diffusion tensor imaging in patients with diffuse axonal injury. Neuro Rehabilitation 2006; 21:239-243.
128. Xu J, Rasmussen IA, Lagopoulos J, Haberg A. Diffuse axonal injury in severe traumatic brain injury visualized using high-resolution diffusion tensor imaging. Journal of Neurotrauma 2007;24:753-765.
129. Sidaros A, Engberg AW, Sidaros K, Liptrot MG, Herning M, Petersen P, Paulson OB, Jernigan TL, Rostrup E. Diffusion tensor imaging during recovery from severe traumatic brain injury and relation to clinical outcome: A longitudinal study. Brain 2008;131: 559-572.
130. Staudt M, Pavlova M, Bohm S, Grodd W, Krageloh-Mann I. Pyramidal tract damage correlates with motor dysfunction in bilateral periventricular leukomalacia (PVL). Neuropediatrics 2003;34:182-188.
131. Hoon AH Jr, Lawrie WT Jr, Melhem ER, Reinhardt EM, Van Zijl PC, Solaiyappan M, Jiang H, Johnston MV, Mori S. Diffusion tensor imaging of periventricular leukomalacia shows affected sensory cortex white matter pathways. Neurology 2002;59:752-756.
132. Nagae LM, Hoon AH Jr, Stashinko E, Lin D, Zhang W, Levey E, Wakana S, Jiang H, Leite CC, Lucato LT, et al. Diffusion tensor imaging in children with periventricular leukomalacia: Variability of injuries to white matter tracts. AJNR: American Journal of Neuroradiology 2007;28:1213-1222.
133. Thomas B, Eyssen M, Peeters R, Molenaers G, Van Hecke P, De Cock P, Sunaert S. Quantitative diffusion tensor imaging in cerebral palsy due to periventricular white matter injury. Brain 2005;128:2562-2577.
134. Provenzale JM, Escolar M, Kurtzberg J. Quantitative analysis of diffusion tensor imaging data in serial assessment of Krabbe disease. Annals of the New York Academy of Sciences 2005;1064:220-229.
135. Suzuki K. Globoid cell leukodystrophy (Krabbe's disease): update. Journal of Child Neurology 2003;18: 595-603.
136. Krivit W, Shapiro EG, Peters C, Wagner JE, Cornu G, Kurtzberg J, Wenger DA, Kolodny EH, Vanier MT, Loes DJ, et al. Hematopoietic stem-cell transplantation in globoid-cell leukodystrophy. New England Journal of Medicine 1998;338:1119-1126.