Diffusion Tensor Imaging in Huntington's disease reveals distinct patterns of white matter degeneration associated with motor and cognitive deficits

Brain Imaging and Behavior

Volumn 5, Issue 3, 2011, Pages 171-180

  Bohanna, India ^a,b   Georgiou Karistianis, Nellie ^c   Sritharan, Anusha ^c   Asadi, Hamed ^a,b   Johnston, Leigh ^a,b   Churchyard, Andrew ^d   Egan, Gary ^a,b  

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

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d MONASH MEDICAL CENTRE   (Australia)

Author keywords

Corpus callosum; Diffusion tensor imaging; Huntington's disease; Tract based spatial statistics; White matter

Indexed keywords

ADULT; ARTICLE; BRAIN SIZE; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CORPUS CALLOSUM; DEGENERATIVE DISEASE; DIFFUSION TENSOR IMAGING; DISEASE ASSOCIATION; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; HUNTINGTON CHOREA; IMAGE ANALYSIS; MALE; MEAN DIFFUSIVITY; MOTOR DYSFUNCTION; PARALLEL DIFFUSIVITY; PERPENDICULAR DIFFUSIVITY; PRIORITY JOURNAL; RADIOLOGICAL PARAMETERS; TRACTOGRAPHY; WHITE MATTER DEGENERATION;

ADULT; ANISOTROPY; BRAIN; COGNITION DISORDERS; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; DISEASE PROGRESSION; FEMALE; HUMANS; HUNTINGTON DISEASE; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MIDDLE AGED; MODELS, STATISTICAL; MOVEMENT; NERVE DEGENERATION; NEUROPSYCHOLOGICAL TESTS;

EID: 79961026808     PISSN: 19317557     EISSN: 19317565     Source Type: Journal    
DOI: 10.1007/s11682-011-9121-8     Document Type: Article

References (54)

1. Aylward, E. H., Anderson, N. B., Bylsma, F. W., Wagster, M. V., Barta, P. E., Sherr, M., et al. (1998). Frontal lobe volume in patients with Huntington's disease. Neurology, 50(1), 252-8.
2. Bartzokis, G., & Tishler, T. A. (2000). MRI evaluation of basal ganglia ferritin iron and neurotoxicity in Alzheimer's and Huntingon's disease. Cellular and Molecular Biology (Noisy-le-grand), 46(4), 821-833.
3. Bartzokis, G., Cummings, J., Perlman, S., Hance, D. B., & Mintz, J. (1999). Increased basal ganglia iron levels in Huntington disease. Archives of Neurology, 56(5), 569-74.
4. Bartzokis, G., Lu, P. H., Tishler, T. A., Fong, S. M., Oluwadara, B., Finn, J. P., et al. (2007). Myelin breakdown and iron changes in Huntington's disease: pathogenesis and treatment implications. Neurochemical Research, 32(10), 1655-64.
5. Basser, P. J., & Pierpaoli, C. (1996). Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. Journal of Magnetic Resonance. Series B, 111(3), 209-19.
6. Beck, A. T., Ward, C. H., Mendelson, M., Mock, J., & Erbaugh, J. (1961). An inventory for measuring depression. Archives of General Psychiatry, 4, 561-71.
7. Beglinger, L. J., Nopoulos, P. C., Jorge, R. E., Langbehn, D. R., Mikos, A. E., Moser, D. J., et al. (2005). White matter volume and cognitive dysfunction in early Huntington's disease. Cognitive and Behavioral Neurology, 18(2), 102-7.
8. Behrens, T. E. J., Johansen-Berg, H., Woolrich, M. W., Smith, S. M., Wheeler-Kingshott, C. A. M., Boulby, P. A., et al. (2003). Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nature Neuroscience, 6(7), 750-7.
9. Blatter, D., Bigler, E., Gale, S., Johnson, S., Anderson, C., Burnett, B., et al. (1995). Quantitative volumetric analysis of brain MR: normative database spanning 5 decades of life. American Journal of Neuroradiology, 16(2), 241.
10. Bohanna, I., Georgiou-Karistianis, N., Hannan, A. J., & Egan, G. F. (2008). Magnetic resonance imaging as an approach towards identifying neuropathological biomarkers for Huntington's disease. Brain Research Reviews, 58(1), 209-25.
11. Ciarmiello, A., Cannella, M., Lastoria, S., Simonelli, M., Frati, L., Rubinsztein, D. C., et al. (2006). Brain White-Matter Volume Loss and Glucose Hypometabolism Precede the Clinical Symptoms of Huntington's Disease, Journal of Nuclear Medicine (Vol. 47, pp. 215-222): Soc Nuclear Med.
12. Concha, L., Gross, D. W., Wheatley, B. M., & Beaulieu, C. (2006). Diffusion tensor imaging of time-dependent axonal and myelin degradation after corpus callosotomy in epilepsy patients. Neuroimage, 32(3), 1090-9.
13. de la Monte, S. M., Vonsattel, J. P., & Richardson, E. P., Jr. (1988). Morphometric demonstration of atrophic changes in the cerebral cortex, white matter, and neostriatum in Huntington's disease. Journal of Neuropathology and Experimental Neurology, 47(5), 516-25.
14. Fennema-Notestine, C., Archibald, S. L., Jacobson, M. W., Corey-Bloom, J., Paulsen, J. S., Peavy, G. M., et al. (2004). In vivo evidence of cerebellar atrophy and cerebral white matter loss in Huntington disease. Neurology, 63(6), 989-95.
15. Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189-98.
16. Folstein, M. F., Robins, L. N., & Helzer, J. E. (1983). The mini-mental state examination. Archives of General Psychiatry, 40(7), 812.
17. Glenn, O. A., Henry, R. G., Berman, J. I., Chang, P. C., Miller, S. P., Vigneron, D. B., et al. (2003). DTI-based three-dimensional tractography detects differences in the pyramidal tracts of infants and children with congenital hemiparesis. Journal of Magnetic Resonance Imaging, 18(6), 641-8.
18. Group, H. S. (1996). Unified Huntington's disease rating scale: reliability and consistency. Huntington study group. Movement Disorders, 11(2), 136-42.
19. Halliday, G. M., McRitchie, D. A., Macdonald, V., Double, K. L., Trent, R. J., & McCusker, E. (1998). Regional specificity of brain atrophy in Huntington's disease. Experimental Neurology, 154(2), 663-72.
20. Jech, R., Klempir, J., Vymazal, J., Zidovska, J., Klempirova, O., Ruzicka, E., et al. (2007). Variation of selective gray and white matter atrophy in Huntington's disease. Movement Disorders, 22(12), 1783-9.
21. Johansen-Berg, H., Della-Maggiore, V., Behrens, T. E. J., Smith, S. M., & Paus, T. (2007). Integrity of white matter in the corpus callosum correlates with bimanual co-ordination skills. Neuroimage, 36, 16-21.
22. Kassubek, J., Bernhard Landwehrmeyer, G., Ecker, D., Juengling, F., Muche, R., Schuller, S., et al. (2004). Global cerebral atrophy in early stages of Huntington's disease: quantitative MRI study. NeuroReport, 15(2), 363.
23. Kloppel, S., Draganski, B., Golding, C. V., Chu, C., Nagy, Z., Cook, P. A., et al. (2008). White matter connections reflect changes in voluntary-guided saccades in pre-symptomatic Huntington's disease. Brain, 131(Pt 1), 196-204.
24. Lee, W. C. M., Yoshihara, M., & Littleton, J. T. (2004). Cytoplasmic aggregates trap polyglutamine-containing proteins and block axonal transport in a Drosophila model of Huntington's disease. Proceedings of the National Academy of Science, 101(9), 3224-9.
25. Li, H., Li, S. H., Cheng, A. L., Mangiarini, L., Bates, G. P., & Li, X. J. (1999). Ultrastructural localization and progressive formation of neuropil aggregates in Huntington's disease transgenic mice. Human Molecular Genetics, 8(7), 1227-36.
26. Li, H., Li, S. H., Yu, Z. X., Shelbourne, P., & Li, X. J. (2001). Huntingtin aggregate-associated axonal degeneration is an early pathological event in Huntington's disease mice. The Journal of Neuroscience, 21(21), 8473.
27. Mann, D. M., Oliver, R., & Snowden, J. S. (1993). The topographic distribution of brain atrophy in Huntington's disease and progressive supranuclear palsy. Acta Neuropathologica, 85(5), 553-9.
28. Mascalchi, M., Lolli, F., Della Nave, R., Tessa, C., Petralli, R., Gavazzi, C., et al. (2004). Huntington disease: volumetric, diffusion-weighted, and magnetization transfer MR imaging of brain. Radiology, 232(3), 867-73.
29. Mori, S., & Wakana, S. (2005). MRI atlas of human white matter.
30. Nelson, H. E., & Willison, J. (1982). National adult reading test (NART): Test manual. Windsor: Nfer-Nelson.
31. Nichols, T. E., & Holmes, A. P. (2002). Nonparametric permutation tests for functional neuroimaging: a primer with examples. Human Brain Mapping, 15(1), 1-25.
32. Ota, M., Sato, N., Ohya, Y., Aoki, Y., Mizukami, K., Mori, T., et al. (2006). Relationship between diffusion tensor imaging and brain morphology in patients with myotonic dystrophy. Neuroscience Letters, 407(3), 234-9.
33. Paulsen, J. S., Magnotta, V. A., Mikos, A. E., Paulson, H. L., Penziner, E., Andreasen, N. C., et al. (2006). Brain structure in preclinical Huntington's disease. Biological Psychiatry, 59(1), 57-63.
34. Paulsen, J. S., Langbehn, D. R., Stout, J. C., Aylward, E., Ross, C. A., Nance, M., et al. (2008). Detection of Huntington's disease decades before diagnosis: the Predict-HD study. Journal of Neurology, Neurosurgery and Psychiatry, 79(8), 874-80.
35. Pierpaoli, C., Barnett, A., Pajevic, S., Chen, R., Penix, L. R., Virta, A., et al. (2001). Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage, 13(6 Pt 1), 1174-85.
36. Reading, S. A., Yassa, M. A., Bakker, A., Dziorny, A. C., Gourley, L. M., Yallapragada, V., et al. (2005). Regional white matter change in pre-symptomatic Huntington's disease: a diffusion tensor imaging study. Psychiatry Research, 140(1), 55-62.
37. Rosas, H. D., Koroshetz, W. J., Chen, Y. I., Skeuse, C., Vangel, M., Cudkowicz, M. E., et al. (2003). Evidence for more widespread cerebral pathology in early HD: an MRI-based morphometric analysis. Neurology, 60(10), 1615-20.
38. Rosas, H. D., Hevelone, N. D., Zaleta, A. K., Greve, D. N., Salat, D. H., & Fischl, B. (2005). Regional cortical thinning in preclinical Huntington disease and its relationship to cognition. Neurology, 65(5), 745-7.
39. Rosas, H. D., Tuch, D. S., Hevelone, N. D., Zaleta, A. K., Vangel, M., Hersch, S. M., et al. (2006). Diffusion tensor imaging in presymptomatic and early Huntington's disease: Selective white matter pathology and its relationship to clinical measures. Movement Disorders, 21(9), 1317-25.
40. Rosas, H. D., Salat, D. H., Lee, S. Y., Zaleta, A. K., Pappu, V., Fischl, B., et al. (2008). Cerebral cortex and the clinical expression of Huntington's disease: complexity and heterogeneity. Brain, 131(Pt 4), 1057-68.
41. Rosas, H. D., Lee, S. Y., Bender, A. C., Zaleta, A. K., Vangel, M., Yu, P., et al. (2009). Altered white matter microstructure in the corpus callosum in Huntington's disease: implications for cortical "disconnection". Neuroimage, 49(4), 2995-3004.
42. Sapp, E., Penney, J., Young, A., Aronin, N., Vonsattel, J. P., & DiFiglia, M. (1999). Axonal transport of N-terminal huntingtin suggests early pathology of corticostriatal projections in Huntington disease. Journal of Neuropathology and Experimental Neurology, 58(2), 165-73.
43. Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., et al. (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage, 31(4), 1487-505.
44. Song, S. K., Sun, S. W., Ju, W. K., Lin, S. J., Cross, A. H., & Neufeld, A. H. (2003). Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage, 20(3), 1714-22.
45. Stoffers, D., Sheldon, S., Kuperman, J. M., Goldstein, J., Corey-Bloom, J., & Aron, A. R. (2010). Contrasting gray and white matter changes in preclinical Huntington disease: an MRI study. Neurology, 74(15), 1208-16.
46. Sullivan, E. V., Rohlfing, T., & Pfefferbaum, A. (2008). Quantitative fiber tracking of lateral and interhemispheric white matter systems in normal aging: relations to timed performance. Neurobiology of Aging.
47. Sun, S. W., Liang, H. F., Le, T. Q., Armstrong, R. C., Cross, A. H., & Song, S. K. (2006). Differential sensitivity of in vivo and ex vivo diffusion tensor imaging to evolving optic nerve injury in mice with retinal ischemia. Neuroimage, 32(3), 1195-204.
48. Sydykova, D., Stahl, R., Dietrich, O., Ewers, M., Reiser, M. F., Schoenberg, S. O., et al. (2007). Fiber connections between the cerebral cortex and the corpus callosum in Alzheimer's disease: a diffusion tensor imaging and voxel-based morphometry study. Cerebral Cortex, 17(10), 2276.
49. Tabrizi, S. J., Langbehn, D. R., Leavitt, B. R., Roos, R. A., Durr, A., Craufurd, D., et al. (2009). Biological and clinical manifestations of Huntington's disease in the longitudinal TRACK-HD study: cross-sectional analysis of baseline data. Lancet Neurol.
50. Tai, Y. F., Pavese, N., Gerhard, A., Tabrizi, S. J., Barker, R. A., Brooks, D. J., et al. (2007a). Imaging microglial activation in Huntington's disease. Brain Research Bulletin, 72(2-3), 148-51.
51. Tai, Y. F., Pavese, N., Gerhard, A., Tabrizi, S. J., Barker, R. A., Brooks, D. J., et al. (2007b). Microglial activation in presymptomatic Huntington's disease gene carriers. Brain, 130(7), 1759.
52. Thieben, M. J., Duggins, A. J., Good, C. D., Gomes, L., Mahant, N., Richards, F., et al. (2002). The distribution of structural neuropathology in pre-clinical Huntington's disease. Brain, 125(8), 1815.
53. Wade, A., Jacobs, P., & Morton, A. J. (2008). Atrophy and degeneration in sciatic nerve of presymptomatic mice carrying the Huntington's disease mutation. Brain Research, 1188, 61-8.
54. Weaver, K. E., Richards, T. L., Liang, O., Laurino, M. Y., Samii, A., & Aylward, E. H. (2009). Longitudinal diffusion tensor imaging in Huntington's Disease. Experimental Neurology, 216(2), 525-9.