Journal of Neurology

, Volume 262, Issue 10, pp 2257–2270 | Cite as

Structural hallmarks of amyotrophic lateral sclerosis progression revealed by probabilistic fiber tractography

  • Robert Steinbach
  • Kristian Loewe
  • Joern Kaufmann
  • Judith Machts
  • Katja Kollewe
  • Susanne Petri
  • Reinhard Dengler
  • Hans-Jochen Heinze
  • Stefan Vielhaber
  • Mircea Ariel Schoenfeld
  • Christian Michael Stoppel
Original Communication

Abstract

Amyotrophic lateral sclerosis (ALS) is a neurodegenerative disease characterized by progressive limb and/or bulbar muscular weakness and atrophy. Although ALS-related alterations of motor and extra-motor neuronal networks have repeatedly been reported, their temporal dynamics during disease progression are not well understood. Recently, we reported a decline of motor system activity and a concurrent increase of hippocampal novelty-evoked modulations across 3 months of ALS progression. To address whether these functional changes are associated with structural ones, the current study employed probabilistic fiber tractography on diffusion tensor imaging (DTI) data using a longitudinal design. Therein, motor network integrity was assessed by DTI-based tracking of the intracranial corticospinal tract, while connectivity estimates of occipito-temporal tracts (between visual and entorhinal, perirhinal or parahippocampal cortices) served to assess structural changes that could be related to the increased novelty-evoked hippocampal activity across time described previously. Complementing these previous functional observations, the current data revealed an ALS-related decrease in corticospinal tract structural connectivity compared to controls, while in contrast, visuo-perirhinal connectivity was relatively increased in the patient group. Importantly, beyond these between-group differences, a rise in the patients’ occipito-temporal tract strengths occurred across a 3-month interval, while at the same time no changes in corticospinal tract connectivity were observed. In line with previously identified functional alterations, the dynamics of these structural changes suggest that the affection of motor- and memory-related networks in ALS emerges at distinct disease stages: while motor network degeneration starts primarily during early (supposedly pre-symptomatic) phases, the hippocampal/medial temporal lobe dysfunctions arise at later stages of the disease.

Keywords

Amyotrophic lateral sclerosis Corticospinal tract Medial temporal lobe Longitudinal DTI Probabilistic fiber tractography 

Notes

Acknowledgments

This work was supported by the Deutsche Forschungsgemeinschaft (Scho 1217/1-2 and SFB 779 - A1 to M.A.S.).

Conflicts of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Hardiman O, van den Berg LH, Kiernan MC (2011) Clinical diagnosis and management of amyotrophic lateral sclerosis. Nature Rev Neurol 7(11):639–649. doi:10.1038/nrneurol.2011.153 CrossRefGoogle Scholar
  2. 2.
    Agosta F, Chio A, Cosottini M, De Stefano N, Falini A, Mascalchi M, Rocca MA, Silani V, Tedeschi G, Filippi M (2010) The present and the future of neuroimaging in amyotrophic lateral sclerosis. AJNR Am J Neuroradiol 31(10):1769–1777. doi:10.3174/ajnr.A2043 CrossRefPubMedGoogle Scholar
  3. 3.
    Menke RA, Korner S, Filippini N, Douaud G, Knight S, Talbot K, Turner MR (2014) Widespread grey matter pathology dominates the longitudinal cerebral MRI and clinical landscape of amyotrophic lateral sclerosis. Brain J Neurol 137(Pt 9):2546–2555. doi:10.1093/brain/awu162 CrossRefGoogle Scholar
  4. 4.
    Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuck T, Grossman M, Clark CM, McCluskey LF, Miller BL, Masliah E, Mackenzie IR, Feldman H, Feiden W, Kretzschmar HA, Trojanowski JQ, Lee VM (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314(5796):130–133. doi:10.1126/science.1134108 CrossRefPubMedGoogle Scholar
  5. 5.
    Takeda T, Uchihara T, Arai N, Mizutani T, Iwata M (2009) Progression of hippocampal degeneration in amyotrophic lateral sclerosis with or without memory impairment: distinction from Alzheimer disease. Acta Neuropathol 117(1):35–44. doi:10.1007/s00401-008-0447-2 CrossRefPubMedGoogle Scholar
  6. 6.
    van der Graaff MM, Sage CA, Caan MW, Akkerman EM, Lavini C, Majoie CB, Nederveen AJ, Zwinderman AH, Vos F, Brugman F, van den Berg LH, de Rijk MC, van Doorn PA, Van Hecke W, Peeters RR, Robberecht W, Sunaert S, de Visser M (2011) Upper and extra-motoneuron involvement in early motoneuron disease: a diffusion tensor imaging study. Brain J Neurol 134(Pt 4):1211–1228. doi:10.1093/brain/awr016 CrossRefGoogle Scholar
  7. 7.
    Wightman G, Anderson VE, Martin J, Swash M, Anderton BH, Neary D, Mann D, Luthert P, Leigh PN (1992) Hippocampal and neocortical ubiquitin-immunoreactive inclusions in amyotrophic lateral sclerosis with dementia. Neurosci Lett 139(2):269–274CrossRefPubMedGoogle Scholar
  8. 8.
    Lomen-Hoerth C, Anderson T, Miller B (2002) The overlap of amyotrophic lateral sclerosis and frontotemporal dementia. Neurology 59(7):1077–1079CrossRefPubMedGoogle Scholar
  9. 9.
    Rademakers R, Neumann M, Mackenzie IR (2012) Advances in understanding the molecular basis of frontotemporal dementia. Nature Rev Neurol 8(8):423–434. doi:10.1038/nrneurol.2012.117 Google Scholar
  10. 10.
    Tsermentseli S, Leigh PN, Goldstein LH (2012) The anatomy of cognitive impairment in amyotrophic lateral sclerosis: more than frontal lobe dysfunction. Cortex 48(2):166–182. doi:10.1016/j.cortex.2011.02.004 CrossRefPubMedGoogle Scholar
  11. 11.
    Hammer A, Vielhaber S, Rodriguez-Fornells A, Mohammadi B, Munte TF (2011) A neurophysiological analysis of working memory in amyotrophic lateral sclerosis. Brain Res 1421:90–99. doi:10.1016/j.brainres.2011.09.010 CrossRefPubMedGoogle Scholar
  12. 12.
    Mantovan MC, Baggio L, Dalla Barba G, Smith P, Pegoraro E, Soraru G, Bonometto P, Angelini C (2003) Memory deficits and retrieval processes in ALS. Eur J Neurol 10(3):221–227. doi:607iiGoogle Scholar
  13. 13.
    Phukan J, Elamin M, Bede P, Jordan N, Gallagher L, Byrne S, Lynch C, Pender N, Hardiman O (2012) The syndrome of cognitive impairment in amyotrophic lateral sclerosis: a population-based study. J Neurol Neurosurg Psychiatry 83(1):102–108. doi:10.1136/jnnp-2011-300188 CrossRefPubMedGoogle Scholar
  14. 14.
    Raaphorst J, de Visser M, Linssen WH, de Haan RJ, Schmand B (2010) The cognitive profile of amyotrophic lateral sclerosis: a meta-analysis. Amyotroph Lateral Scler 11(1–2):27–37. doi:10.3109/17482960802645008 CrossRefPubMedGoogle Scholar
  15. 15.
    Anderson VE, Cairns NJ, Leigh PN (1995) Involvement of the amygdala, dentate and hippocampus in motor neuron disease. J Neurol Sci 129(Suppl):75–78. doi:0022510X9500069EGoogle Scholar
  16. 16.
    Takeda T, Uchihara T, Mochizuki Y, Mizutani T, Iwata M (2007) Memory deficits in amyotrophic lateral sclerosis patients with dementia and degeneration of the perforant pathway A clinicopathological study. J Neurol Sci 260(1–2):225–230. doi:10.1016/j.jns.2007.05.010 CrossRefPubMedGoogle Scholar
  17. 17.
    Stoppel CM, Vielhaber S, Eckart C, Machts J, Kaufmann J, Heinze HJ, Kollewe K, Petri S, Dengler R, Hopf JM, Schoenfeld MA (2014) Structural and functional hallmarks of amyotrophic lateral sclerosis progression in motor- and memory-related brain regions. NeuroImage Clin 5:277–290. doi:10.1016/j.nicl.2014.07.007 PubMedCentralCrossRefPubMedGoogle Scholar
  18. 18.
    Bookheimer SY, Strojwas MH, Cohen MS, Saunders AM, Pericak-Vance MA, Mazziotta JC, Small GW (2000) Patterns of brain activation in people at risk for Alzheimer’s disease. N Engl J Med 343(7):450–456. doi:10.1056/NEJM200008173430701 PubMedCentralCrossRefPubMedGoogle Scholar
  19. 19.
    Dickerson BC, Sperling RA (2008) Functional abnormalities of the medial temporal lobe memory system in mild cognitive impairment and Alzheimer’s disease: insights from functional MRI studies. Neuropsychologia 46(6):1624–1635. doi:10.1016/j.neuropsychologia.2007.11.030 PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    Woodard JL, Seidenberg M, Nielson KA, Antuono P, Guidotti L, Durgerian S, Zhang Q, Lancaster M, Hantke N, Butts A, Rao SM (2009) Semantic memory activation in amnestic mild cognitive impairment. Brain 132(Pt 8):2068–2078. doi:10.1093/brain/awp157 PubMedCentralCrossRefPubMedGoogle Scholar
  21. 21.
    Bakker A, Krauss GL, Albert MS, Speck CL, Jones LR, Stark CE, Yassa MA, Bassett SS, Shelton AL, Gallagher M (2012) Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron 74(3):467–474. doi:10.1016/j.neuron.2012.03.023 PubMedCentralCrossRefPubMedGoogle Scholar
  22. 22.
    Lavenex P, Amaral DG (2000) Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10(4):420–430. doi:10.1002/1098-1063(2000)10:4<420:AID-HIPO8>3.0.CO;2-5 CrossRefPubMedGoogle Scholar
  23. 23.
    Powell HW, Guye M, Parker GJ, Symms MR, Boulby P, Koepp MJ, Barker GJ, Duncan JS (2004) Noninvasive in vivo demonstration of the connections of the human parahippocampal gyrus. NeuroImage 22(2):740–747. doi:10.1016/j.neuroimage.2004.01.011 CrossRefPubMedGoogle Scholar
  24. 24.
    Squire LR (1992) Declarative and nondeclarative memory: multiple brain systems supporting learning and memory. J Cogn Neurosci 4(3):232–243. doi:10.1162/jocn.1992.4.3.232 CrossRefPubMedGoogle Scholar
  25. 25.
    Brooks BR, Miller RG, Swash M, Munsat TL, World Federation of Neurology Research Group on Motor Neuron D (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1(5):293–299CrossRefPubMedGoogle Scholar
  26. 26.
    Cedarbaum JM, Stambler N, Malta E, Fuller C, Hilt D, Thurmond B, Nakanishi A (1999) The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci 169(1–2):13–21. doi:S0022510X99002105Google Scholar
  27. 27.
    Neary D, Snowden JS, Gustafson L, Passant U, Stuss D, Black S, Freedman M, Kertesz A, Robert PH, Albert M, Boone K, Miller BL, Cummings J, Benson DF (1998) Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 51(6):1546–1554CrossRefPubMedGoogle Scholar
  28. 28.
    Machts J, Bittner V, Kasper E, Schuster C, Prudlo J, Abdulla S, Kollewe K, Petri S, Dengler R, Heinze HJ, Vielhaber S, Schoenfeld MA, Bittner DM (2014) Memory deficits in amyotrophic lateral sclerosis are not exclusively caused by executive dysfunction: a comparative neuropsychological study of amnestic mild cognitive impairment. BMC Neurosci 15:83. doi:10.1186/1471-2202-15-83 PubMedCentralCrossRefPubMedGoogle Scholar
  29. 29.
    Reese TG, Heid O, Weisskoff RM, Wedeen VJ (2003) Reduction of eddy-current-induced distortion in diffusion MRI using a twice-refocused spin echo. Magnetic Reson Med 49(1):177–182. doi:10.1002/mrm.10308 CrossRefGoogle Scholar
  30. 30.
    Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM (2012) Fsl. NeuroImage 62(2):782–790. doi:10.1016/j.neuroimage.2011.09.015 CrossRefPubMedGoogle Scholar
  31. 31.
    Geyer S, Ledberg A, Schleicher A, Kinomura S, Schormann T, Burgel U, Klingberg T, Larsson J, Zilles K, Roland PE (1996) Two different areas within the primary motor cortex of man. Nature 382(6594):805–807. doi:10.1038/382805a0 CrossRefPubMedGoogle Scholar
  32. 32.
    Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 25(4):1325–1335. doi:10.1016/j.neuroimage.2004.12.034 CrossRefPubMedGoogle Scholar
  33. 33.
    Amunts K, Malikovic A, Mohlberg H, Schormann T, Zilles K (2000) Brodmann’s areas 17 and 18 brought into stereotaxic space-where and how variable? NeuroImage 11(1):66–84. doi:10.1006/nimg.1999.0516 CrossRefPubMedGoogle Scholar
  34. 34.
    Pruessner JC, Kohler S, Crane J, Pruessner M, Lord C, Byrne A, Kabani N, Collins DL, Evans AC (2002) Volumetry of temporopolar, perirhinal, entorhinal and parahippocampal cortex from high-resolution MR images: considering the variability of the collateral sulcus. Cereb Cortex 12(12):1342–1353CrossRefPubMedGoogle Scholar
  35. 35.
    Bodammer NC, Kaufmann J, Kanowski M, Tempelmann C (2009) Monte Carlo-based diffusion tensor tractography with a geometrically corrected voxel-centre connecting method. Phys Med Biol 54(4):1009–1033. doi:10.1088/0031-9155/54/4/013 CrossRefPubMedGoogle Scholar
  36. 36.
    Agosta F, Gorno-Tempini ML, Pagani E, Sala S, Caputo D, Perini M, Bartolomei I, Fruguglietti ME, Filippi M (2009) Longitudinal assessment of grey matter contraction in amyotrophic lateral sclerosis: a tensor based morphometry study. Amyotroph Lateral Scler 10(3):168–174. doi:10.1080/17482960802603841 CrossRefPubMedGoogle Scholar
  37. 37.
    Foerster BR, Welsh RC, Feldman EL (2013) 25 years of neuroimaging in amyotrophic lateral sclerosis. Nature Rev Neurol 9(9):513–524. doi:10.1038/nrneurol.2013.153 CrossRefGoogle Scholar
  38. 38.
    Aggarwal A, Nicholson G (2002) Detection of preclinical motor neurone loss in SOD1 mutation carriers using motor unit number estimation. J Neurol Neurosurg Psychiatry 73(2):199–201PubMedCentralCrossRefPubMedGoogle Scholar
  39. 39.
    de Carvalho M, Swash M (2006) The onset of amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 77(3):388–389. doi:10.1136/jnnp.2005.073031 PubMedCentralCrossRefPubMedGoogle Scholar
  40. 40.
    Ng MC, Ho JT, Ho SL, Lee R, Li G, Cheng TS, Song YQ, Ho PW, Fong GC, Mak W, Chan KH, Li LS, Luk KD, Hu Y, Ramsden DB, Leong LL (2008) Abnormal diffusion tensor in nonsymptomatic familial amyotrophic lateral sclerosis with a causative superoxide dismutase 1 mutation. J Magn Reson Imaging 27(1):8–13. doi:10.1002/jmri.21217 CrossRefPubMedGoogle Scholar
  41. 41.
    Kew JJ, Leigh PN, Playford ED, Passingham RE, Goldstein LH, Frackowiak RS, Brooks DJ (1993) Cortical function in amyotrophic lateral sclerosis. A positron emission tomography study. Brain 116(Pt 3):655–680CrossRefPubMedGoogle Scholar
  42. 42.
    Kollewe K, Munte TF, Samii A, Dengler R, Petri S, Mohammadi B (2011) Patterns of cortical activity differ in ALS patients with limb and/or bulbar involvement depending on motor tasks. J Neurol 258(5):804–810. doi:10.1007/s00415-010-5842-7 CrossRefPubMedGoogle Scholar
  43. 43.
    Schoenfeld MA, Tempelmann C, Gaul C, Kuhnel GR, Duzel E, Hopf JM, Feistner H, Zierz S, Heinze HJ, Vielhaber S (2005) Functional motor compensation in amyotrophic lateral sclerosis. J Neurol 252(8):944–952. doi:10.1007/s00415-005-0787-y CrossRefPubMedGoogle Scholar
  44. 44.
    Mohammadi B, Kollewe K, Samii A, Dengler R, Munte TF (2011) Functional neuroimaging at different disease stages reveals distinct phases of neuroplastic changes in amyotrophic lateral sclerosis. Hum Brain Mapp 32(5):750–758. doi:10.1002/hbm.21064 CrossRefPubMedGoogle Scholar
  45. 45.
    Blain CR, Williams VC, Johnston C, Stanton BR, Ganesalingam J, Jarosz JM, Jones DK, Barker GJ, Williams SC, Leigh NP, Simmons A (2007) A longitudinal study of diffusion tensor MRI in ALS. Amyotroph Lateral Scler 8(6):348–355. doi:10.1080/17482960701548139 CrossRefPubMedGoogle Scholar
  46. 46.
    Kwan JY, Meoded A, Danielian LE, Wu T, Floeter MK (2012) Structural imaging differences and longitudinal changes in primary lateral sclerosis and amyotrophic lateral sclerosis. NeuroImage Clin 2:151–160. doi:10.1016/j.nicl.2012.12.003 PubMedCentralCrossRefPubMedGoogle Scholar
  47. 47.
    Menke RA, Abraham I, Thiel CS, Filippini N, Knight S, Talbot K, Turner MR (2012) Fractional anisotropy in the posterior limb of the internal capsule and prognosis in amyotrophic lateral sclerosis. Arch Neurol 69(11):1493–1499. doi:10.1001/archneurol.2012.1122 CrossRefPubMedGoogle Scholar
  48. 48.
    Mitsumoto H, Ulug AM, Pullman SL, Gooch CL, Chan S, Tang MX, Mao X, Hays AP, Floyd AG, Battista V, Montes J, Hayes S, Dashnaw S, Kaufmann P, Gordon PH, Hirsch J, Levin B, Rowland LP, Shungu DC (2007) Quantitative objective markers for upper and lower motor neuron dysfunction in ALS. Neurology 68(17):1402–1410. doi:10.1212/01.wnl.0000260065.57832.87 CrossRefPubMedGoogle Scholar
  49. 49.
    Keil C, Prell T, Peschel T, Hartung V, Dengler R, Grosskreutz J (2012) Longitudinal diffusion tensor imaging in amyotrophic lateral sclerosis. BMC Neurosci 13:141. doi:10.1186/1471-2202-13-141 PubMedCentralCrossRefPubMedGoogle Scholar
  50. 50.
    Zhang Y, Schuff N, Woolley SC, Chiang GC, Boreta L, Laxamana J, Katz JS, Weiner MW (2011) Progression of white matter degeneration in amyotrophic lateral sclerosis: a diffusion tensor imaging study. Amyotroph Lateral Scler 12(6):421–429. doi:10.3109/17482968.2011.593036 PubMedCentralCrossRefPubMedGoogle Scholar
  51. 51.
    Bhagat YA, Hussain MS, Stobbe RW, Butcher KS, Emery DJ, Shuaib A, Siddiqui MM, Maheshwari P, Al-Hussain F, Beaulieu C (2008) Elevations of diffusion anisotropy are associated with hyper-acute stroke: a serial imaging study. Magn Reson Imaging 26(5):683–693. doi:10.1016/j.mri.2008.01.015 CrossRefPubMedGoogle Scholar
  52. 52.
    Herve D, Molko N, Pappata S, Buffon F, LeBihan D, Bousser MG, Chabriat H (2005) Longitudinal thalamic diffusion changes after middle cerebral artery infarcts. J Neurol Neurosurg Psychiatry 76(2):200–205. doi:10.1136/jnnp.2004.041012 PubMedCentralCrossRefPubMedGoogle Scholar
  53. 53.
    Yang Q, Tress BM, Barber PA, Desmond PM, Darby DG, Gerraty RP, Li T, Davis SM (1999) Serial study of apparent diffusion coefficient and anisotropy in patients with acute stroke. Stroke 30(11):2382–2390CrossRefPubMedGoogle Scholar
  54. 54.
    Green HA, Pena A, Price CJ, Warburton EA, Pickard JD, Carpenter TA, Gillard JH (2002) Increased anisotropy in acute stroke: a possible explanation. Stroke 33(6):1517–1521CrossRefPubMedGoogle Scholar
  55. 55.
    Mayer AR, Ling J, Mannell MV, Gasparovic C, Phillips JP, Doezema D, Reichard R, Yeo RA (2010) A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology 74(8):643–650. doi:10.1212/WNL.0b013e3181d0ccdd PubMedCentralCrossRefPubMedGoogle Scholar
  56. 56.
    Nael K, Trouard TP, Lafleur SR, Krupinski EA, Salamon N, Kidwell CS (2015) White matter ischemic changes in hyperacute ischemic stroke: voxel-based analysis using diffusion tensor imaging and MR perfusion. Stroke 46(2):413–418. doi:10.1161/STROKEAHA.114.007000 PubMedCentralCrossRefPubMedGoogle Scholar
  57. 57.
    Zelaya F, Flood N, Chalk JB, Wang D, Doddrell DM, Strugnell W, Benson M, Ostergaard L, Semple J, Eagle S (1999) An evaluation of the time dependence of the anisotropy of the water diffusion tensor in acute human ischemia. Magn Reson Imaging 17(3):331–348CrossRefPubMedGoogle Scholar
  58. 58.
    Alexander AL, Lee JE, Lazar M, Field AS (2007) Diffusion tensor imaging of the brain. Neurotherapeutics 4(3):316–329. doi:10.1016/j.nurt.2007.05.011 PubMedCentralCrossRefPubMedGoogle Scholar
  59. 59.
    Carano RA, Li F, Irie K, Helmer KG, Silva MD, Fisher M, Sotak CH (2000) Multispectral analysis of the temporal evolution of cerebral ischemia in the rat brain. J Magn Reson Imaging 12(6):842–858CrossRefPubMedGoogle Scholar
  60. 60.
    Liu Y, D’Arceuil HE, Westmoreland S, He J, Duggan M, Gonzalez RG, Pryor J, de Crespigny AJ (2007) Serial diffusion tensor MRI after transient and permanent cerebral ischemia in nonhuman primates. Stroke 38(1):138–145. doi:10.1161/01.STR.0000252127.07428.9c CrossRefPubMedGoogle Scholar
  61. 61.
    Sotak CH (2002) The role of diffusion tensor imaging in the evaluation of ischemic brain injury—a review. NMR Biomed 15(7–8):561–569. doi:10.1002/nbm.786 CrossRefPubMedGoogle Scholar
  62. 62.
    Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15(7–8):435–455. doi:10.1002/nbm.782 CrossRefPubMedGoogle Scholar
  63. 63.
    Sen PN, Basser PJ (2005) A model for diffusion in white matter in the brain. Biophys J 89(5):2927–2938. doi:10.1529/biophysj.105.063016 PubMedCentralCrossRefPubMedGoogle Scholar
  64. 64.
    Stanisz G, Henkelman RM (2001) Effects of cellular swelling on diffusion in white matter. In: Proceedings of the 9th ISMRM, Glasgow, Scotland, p 350Google Scholar
  65. 65.
    Peled S (2007) New perspectives on the sources of white matter DTI signal. IEEE Trans Med Imaging 26(11):1448–1455PubMedCentralCrossRefPubMedGoogle Scholar
  66. 66.
    Douaud G, Jbabdi S, Behrens TE, Menke RA, Gass A, Monsch AU, Rao A, Whitcher B, Kindlmann G, Matthews PM, Smith S (2011) DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer’s disease. NeuroImage 55(3):880–890. doi:10.1016/j.neuroimage.2010.12.008 CrossRefPubMedGoogle Scholar
  67. 67.
    Pierpaoli C, Barnett A, Pajevic S, Chen R, Penix LR, Virta A, Basser P (2001) Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. NeuroImage 13(6 Pt 1):1174–1185. doi:10.1006/nimg.2001.0765 CrossRefPubMedGoogle Scholar
  68. 68.
    Teipel S, Ehlers I, Erbe A, Holzmann C, Lau E, Hauenstein K, Berger C (2014) Structural connectivity changes underlying altered working memory networks in mild cognitive impairment: a three-way image fusion analysis. J Neuroimaging. doi:10.1111/jon.12178 PubMedGoogle Scholar
  69. 69.
    Adluru N, Destiche DJ, Lu SY, Doran ST, Birdsill AC, Melah KE, Okonkwo OC, Alexander AL, Dowling NM, Johnson SC, Sager MA, Bendlin BB (2014) White matter microstructure in late middle-age: effects of apolipoprotein E4 and parental family history of Alzheimer’s disease. NeuroImage Clin 4:730–742. doi:10.1016/j.nicl.2014.04.008 PubMedCentralCrossRefPubMedGoogle Scholar
  70. 70.
    Racine AM, Adluru N, Alexander AL, Christian BT, Okonkwo OC, Oh J, Cleary CA, Birdsill A, Hillmer AT, Murali D, Barnhart TE, Gallagher CL, Carlsson CM, Rowley HA, Dowling NM, Asthana S, Sager MA, Bendlin BB, Johnson SC (2014) Associations between white matter microstructure and amyloid burden in preclinical Alzheimer’s disease: a multimodal imaging investigation. NeuroImage Clin 4:604–614. doi:10.1016/j.nicl.2014.02.001 PubMedCentralCrossRefPubMedGoogle Scholar
  71. 71.
    Ryan NS, Keihaninejad S, Shakespeare TJ, Lehmann M, Crutch SJ, Malone IB, Thornton JS, Mancini L, Hyare H, Yousry T, Ridgway GR, Zhang H, Modat M, Alexander DC, Rossor MN, Ourselin S, Fox NC (2013) Magnetic resonance imaging evidence for presymptomatic change in thalamus and caudate in familial Alzheimer’s disease. Brain 136(Pt 5):1399–1414. doi:10.1093/brain/awt065 PubMedCentralCrossRefPubMedGoogle Scholar
  72. 72.
    Hasan KM, Halphen C, Boska MD, Narayana PA (2008) Diffusion tensor metrics, T2 relaxation, and volumetry of the naturally aging human caudate nuclei in healthy young and middle-aged adults: possible implications for the neurobiology of human brain aging and disease. Magn Reson Med 59(1):7–13. doi:10.1002/mrm.21434 CrossRefPubMedGoogle Scholar
  73. 73.
    Takenobu Y, Hayashi T, Moriwaki H, Nagatsuka K, Naritomi H, Fukuyama H (2014) Motor recovery and microstructural change in rubro-spinal tract in subcortical stroke. NeuroImage Clin 4:201–208. doi:10.1016/j.nicl.2013.12.003 PubMedCentralCrossRefPubMedGoogle Scholar
  74. 74.
    Hope T, Westlye LT, Bjornerud A (2012) The effect of gradient sampling schemes on diffusion metrics derived from probabilistic analysis and tract-based spatial statistics. Magn Reson Imaging 30(3):402–412. doi:10.1016/j.mri.2011.11.003 CrossRefPubMedGoogle Scholar
  75. 75.
    Tensaouti F, Lahlou I, Clarisse P, Lotterie JA, Berry I (2011) Quantitative and reproducibility study of four tractography algorithms used in clinical routine. J Magn Reson Imaging 34(1):165–172. doi:10.1002/jmri.22584 CrossRefPubMedGoogle Scholar
  76. 76.
    Unrath A, Muller HP, Riecker A, Ludolph AC, Sperfeld AD, Kassubek J (2010) Whole brain-based analysis of regional white matter tract alterations in rare motor neuron diseases by diffusion tensor imaging. Hum Brain Mapp 31(11):1727–1740. doi:10.1002/hbm.20971 PubMedGoogle Scholar
  77. 77.
    Tuch DS, Reese TG, Wiegell MR, Makris N, Belliveau JW, Wedeen VJ (2002) High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity. Magn Reson Med 48(4):577–582. doi:10.1002/mrm.10268 CrossRefPubMedGoogle Scholar
  78. 78.
    Zhang H, Schneider T, Wheeler-Kingshott CA, Alexander DC (2012) NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. NeuroImage 61(4):1000–1016. doi:10.1016/j.neuroimage.2012.03.072 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Robert Steinbach
    • 1
  • Kristian Loewe
    • 1
    • 2
  • Joern Kaufmann
    • 1
  • Judith Machts
    • 1
  • Katja Kollewe
    • 3
  • Susanne Petri
    • 3
  • Reinhard Dengler
    • 3
  • Hans-Jochen Heinze
    • 1
    • 4
  • Stefan Vielhaber
    • 1
  • Mircea Ariel Schoenfeld
    • 1
    • 4
    • 5
  • Christian Michael Stoppel
    • 1
    • 4
    • 6
  1. 1.Department of NeurologyOtto-von-Guericke-UniversityMagdeburgGermany
  2. 2.Department of Knowledge and Language ProcessingOtto-von-Guericke-UniversityMagdeburgGermany
  3. 3.Department of Neurology, Medical School HannoverHannoverGermany
  4. 4.Leibniz-Institute for NeurobiologyMagdeburgGermany
  5. 5.Kliniken SchmiederAllensbachGermany
  6. 6.Department of Psychiatry and PsychotherapyCharité-Universitätsmedizin BerlinBerlinGermany

Personalised recommendations