Neurobiology of Aging
Volume 33, Issue 5 , Pages 945-959 , May 2012

A complementary diffusion tensor imaging (DTI)-histological study in a model of Huntington's disease

  • Nadja Van Camp

      Affiliations

    • Bio-Imaging Laboratory, University of Antwerp (CGB), Groenenborgerlaan 171, 2610 Wilrijk (Antwerp), Belgium
    • ,
  • Ines Blockx

      Affiliations

    • Bio-Imaging Laboratory, University of Antwerp (CGB), Groenenborgerlaan 171, 2610 Wilrijk (Antwerp), Belgium
    • ,
  • Lluïsa Camón

      Affiliations

    • Institute for Biomedical Research (IIBB-CSIC), IDIBAPS, Rossello 161, 08036 Barcelona, Spain
    • ,
  • Nuria de Vera

      Affiliations

    • Institute for Biomedical Research (IIBB-CSIC), IDIBAPS, Rossello 161, 08036 Barcelona, Spain
    • ,
  • Marleen Verhoye

      Affiliations

    • Bio-Imaging Laboratory, University of Antwerp (CGB), Groenenborgerlaan 171, 2610 Wilrijk (Antwerp), Belgium
    • ,
  • Jelle Veraart

      Affiliations

    • Visionlab (Department of Physics), University of Antwerp (CDE), Universiteitsplein 1, Antwerp, Belgium
    • ,
  • Wim Van Hecke

      Affiliations

    • Visionlab (Department of Physics), University of Antwerp (CDE), Universiteitsplein 1, Antwerp, Belgium
    • ,
  • Emili Martínez

      Affiliations

    • Institute for Biomedical Research (IIBB-CSIC), IDIBAPS, Rossello 161, 08036 Barcelona, Spain
    • ,
  • Guadalupe Soria

      Affiliations

    • Institute for Biomedical Research (IIBB-CSIC), IDIBAPS, Rossello 161, 08036 Barcelona, Spain
    • ,
  • Jan Sijbers

      Affiliations

    • Visionlab (Department of Physics), University of Antwerp (CDE), Universiteitsplein 1, Antwerp, Belgium
    • ,
  • Anna M. Planas

      Affiliations

    • Institute for Biomedical Research (IIBB-CSIC), IDIBAPS, Rossello 161, 08036 Barcelona, Spain
    • ,
  • Annemie Van der Linden

      Affiliations

    • Bio-Imaging Laboratory, University of Antwerp (CGB), Groenenborgerlaan 171, 2610 Wilrijk (Antwerp), Belgium
    • Corresponding Author InformationCorresponding author. Tel: +32 (0)3 265 32 30; fax: +32 (0)3 265 32 33

Received 11 December 2009 ,Revised 30 June 2010 ,Accepted 3 July 2010.

References 

  1. Acosta-Cabronero J , Williams GB , Pengas G , Nestor PJ . Absolute diffusivities define the landscape of white matter degeneration in Alzheimer's disease . Brain . 2010;133:529–539
  2. Aguilera P, Chanez-Cardenas ME, Floriano-Sanchez E, Barrera D, Santamaria A, Sanchez-Gonzalez DJ, et al. Time-related changes in constitutive and inducible nitric oxide synthases in the rat striatum in a model of Huntington's disease . Neurotoxicology . 2007;28:1200–1207
  3. Alexander AL , Lee JE , Lazar M , Field AS . Diffusion tensor imaging of the brain . Neurotherapeutics . 2007;4:316–329
  4. Araujo DM , Cherry SR , Tatsukawa KJ , Toyokuni T , Kornblum HI . Deficits in striatal dopamine D(2) receptors and energy metabolism detected by in vivo microPET imaging in a rat model of Huntington's disease . Exp. Neurol. . 2000;166:287–297
  5. Basser PJ , Mattiello J , LeBihan D . Estimation of the effective self-diffusion tensor from the NMR spin echo . J. Magn. Reson. B . 1994;103:247–254
  6. Beal MF , Ferrante RJ , Swartz KJ , Kowall NW . Chronic quinolinic acid lesions in rats closely resemble Huntington disease . J. Neurosci. . 1991;11:1649–1659
  7. Bohanna I , Georgiou-Karistianis N , Hannan AJ , Egan GF . Magnetic resonance imaging as an approach towards identifying neuropathological biomarkers for Huntington disease . Brain Res. Rev. . 2008;58:209–225
  8. Brouillet E , Conde F , Beal MF , Hantraye P . Replicating Huntington disease phenotype in experimental animals . Prog. Neurobiol. . 1999;59:427–468
  9. Budde MD , Xie M , Cross AH , Song SK . Axial diffusivity is the primary correlate of axonal injury in the experimental autoimmune encephalomyelitis spinal cord: a quantitative pixelwise analysis . J. Neurosci. . 2009;29:2805–2813
  10. D'Agostino E , Maes F , Vandermeulen D , Suetens P . A viscous fluid model for multimodal non-rigid image registration using mutual information . Med. Image Anal. . 2003;7:565–575
  11. 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;46:958–966
  12. Estrada Sanchez AM , Mejia-Toiber J , Massieu L . Excitotoxic neuronal death and the pathogenesis of Huntington's disease . Arch. Med. Res. . 2008;39:265–276
  13. Fennema-Notestine C, Archibald SL, Jacobson MW, Corey-Bloom J, Paulsen JS, Peavy GM, et al. In vivo evidence of cerebellar atrophy and cerebral white matter loss in Huntington disease . Neurology . 2004;63:989–995
  14. Ferrante RJ , Kowall NW , Cipolloni PB , Storey E , Beal MF . Excitotoxin lesions in primates as a model for Huntington disease: histopathologic and neurochemical characterization . Exp. Neurol. . 1993;119:46–71
  15. Gimenez-Llort L , de VN , Martinez E . Analysis of chemically induced alterations of the motor activity in rats . Neurotoxicology . 1998;19:371–379
  16. Gimenez-Llort L , Ferre S , Martinez E . Effects of the systemic administration of kainic acid and NMDA on exploratory activity in rats . Pharmacol. Biochem. Behav. . 1995;51:205–210
  17. Kim JH, Budde MD, Liang HF, Klein RS, Russell JH, Cross AH, et al. Detecting axon damage in spinal cord from a mouse model of multiple sclerosis . Neurobiol. Dis. . 2006;21:626–632
  18. Kloppel S, Draganski B, Golding CV, Chu C, Nagy Z, Cook PA, et al. White matter connections reflect changes in voluntary-guided saccades in pre-symptomatic Huntington disease . Brain . 2008;131:196–204
  19. Maes F , Collignon A , Vandermeulen D , Marchal G , Suetens P . Multimodality image registration by maximization of mutual information . IEEE Trans. Med. Imaging . 1997;16:187–198
  20. Marrannes R , Wauquier A . Episodic barrel rotations induced by intrastriatal injection of quinolinic acid in rats (Inhibition by anticonvulsants) . Pharmacol. Biochem. Behav. . 1988;31:153–162
  21. Moresco RM, Lavazza T, Belloli S, Lecchi M, Pezzola A, Todde S, et al. Quinolinic acid induced neurodegeneration in the striatum: a combined in vivo and in vitro analysis of receptor changes and microglia activation . Eur. J. Nucl. Med. Mol. Imaging . 2008;35:704–715
  22. Nicholson LF , Faull RL , Waldvogel HJ , Dragunow M . GABA and GABAA receptor changes in the substantia nigra of the rat following quinolinic acid lesions in the striatum closely resemble Huntington disease . Neuroscience . 1995;66:507–521
  23. Paxinos G , Watson C . The rat brain in stereotaxic coordinates . 4td ed.. Elsevier; 2006;
  24. Roberts RC , Ahn A , Swartz KJ , Beal MF , DiFiglia M . Intrastriatal Injections of Quinolinic Acid or Kainic Acid: Differential Patterns of Cell Survival and the Effects of Data Analysis on Outcome . Exp. Neurol. . 1993;124:274–282
  25. Rosas HD, Tuch DS, Hevelone ND, Zaleta AK, Vangel M, Hersch SM, et al. Diffusion tensor imaging in presymptomatic and early Huntington disease: Selective white matter pathology and its relationship to clinical measures . Mov. Disord. . 2006;21:1317–1325
  26. Rosas HD, Lee SY, Bender AC, Zaleta AK, Vangel M, Yu P, et al. Altered white matter microstructure in the corpus callosum in Huntington's disease: Implications for cortical “disconnection” . Neuroimage . 2010;49:2995–3004
  27. Salat DH, Tuch DS, van der Kouwe AJW, Greve DN, Pappu V, Lee SY, et al. White matter pathology isolates the hippocampal formation in Alzheimer's disease . Neurobiol. Aging . 2010;31:244–256
  28. Sapp E, Kegel KB, Aronin N, Hashikawa T, Uchiyama Y, Tohyama K, et al. Early and progressive accumulation of reactive microglia in the Huntington disease brain . J. Neuropathol. Exp. Neurol. . 2001;60:161–172
  29. Scattoni ML , Valanzano A , Popoli P , Pezzola A , Reggio R , Calamandrei G . Progressive behavioural changes in the spatial open-field in the quinolinic acid rat model of Huntington's disease . Behav. Brain Res. . 2004;152:375–383
  30. Schwarcz R , Foster AC , French ED , Whetsell WO , Kohler C . Excitotoxic models for neurodegenerative disorders . Life Sci. . 1984;35:19–32
  31. Schwarcz R , Guidetti P , Sathyasaikumar KV , Muchowski PJ . Of mice, rats and men: Revisiting the quinolinic acid hypothesis of Huntington's disease . Prog. Neurobiol. . 2009;90:230–245
  32. Shear DA , Dong J , Gundy CD , Haik-Creguer KL , Dunbar GL . Comparison of intrastriatal injections of quinolinic acid and 3-nitropropionic acid for use in animal models of Huntington's disease . Prog. Neuropsychopharmacol. Biol. Psychiatry . 1998;22:1217–1240
  33. Song SK , Kim JH , Lin SJ , Brendza RP , Holtzman DM . Diffusion tensor imaging detects age-dependent white matter changes in a transgenic mouse model with amyloid deposition . Neurobiol. Dis. . 2004;15:640–647
  34. 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
  35. Stoffers D , Sheldon S , Kuperman JM , Goldstein J , Corey-Bloom J , Aron AR . Contrasting gray and white matter changes in preclinical Huntington disease: an MRI study . Neurology . 2010;74:1208–1216
  36. Sun SW , Liang HF , Trinkaus K , Cross AH , Armstrong RC , Song SK . Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum . Magn. Reson. Med. . 2006;55:302–308
  37. Sun SW, Song SK, Harms MP, Lin SJ, Holtzman DM, Merchant KM, et al. Detection of age-dependent brain injury in a mouse model of brain amyloidosis associated with Alzheimer's disease using magnetic resonance diffusion tensor imaging . Exp. Neurol. . 2005;191:77–85
  38. Tai YF, Pavese N, Gerhard A, Tabrizi SJ, Barker RA, Brooks DJ, et al. Imaging microglial activation in Huntington's disease . Brain Res. Bull. . 2007;72:148–151
  39. Tai YF, Pavese N, Gerhard A, Tabrizi SJ, Barker RA, Brooks DJ, et al. Microglial activation in presymptomatic Huntington disease gene carriers . Brain . 2007;130:1759–1766
  40. The Huntington's Disease Collaborative Research Group . A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington disease chromosomes . Cell . 1993;72:971–983
  41. Thieben MJ, Duggins AJ, Good CD, Gomes L, Mahant N, Richards F, et al. The distribution of structural neuropathology in pre-clinical Huntington disease . Brain . 2002;125:1815–1828
  42. Underwood BR, Broadhurst D, Dunn WB, Ellis DI, Michell AW, Vacher C, et al. Huntington disease patients and transgenic mice have similar pro-catabolic serum metabolite profiles . Brain . 2006;129:877–886
  43. Van Camp N, Blockx I, Verhoye M, Casteels C, Coun F, Leemans A, et al. Diffusion Tensor Imaging in a Rat Model of Parkinson's Disease After Lesioning of the Nigrostriatal Tract . NMR Biomed. . 2009;22:697–706
  44. Van Hecke W, Leemans A, D'Agostino E, De Backer S, Vandervliet E, Parizel PM, et al. Nonrigid coregistration of diffusion tensor images using a viscous fluid model and mutual information . IEEE Trans. Med. Imaging . 2007;26:1598–1612
  45. Van Hecke W , Sijbers J , De Backer S , Poot D , Parizel PM , Leemans A . On the construction of a ground truth framework for evaluating voxel-based diffusion tensor MRI analysis methods . Neuroimage . 2009;46:692–707
  46. Vivo M , Camon L , de VN , Martinez E . Lesion of substantia nigra pars compacta by the GluR5 agonist ATPA . Brain Res. . 2002;955:104–114
  47. Vonsattel JP , DiFiglia M . Huntington disease . J. Neuropathol. Exp. Neurol. . 1998;57:369–384
  48. Vymazal J, Klempir J, Jech R, Zidovska J, Syka M, Ruzicka E, et al. MR relaxometry in Huntington's disease: correlation between imaging, genetic and clinical parameters . J. Neurol. Sci. . 2007;263:20–25
  49. Weaver KE , Richards TL , Liang O , Laurino MY , Samii A , Aylward EH . Longitudinal diffusion tensor imaging in Huntington's Disease . Exp. Neurol. . 2009;216:525–529
  50. Xu J , Sun SW , Naismith RT , Snyder AZ , Cross AH , Song SK . Assessing optic nerve pathology with diffusion MRI: from mouse to human . NMR Biomed. . 2008;21:928–940

PII: S0197-4580(10)00308-8

doi: 10.1016/j.neurobiolaging.2010.07.001

Neurobiology of Aging
Volume 33, Issue 5 , Pages 945-959 , May 2012

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