Structural and functional MRI abnormalities of cerebellar cortex and nuclei in SCA3, SCA6 and Friedreich's ataxia

Brain

Volumn 138, Issue 5, 2015, Pages 1182-1197

  Stefanescu, Maria R ^a,b   Dohnalek, Moritz ^a   Maderwald, Stefan ^b   Thürling, Markus ^a,b   Minnerop, Martina ^c,d   Beck, Andreas ^e   Schlamann, Marc ^b   Diedrichsen, Joern ^f   Ladd, Mark E ^b,g   Timmann, Dagmar ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

^d UNIVERSITY OF BONN   (Germany)

^e HEINRICH HEINE UNIVERSITY   (Germany)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

^g UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Cerebellar atrophy; Dentate nuclei; Functional magnetic resonance imaging; Hereditary ataxia; Spinocerebellar degeneration; Structural magnetic resonance imaging

Indexed keywords

ATAXIN 3; PROTEIN; SPINOCEREBELLAR ATAXIA TYPE 6 PROTEIN; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; ASSOCIATION; BRAIN ATROPHY; BRAIN CORTEX; BRAIN FUNCTION; BRAIN SIZE; CAG REPEAT; CEREBELLUM CORTEX; CEREBELLUM NUCLEUS; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; DENTATE NUCLEUS; ECHO PLANAR IMAGING; FEMALE; FRIEDREICH ATAXIA; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HAND MOVEMENT; HUMAN; INFERIOR FRONTAL GYRUS; MALE; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; SUSCEPTIBILITY WEIGHTED IMAGING; TRINUCLEOTIDE REPEAT; ATROPHY; MACHADO JOSEPH DISEASE; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PROCEDURES; SPINOCEREBELLAR DEGENERATION;

ADULT; AGED; ATROPHY; CEREBELLAR CORTEX; CEREBELLAR NUCLEI; FEMALE; FRIEDREICH ATAXIA; HUMANS; MACHADO-JOSEPH DISEASE; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; SPINOCEREBELLAR ATAXIAS; SPINOCEREBELLAR DEGENERATIONS;

EID: 84929658363     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awv064     Document Type: Article

References (72)

1. Akhlaghi H, Corben L, Georgiou-Karistianis N, Bradshaw J, Delatycki MB, Storey E, et al. A functional MRI study of motor dysfunction in Friedreich's ataxia. Brain Res 2012; 1471: 138-54.
2. Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage 2007; 38: 95-113.
3. Ashburner J. Computational anatomy with the SPM software. Magn Reson Imaging 2009; 27: 1163-74.
4. Binkofski F, Buccino G. Motor functions of the Broca's region. Brain Lang 2004; 89: 362-9.
5. Boddaert N, Le Quan Sang KH, Rö tig A, Leroy-Willig A, Gallet S, Brunelle F, et al. Selective iron chelation in Friedreich ataxia: biologic and clinical implications. Blood 2007; 110: 401-8.
6. Bonilha da Silva C, Bergo FP, D'Abreu A, Cendes F, Lopes-Cendes I, França MC Jr. Dentate nuclei T2 relaxometry is a reliable neuroimaging marker in Friedreich's ataxia. Eur J Neurol 2014; 21: 1131-6.
7. Brandauer B, Hermsdö rfer J, Beck A, Aurich V, Gizewski ER, Marquardt C, et al. Impairments of prehension kinematics and grasping forces in patients with cerebellar degeneration and the relationship to cerebellar atrophy. Clin Neurophysiol 2008; 119: 2528-37.
8. Bürk K, Abele M, Fetter M, Dichgans J, Skalej M, Laccone F, et al. Autosomal dominant cerebellar ataxia type I clinical features and MRI in families with SCA1, SCA2 and SCA3. Brain 1996; 119: 1497-505.
9. Deistung A, Schäfer A, Schweser F, Biedermann U, Turner R, Reichenbach JR. Toward in vivo histology: A comparison of quantitative susceptibility mapping (QSM) with magnitude-, phase-, and R2-imaging at ultra-high magnetic field strength. Neuroimage 2013; 65: 299-314.
10. Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. Neuroimage 2006; 33: 127-38.
11. Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N. A probabilistic MR atlas of the human cerebellum. Neuroimage 2009; 46: 39-46.
12. Diedrichsen J, Maderwald S, Küper M, Thürling M, Rabe K, Gizewski ER, et al. Imaging the deep cerebellar nuclei: A probabilistic atlas and normalization procedure. Neuroimage 2011; 54: 1786-94.
13. Du AX, Cuzzocreo JL, Landman BA, Zee DS, Prince JL, Ying SH. Diffusion tensor imaging reveals disease-specific deep cerebellar nuclear changes in cerebellar degeneration. J Neurol 2010; 257: 1406-8.
14. Dürr A, Stevanin G, Cancel G, Duyckaerts C, Abbas N, Didierjean O, et al. Spinocerebellar ataxia 3 and Machado-Joseph disease: clinical, molecular, and neuropathological features. Ann Neurol 1996; 39: 490-9.
15. Dürr A. Autosomal dominant cerebellar ataxias: polyglutamine expansions and beyond. Lancet Neurol 2010; 9: 885-94.
16. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 2005; 25: 1325-35.
17. Evers MM, Toonen LJ, van Roon-Mom WM. Ataxin-3 protein and RNA toxicity in spinocerebellar ataxia type 3: current insights and emerging therapeutic strategies. Mol Neurobiol 2014; 49: 1513-31.
18. Friston KJ, Frith CD, Turner R, Frackowiak RS. Characterizing evoked hemodynamics with fMRI. Neuroimage 1995; 2: 157-65.
19. Gasparotti R, Pinelli L, Liserre R. New MR sequences in daily practice: susceptibility weighted imaging. A pictorial essay. Insights Imaging 2011; 2: 335-47.
20. Geyer S, Ledberg A, Schleicher A, Kinomura S, Schormann T, Bürgel U, et al. Two different areas within the primary motor cortex of man. Nature 1996; 382: 805-7.
21. Gierga K, Schelhaas HJ, Brunt ER, Seidel K, Scherzed W, Egensperger R, et al. Spinocerebellar ataxia type 6 (SCA6): neurodegeneration goes beyond the known brain predilection sites. Neuropathol Appl Neurobiol 2009; 35: 515-27.
22. Ginestroni A, Diciotti S, Cecchi P, Pesaresi I, Tessa C, Giannelli M, et al. Neurodegeneration in Friedreich's ataxia is associated with a mixed activation pattern of the brain. A fMRI study. Hum Brain Mapp 2012; 33: 1780-91.
23. Glickstein M, Doron K. Cerebellum: connections and functions. Cerebellum 2008; 7: 589-94.
24. Glover GH, Li TQ, Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn Reson Med 2000; 44: 162-7.
25. Grodd W, Hülsmann E, Lotze M, Wildgruber D, Erb M. Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization. Hum Brain Mapp 2001; 13: 55-73.
26. Habas C. Functional imaging of the deep cerebellar nuclei: A review. Cerebellum 2010; 9: 22-8.
27. Hashimoto M, Takahara D, Hirata Y, Inoue K, Miyachi S, Nambu A, Tanji J, Takada M, Hoshi E. Motor and non-motor projections from the cerebellum to rostrocaudally distinct sectors of the dorsal premotor cortex in macaques. Eur J Neurosci 2010; 31: 1402-13.
28. Hayasaka S, Nichols TE. Validating cluster size inference: random field and permutation methods. Neuroimage 2003; 20: 2343-56.
29. Heckroth JA. A quantitative morphological analysis of the cerebellar nuclei in normal and lurcher mutant mice. II. Volumetric changes in cytological components. J Comp Neurol 1994; 343: 183-92.
30. Hö pker W. Das Altern des Nucleus dentatus. Z. Altersforschung 1951; 5: 256-77.
31. Klockgether T. Update on degenerative ataxias. Curr Opin Neurol 2011; 24: 339-45.
32. Klockgether T, Petersen D, Grodd W, Dichgans J. Early onset cerebellar ataxia with retained tendon reflexes. Clinical, electrophysiological and MRI observations in comparison with Friedreich's ataxia. Brain 1991; 114: 1559-73.
33. Klockgether T, Skalej M, Wedekind D, Luft AR, Welte D, Schulz JB, et al. Autosomal dominant cerebellar ataxia type I. MRI-based volumetry of posterior fossa structures and basal ganglia in spinocerebellar ataxia types 1, 2 and 3. Brain 1998; 121: 1687-93.
34. Koeppen AH. The pathogenesis of spinocerebellar ataxia. Cerebellum 2005; 4: 62-73.
35. Koeppen AH, Mazurkiewicz JE. Friedreich ataxia: neuropathology revised. J Neuropathol Exp Neurol 2013; 72: 78-90.
36. Koeppen AH, Michael SC, Knutson MD, Haile DJ, Qian J, Levi S, et al. The dentate nucleus in Friedreich's ataxia: the role of ironresponsive proteins. Acta Neuropathol 2007; 114: 163-73.
37. Koeppen AH, Ramirez RL, Bjork ST, Bauer P, Feustel PJ. The reciprocal cerebellar circuitry in human hereditary ataxia. Cerebellum 2013; 12: 493-503.
38. Küper M, Dimitrova A, Thürling M, Maderwald S, Roths J, Elles HG, et al. Evidence for a motor and a non-motor domain in the human dentate nucleus-an fMRI study. Neuroimage 2011; 54: 2612-22.
39. Küper M, Thürling M, Stefanescu R, Maderwald S, Roths J, Elles HG, et al. Evidence for a motor somatotopy in the cerebellar dentate nucleus-an FMRI study in humans. Hum Brain Mapp 2012; 33: 2741-9.
40. Langkammer C, Schweser F, Krebs N, Deistung A, Goessler W, Scheurer E, et al. Quantitative susceptibility mapping (QSM) as a means to measure brain iron? A post mortem validation study. Neuroimage 2012; 62: 1593-9.
41. Lauritzen M, Mathiesen C, Schaefer K, Thomsen KJ. Neuronal inhibition and excitation, and the dichotomic control of brain hemodynamic and oxygen responses. Neuroimage 2012; 62: 1040-50.
42. Linnemann C, Sultan F, Pedroarena CM, Schwarz C, Thier P. Lurcher mice exhibit potentiation of GABA(A)-receptor-mediated conductance in cerebellar nuclei neurons in close temporal relationship to Purkinje cell death. J Neurophysiol 2004; 91: 1102-7.
43. Lukas C, Schö ls L, Bellenberg B, Rüb U, Przuntek H, Schmid G, et al. Dissociation of grey and white matter reduction in spinocerebellar ataxia type 3 and 6: A voxel-based morphometry study. Neurosci Lett 2006; 408: 230-5.
44. Maderwald S, Thürling M, Küper M, Theysohn N, Müller O, Beck A, et al. Direct visualization of cerebellar nuclei in patients with focal cerebellar lesions and its application for lesion-symptom mapping. Neuroimage 2012; 63: 1421-31.
45. Marques JP, Gruetter R, van der Zwaag W. In vivo structural imaging of the cerebellum, the contribution of ultra-high fields. Cerebellum 2012; 11: 384-91.
46. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971; 9: 97-113.
47. Ormerod IE, Harding AE, Miller DH, Johnson G, MacManus D, du Boulay EP, et al. Magnetic resonance imaging in degenerative ataxic disorders. J Neurol Neurosurg Psychiatry 1994; 57: 51-57.
48. Orr HT. Cell biology of spinocerebellar ataxia. J Cell Biol 2012; 197: 167-77.
49. Poser BA, Norris DG. Investigating the benefits of multi-echo EPI for fMRI at 7 T. Neuroimage 2009; 45: 1162-72.
50. Reetz K, Costa AS, Mirzazade S, Lehmann A, Juzek A, Rakowicz M, et al. Genotype-specific patterns of atrophy progression are more sensitive than clinical decline in SCA1, SCA3 and SCA6. Brain 2013; 136: 905-17.
51. Richardson DR, Huang ML, Whitnall M, Becker EM, Ponka P, Suryo Rahmanto Y. The ins and outs of mitochondrial iron-loading: the metabolic defect in Friedreich's ataxia. J Mol Med (Berl) 2010; 88: 323-9.
52. Rüb U, Schö ls L, Paulson H, Auburger G, Kermer P, Jen JC, et al. Clinical features, neurogenetics and neuropathology of the polyglutamine spinocerebellar ataxias type 1, 2, 3, 6 and 7. Prog Neurobiol 2013; 104: 38-66.
53. Sasaki H, Kojima H, Yabe I, Tashiro K, Hamada T, Sawa H, et al. Neuropathological and molecular studies of spinocerebellar ataxia type 6 (SCA6). Acta Neuropathol 1998; 95: 199-204.
54. Scherzed W, Brunt ER, Heinsen H, de Vos RA, Seidel K, Bürk K, et al. Pathoanatomy of cerebellar degeneration in spinocerebellar ataxia type 2 (SCA2) and type 3 (SCA3). Cerebellum 2012; 11: 749-60.
55. Schmitz-Hübsch T, du Montcel ST, Baliko L, Berciano J, Boesch S, Depondt C, et al. Scale for the assessment and rating of ataxia: development of a new clinical scale. Neurology 2006; 66: 1717-20.
56. Schulz JB, Boesch S, Bürk K, Dürr A, Giunti P, Mariotti C, et al. Diagnosis and treatment of Friedreich ataxia: A European perspective. Nat Rev Neurol 2009; 5: 222-34.
57. Schulz JB, Borkert J, Wolf S, Schmitz-Hübsch T, Rakowicz M, Mariotti C, et al. Visualization, quantification and correlation of brain atrophy with clinical symptoms in spinocerebellar ataxia types 1, 3 and 6. Neuroimage 2010; 49: 158-68.
58. Schmahmann JD, Doyon J, McDonald D, Holmes C, Lavoie K, Hurwitz AS, et al. Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. Neuroimage 1999; 10: 233-60.
59. Seidel K, Siswanto S, Brunt ER, den Dunnen W, Korf HW, Rüb U. Brain pathology of spinocerebellar ataxias. Acta Neuropathol 2012; 124: 1-21.
60. Solbach K, Kraff O, Minnerop M, Beck A, Schö ls L, Ladd M, et al. Cerebellar pathology in Friedreich's ataxia: Atrophied nuclei with normal iron content. Neuroimage Clin 2014; 6: 93-9.
61. Stefanescu MR, Thürling M, Maderwald S, Wiestler T, Ladd ME, Diedrichsen J, et al. A 7T fMRI study of cerebellar activation in sequential finger movement tasks. Exp Brain Res 2013; 228: 243-54.
62. Synofzik M, Godau J, Lindig T, Schö ls L, Berg D. Transcranial sonography reveals cerebellar, nigral, and forebrain abnormalities in Friedreich's ataxia. Neurodegener Dis 2011; 8: 470-5.
63. Theysohn JM, Maderwald S, Kraff O, Moenninghoff C, Ladd ME, Ladd SC. Subjective acceptance of 7 Tesla MRI for human imaging. MAGMA 2008; 21: 63-72.
64. Thürling M, Küper M, Stefanescu R, Maderwald S, Gizewski ER, Ladd ME, et al. Activation of the dentate nucleus in a verb generation task: A 7T MRI study. Neuroimage 2011; 57: 1184-91.
65. Triarhou LC, Norton J, Ghetti B. Anterograde transsynaptic degeneration in the deep cerebellar nuclei of Purkinje cell degeneration (pcd) mutant mice. Exp Brain Res 1987; 66: 577-88.
66. van de Warrenburg BP, van Gaalen J, Boesch S, Burgunder JM, Dürr A, Giunti P, et al. EFNS/ENS Consensus on the diagnosis and management of chronic ataxias in adulthood. Eur J Neurol 2014; 21: 552-62.
67. Verstynen TD, Deshpande V. Using pulse oximetry to account for high and low frequency physiological artifacts in the BOLD signal. Neuroimage 2011; 55: 1633-44.
68. Waldvogel D, van Gelderen P, Hallett M. Increased iron in the dentate nucleus of patients with Friedrich's ataxia. Ann Neurol 1999; 46: 123-5.
69. Wang X, Wang H, Xia Y, Jiang H, Shen L, Wang S, et al. A neuropathological study at autopsy of early onset spinocerebellar ataxia 6.
70. J Clin Neurosci 2010; 17: 751-5.
71. Weier K, Beck A, Magon S, Amann M, Naegelin Y, Penner IK, et al. Evaluation of a new approach for semi-automatic segmentation of the cerebellum in patients with multiple sclerosis. J Neurol 2012; 259: 2673-80.
72. Yang Q, Hashizume Y, Yoshida M, Wang Y, Goto Y, Mitsuma N, et al. Morphological Purkinje cell changes in spinocerebellar ataxia type 6. Acta Neuropathol 2000; 100: 371-6.