The Cerebellum

, 6:280 | Cite as

Cognition in hereditary ataxia

  • Katrin BurkEmail author
Original Article


Apart from motor control the cerebellum has been implicated in higher cortical functions such as memory, fronto-executive functions, visuoconstructive skills and emotion. Clinical descriptions of hereditary ataxias mention cognitive impairment to a variable extent. Systematic neuropsychological studies are limited. Regarding the neuropathological pattern in different SCA types, cognitive deficits in hereditary ataxias are not likely to be contingent upon cerebellar degeneration but to result from disruption of cerebrocerebellar circuitries at various levels in the CNS.

Key words

Ataxia cognitive deficits dominant genes recessive genes 


  1. 1.
    Daum I, Ackermann H, Schugens MM, Reimold C, Dichgans J, Birbaumer N. The cerebellum and cognitive functions in humans. Behav Neurosci. 1993;107(3):411–9.PubMedGoogle Scholar
  2. 2.
    Wollmann T, Barroso J, Monton FAN. Neuropsychological test performance of patients with Friedreich’s ataxia. J Clin Exp Neuropsy. 2002;24:677–86.Google Scholar
  3. 3.
    Hart RP, Kwentus JA, Leshner RT, Frazier R. Information processing speed in Friedreich’s ataxia. Neurology. 1985;17:612–14.Google Scholar
  4. 4.
    Botez-Marquard T, Botez MI. Botez-Marquard T, Botez MI. Cognitive behavior in heredodegenerative ataxias. Eur Neurol. 1993;33:351–7.PubMedGoogle Scholar
  5. 5.
    Davies DL. The intelligence of patients with Friedreich’s ataxia. J Neurol Neurosurg Psychiatry. 1949;12:34–8.PubMedGoogle Scholar
  6. 6.
    White M, Lalonde R, Botez-Marquard T. Neuropsychological and neuropsychiatric characteristics of patients with Friedreich’s ataxia. Acta Neurol Scand. 2000;102:222–6.PubMedGoogle Scholar
  7. 7.
    Leclercq M, Harmant J, De Barsy T. Psychometric studies in Friedreich’s ataxia. Acta Neurol Belg. 1985;85:202–21.PubMedGoogle Scholar
  8. 8.
    Mantovan MC, Martinuzzi A, Squarzanti F, Bolla A, Silvestri I, Liessi G, et al. Exploring mental status in Friedreich’s ataxia: A combined neuropsychological, behavioral and neuroimaging study. Eur J Neurol. 2006;13:827–35.PubMedGoogle Scholar
  9. 9.
    Shimazaki H, Takiyama Y, Sakoe K, Ikeguchi K, Niijima K, Kaneko J, et al. Early-onset ataxia with ocular motor apraxia and hypoalbuminemia: The aprataxin gene mutations. Neurology. 2002;59:590–5.PubMedGoogle Scholar
  10. 10.
    Le Ber I, Moreira MC, Rivaud-Pechoux S, Chamayou C, Ochsner F, Kuntzer T, et al. Cerebellar ataxia with oculomotor apraxia type 1: Clinical and genetic studies. Brain. 2003;126:2761–72.PubMedGoogle Scholar
  11. 11.
    Bomont P, Watanabe M, Gershoni-Barush R, Shizuka M, Tananka M, Sugano J. Homozygosity mapping of spinocerebellar ataxia with cerebellar atrophy and peripheral neuropathy to 9q33±34, and with hearing impairment and optic atrophy to 6p21±23. Eur J Hum Genet. 2000;8:986–90.PubMedGoogle Scholar
  12. 12.
    Németh AH, Bochukova E, Dunne E, Huson SM, Elston J, Hannan MA, et al. Autosomal recessive cerebellar ataxia with oculomotor apraxia (ataxiatelangiectasia-like syndrome) is linked to chromosome 9q34. Am J Hum Genet. 2000;67:1320–6.PubMedGoogle Scholar
  13. 13.
    Le Ber I, Bouslam N, Rivaud-Pechoux S, Guimaraes J, Benomar A, Chamayou C, et al. Frequency and phenotypic spectrum of ataxia with oculomotor apraxia 2: A clinical and genetic study in 18 patients. Brain. 2004;127:759–67.PubMedGoogle Scholar
  14. 14.
    Crawford TO. Ataxia-telangiectasia. Semin Pediatr Neurol. 1998;5:287–94.PubMedGoogle Scholar
  15. 15.
    Mostofsky SH, Kunze JC, Cutting LE, Lederman HM, Denckla MB. Judgment of duration in individuals with ataxia-telangiectasia. Dev Neuropsychol. 2000;17:63–74.PubMedGoogle Scholar
  16. 16.
    Goldfarb LG, Chumakov MP, Petrov PA, Fedorova NI, Gajdusek DC. Olivopontocerebellar atrophy in a large Iakut kinship in eastern Siberia. Neurology. 1989;39(11):1527–30.PubMedGoogle Scholar
  17. 17.
    Spadaro M, Giunti P, Lulli P, Frontali M, Jodice C, Cappellacci S, et al. HLA-linked spinocerebellar ataxia: a clinical and genetic study of large Italian kindreds. Acta Neurol Scand. 1992;85(4):257–65.PubMedGoogle Scholar
  18. 18.
    Dubourg O, Dürr A, Cancel G, Stevanin G, Chneiweiss H, Penet C, et al. Analysis of the SCA1 CAG repeat in a large number of families with dominant ataxia: Clinical and molecular correlations. Ann Neurol. 1995;37(2):176–80.PubMedGoogle Scholar
  19. 19.
    Sasaki H, Fukazawa T, Yanagihara T, Hamada T, Shima K, Matsumoto A, et al. Clinical features and natural history of spinocerebellar ataxia type 1. Acta Neurol Scand. 1996;93(1):64–71.PubMedGoogle Scholar
  20. 20.
    Giunti P, Sweeney MG, Spadaro M, Jodice C, Novelletto A, Malaspina P, et al. The trinucleotide repeat expansion on chromosome 6p (SCA1) in autosomal dominant cerebellar ataxias. Brain. 1994;117(Pt 4):645–9.PubMedGoogle Scholar
  21. 21.
    Kameya T, Abe K, Aoki M, Sahara M, Tobita M, Konno H, et al. Analysis of spinocerebellar ataxia type 1 (SCA1)-related CAG trinucleotide expansion in Japan. Neurology. 1995;45(8):1587–94.PubMedGoogle Scholar
  22. 22.
    Ranum LP, Chung MY, Banfi S, Bryer A, Schut LJ, Ramesar R, et al. Molecular and clinical correlations in spinocerebellar ataxia type I: Evidence for familial effects on the age at onset. Am J Hum Genet. 1994;55(2):244–52.PubMedGoogle Scholar
  23. 23.
    Genis D, Matilla T, Volpini V, Rosell J, Davalos A, Ferrer I, et al. Clinical, neuropathologic, and genetic studies of a large spinocerebellar ataxia type 1 (SCA1) kindred: (CAG)n expansion and early premonitory signs and symptoms. Neurology. 1995;45(1):24–30.PubMedGoogle Scholar
  24. 24.
    Kish SJ, Schut L, Simmons J, Gilbert J, Chang LJ, Rebbetoy M. Brain acetylcholinesterase activity is markedly reduced in dominantly-inherited olivopontocerebellar atrophy. J Neurol Neurosurg Psychiatry. 1988;51(4):544–8.PubMedCrossRefGoogle Scholar
  25. 25.
    Bürk K, Bösch S, Globas C, Zühlke C, Daum I, Klockgether T, et al. Executive dysfunction in spinocerebellar ataxia type 1. Eur Neurol. 2001;46(1):43–8.PubMedGoogle Scholar
  26. 26.
    Wadia NH. A variety of olivopontocerebellar atrophy distinguished by slow eye movements and peripheral neuropathy. Adv Neurol. 1984;41:149–77.PubMedGoogle Scholar
  27. 27.
    Dürr A, Smadja D, Cancel G, Lezin A, Stevanin G, Mikol J, et al. Autosomal dominant cerebellar ataxia type I in Martinique (French West Indies). Clinical and neuropathological analysis of 53 patients from three unrelated SCA2 families. Brain. 1995;118(Pt 6):1573–81.PubMedGoogle Scholar
  28. 28.
    Cancel G, Dürr A, Didierjean O, Imbert G, Bürk K, Lezin A, et al. Molecular and clinical correlations in spinocerebellar ataxia 2: a study of 32 families. Hum Mol Genet. 1997;6(5):709–15.PubMedGoogle Scholar
  29. 29.
    Bürk K, Stevanin G, Didierjean O, Cancel G, Trottier Y, Skalej M, et al. Clinical and genetic analysis of three German kindreds with autosomal dominant cerebellar ataxia type I linked to the SCA2 locus. J Neurol. 1997;244(4):256–61.PubMedGoogle Scholar
  30. 30.
    Storey E, Forrest SM, Shaw JH, Mitchell P, Gardner RJ. Spinocerebellar ataxia type 2: clinical features of a pedigree displaying prominent frontal-executive dysfunction. Arch Neurol. 1999;56(1):43–50.PubMedGoogle Scholar
  31. 31.
    Moretti P, Blazo M, Garcia L, Armstrong D, Lewis RA, Roa B, et al. Spinocerebellar ataxia type 2 (SCA2) presenting with ophthalmoplegia and developmental delay in infancy. Am J Med Genet. 2004;124(4):392–396.Google Scholar
  32. 32.
    Bürk K, Globas C, Bösch S, Gräber S, Abele M, Brice A, et al. Cognitive deficits in spinocerebellar ataxia 2. Brain. 1999;122(Pt 4):769–77.PubMedGoogle Scholar
  33. 33.
    Shimohata T, Matsuzawa Y, Tanaka K, Onodera O, Tanaka K, Nishizawa M. Evaluation of two patients with frontal lobe dysfunction using brain SPECT with three-dimensional stereotactic surface projection (3D-SSP). Rinsho Shinkeigaku. 2005;45(1):22–6.PubMedGoogle Scholar
  34. 34.
    Gambardella A, Annesi G, Bono F, Spadafora P, Valentino P, PA A, et al. CAG repeat length and clinical features in three Italian families with spinocerebellar ataxia type 2 (SCA2): Early impairment of Wisconsin Card Sorting Test and saccade velocity. J Neurol. 1998;245(10):647–52.PubMedGoogle Scholar
  35. 35.
    Le Pira F, Zappala G, Saponara R, Domina E, Restivo DA, Reggio E, et al. Cognitive findings in spinocerebellar ataxia type 2: Relationship to genetic and clinical variables. J Neurol Sci. 2002;201:53–7.PubMedGoogle Scholar
  36. 36.
    Rosenberg RN, Nyhan WL, Bay C, Shore P. Autosomal dominant striatonigral degeneration. Neurology. 1976;26:703–14.PubMedGoogle Scholar
  37. 37.
    Coutinho P, Andrade C. Autosomal dominant system degeneration in Portuguese families of the Azores Islands. A new genetic disorder involving cerebellar, pyramidal, extrapyramidal and spinal cord motor functions. Neurology. 1978;28(7):703–9.PubMedGoogle Scholar
  38. 38.
    Fowler HL. Machado-Joseph-Azorean disease. A ten-year study. Arch Neurol. 1984;41:921–5.PubMedGoogle Scholar
  39. 39.
    Burt T, Blumberg P, Currie B. A dominant hereditary ataxia resembling Machado-Joseph disease in Arnhem Land, Australia. Neurology. 1993;43:1750–2.PubMedGoogle Scholar
  40. 40.
    Sequeiros J, Coutinho P. Epidemiology and clinical aspects of Machado-Joseph disease. Adv Neurol. 1993;61:139–53.PubMedGoogle Scholar
  41. 41.
    Zawacki T, Grace J, Friedman J, Sudarsky L. Executive and emotional dysfunction in Machado-Joseph disease. Mov Disord. 2002; 17(5): 1004–10.PubMedGoogle Scholar
  42. 42.
    Kawai Y, Takeda A, Abe Y, Washimi Y. Cognitive impairments in Machado-Joseph disease. Arch Neurol. 2004;61:1757–60.PubMedGoogle Scholar
  43. 43.
    Maruff P, Tyler P, Burt T, Currie B, Burns C, Currie J. Cognitive deficits in Machado-Joseph disease. Ann Neurol. 1996;40(3):421–7.PubMedGoogle Scholar
  44. 44.
    Radvany J, Camargo CHP, Costa ZM, Fonseca NC, Nascimento ED. Machado-Joseph disease of Azorean ancestry in Brazil: The Catarina kindred: Neurological, neuroimaging, psychiatric and neuropsychological findings in the largest known family, the ‘Catarina’ kindred. Arquivos de Neuro Psiquiatria. 1993;5:21–30.Google Scholar
  45. 45.
    Bürk K, Globas C, Bösch S, Klockgether T, Zühlke C, Daum I, et al. Cognitive deficits in spinocerebellar ataxia type 1, 2, and 3. J Neurol. 2003;250(2):207–11.PubMedGoogle Scholar
  46. 46.
    Schöls L, Krüger R, Amoiridis G, Przuntek H, Epplen JT, Riess O. Spinocerebellar ataxia type 6: genotype and phenotype in German kindreds. J Neurol Neurosurg Psychiatry. 1998;64(1):67–73.PubMedGoogle Scholar
  47. 47.
    Matsumura R, Futamura N, Fujimoto Y, Yanagimoto S, Horikawa H, Suzumura A, et al. Spinocerebellar ataxia type 6. Molecular and clinical features of 35 Japanese patients including one homozygous for the CAG repeat expansion. Neurology. 1997;49(5):1238–43.PubMedGoogle Scholar
  48. 48.
    Stevanin G, Dürr A, David G, Didierjean O, Cancel G, Rivaud S, et al. Clinical and molecular features of spinocere-bellar ataxia type 6. Neurology. 1997;49(5):1243–6.PubMedGoogle Scholar
  49. 49.
    Tashiro H, Suzuki SO, Hitotsumatsu T, Iwaki T. An autopsy case of spinocerebellar ataxia type 6 with mental symptoms of schizophrenia and dementia. Clin Neuropathol. 1999;18(4):198–204.PubMedGoogle Scholar
  50. 50.
    Globas C, Bösch S, Zühlke C, Daum I, Dichgans J, Bürk K. The cerebellum and cognition: intellectual function in spinocerebellar ataxia type 6 (SCA6). J Neurol. 2003;250:1482–7.PubMedGoogle Scholar
  51. 51.
    Schelhaas HJ, van de Warrenburg BP, Hageman G, Ippel EE, van Hout m, Kremer B. Cognitive impairment in SCA19. Acta Neurol Belg. 2003;103(4):199–205.PubMedGoogle Scholar
  52. 52.
    Shatunov A, Fridman EA, Pagan FI, Leib J, Singleton A, Hallett M, et al. Small de novo duplication in the repeat region of the TATA-box-binding protein gene manifest with a phenotype similar to variant Creutzfeldt-Jakob disease. Clin Genet. 2004;66(6):496–501.PubMedGoogle Scholar
  53. 53.
    De Michele G, Maltecca F, Carella M, Volpe G, Orio M, De Falco A, et al. Dementia, ataxia, extrapyramidal features, and epilepsy: phenotype spectrum in two Italian families with spinocerebellar ataxia type 17. Neurol Sci. 2003;24(3):166–7.PubMedGoogle Scholar
  54. 54.
    Klebe S, Dürr A, Rentschier A, Hahn-Barma V, Abele M, Bouslam N, et al. New mutation in protein kinse C gamma associated with spinocerebellar ataxia type 14. Ann Neurol. 2005;58(5):720–9.PubMedGoogle Scholar
  55. 55.
    Stevanin G, Hahn V, Lohmann E, Boustany RM, Gouttard M, Soumphonphakdy C, et al. Mutation in the catalytic domain of protein kinase C gamma and extension of the phenotype associated with spinocerebellar ataxia type 14. Arch Neurol. 2004;61(8):1242–8.PubMedGoogle Scholar
  56. 56.
    Lin X, Ashizawa T. Recent progress in spinocerebellar ataxia type-10 (SCA10). Cerebellum. 2005;4(1):37–42.PubMedGoogle Scholar
  57. 57.
    Le Ber I, Camuzat A, Castelnovo G, Azulay JP, Genton P, Gastaut JL, et al. Prevalence of dentatorubral-pallidoluysian atrophy in a large series of white patients with cerebellar ataxia. Arch Neurol. 2003;60(8):1097–9.PubMedGoogle Scholar
  58. 58.
    Gao JH, Parsons LM, Bower JM, Xiong J, Li J, Fox PT. Cerebellum implicated in sensory acquisition and discrimination rather than motor control. Science. 1996;272(5261): 545–7.PubMedGoogle Scholar
  59. 59.
    Akshoomoff NA, Courchesne E. A new role for the cerebellum in cognitive operations. Behav Neurosci. 1992;106(5):731–8.PubMedGoogle Scholar
  60. 60.
    Leiner HC, Leiner AL, Dow RS. The underestimated cerebellum. Hum Brain Mapp. 1995;2:244–54.Google Scholar
  61. 61.
    Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome [see comments]. Brain. 1998;121:561–79.PubMedGoogle Scholar
  62. 62.
    Grafman J, Litvan I, Massaquoi S, Stewart M, Sirigu A, Hallett M. Cognitive planning deficit in patients with cerebellar atrophy. Neurology. 1992;42(8):1493–6.PubMedGoogle Scholar
  63. 63.
    Desmond JE, Gabrieli JD, Wagner AD, Ginier BL, Glover GH. Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tests as revealed by functional MRI. J Neurosci. 1997;17:9675–85.PubMedGoogle Scholar
  64. 64.
    Grasby PM, Frith CD, Fristen KJ, Bench C, Frackowiak RS, Dolan RJ. Functional mapping of brain areas implicated in auditory-verbal memory function. Brain. 1993;116:1–20.PubMedGoogle Scholar
  65. 65.
    Petersen SE, Fox PT, Posner MI, Mintum MA, Raichle ME. Positron emission tomographic studies of the processing of single words. J Cogn Neurosci. 1989;1:153–70.Google Scholar
  66. 66.
    Klein D, Milner B, Zatorre RJ, Meyer E, Evans AC. The neural substrates underlying word generation: A bilingual functional-imaging study. Proc Natl Acad Sci USA. 1995;92:2899–903.PubMedGoogle Scholar
  67. 67.
    Jenkins IH, Brooks DJ, Nixon PD, Frackowiak RS, Passingham RE. Motor sequence learning: A study with positron emission tomography. J Neurosci. 1994;14(6): 3775–90.PubMedGoogle Scholar
  68. 68.
    Kim SG, Ugurbil K, Strick PL. Activation of a cerebellar output nucleus during cognitive processing. Science. 1994;265:949–51.PubMedGoogle Scholar
  69. 69.
    Logan CG, Grafton ST. Functional anatomy of human eyeblink conditioning determined with regional cerebral glucose metabolism and positron-emission tomography. Proc Natl Acad Sci USA. 1995;92(16):7500–04.PubMedGoogle Scholar
  70. 70.
    Allen G, Buxton RB, Wong EC, Courchesne E. Attentional activation of the cerebellum independent of motor involvement. Science. 1997;275(5308):1940–3.PubMedGoogle Scholar
  71. 71.
    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(4):490–9.PubMedGoogle Scholar
  72. 72.
    Takiyama Y, Oyanagi S, Kawashima S, Sakamoto H, Saito K, Yoshida M, et al. A clinical and pathologic study of a large Japanese family with Machado-Joseph disease tightly linked to the DNA markers on chromosome 14q. Neurology. 1994;44(7):1302–08.PubMedGoogle Scholar
  73. 73.
    Bruni AC, Takahashi-Fujigasaki J, Maltecca F, Foncin JF, Servadio A, Casari G, et al. Behavioral disorder, dementia, ataxia, and rigidity in a large family with TATA box-binding protein mutation. Arch Neurol. 2004;61(8):1314–20.PubMedGoogle Scholar
  74. 74.
    Rolfs A, Koeppen AH, Bauer I, Bauer P, Buhlmann S, Topka H, et al. Clinical features and neuropathology of autosomal dominant spinocerebellar ataxia (SCA17). Ann Neurol. 2003;54:367–75.PubMedGoogle Scholar
  75. 75.
    Orozco G, Estrada R, Perry TL, Arana J, Fernandez R, Gonzalez Quevedo A, et al. Dominantly inherited olivopontocerebellar atrophy from eastern Cuba. Clinical, neuropathological, and biochemical findings. J Neurol Sci. 1989;93(1):37–50.PubMedGoogle Scholar
  76. 76.
    Estrada R, Galarraga J, Orozco G, Nodarse A, Auburger G. Spinocerebellar ataxia 2 (SCA2): morphometric analyses in 11 autopsies. Acta Neuropathol Berl. 1999;97(3):306–10.PubMedGoogle Scholar
  77. 77.
    Pang JT, Giunti P, Chamberlain S, An SF, Vitaliani R, Scaravilli T, et al. Neuronal intranuclear inclusions in SCA2: A genetic, morphological and immunohistochemical study of two cases. Brain. 2002;1425:656–63.Google Scholar
  78. 78.
    Spinella GM, Sheridan PH. Research initiatives on Machado-Joseph disease: National Institute of Neurological Disorders and Stroke Workshop Summary. Neurology. 1992;42:2048–51.PubMedGoogle Scholar
  79. 79.
    Zubenko GS, Moossy J, Martinez AJ, Rao GR, Kopp U, Hanin I. A brain regional analysis of morphologic and cholinergic abnormalities in Alzheimer’s disease. Arch Neurol. 1989;46(6):634–8.PubMedGoogle Scholar
  80. 80.
    Fishman EB, Siek GC, MacCallum RD, Bird ED, Volicer L, Marquis JK. Distribution of the molecular forms of acetylcholinesterase in human brain: Alterations in dementia of the Alzheimer type. Ann Neurol. 1986;19(3):246–52.PubMedGoogle Scholar
  81. 81.
    Iyo M, Namba H, Fukushi K, Shinotoh H, Nagatsuka S, Suhara T, et al. Measurement of acetylcholinesterase by positron emission tomography in the brains of healthy controls and patients with Alzheimer’s disease. Lancet. 1997;349(9068):1805–9.PubMedGoogle Scholar
  82. 82.
    Kish SJ, el Awar M, Schut L, Leach L, Oscar Berman M, Freedman M. Cognitive deficits in olivopontocerebellar atrophy: Implications for the cholinergic hypothesis of Alzheimer’s dementia. Ann Neurol. 1988;24(2):200–6.PubMedGoogle Scholar
  83. 83.
    Andreasen NC, O’Leary DS, Arndt S, Cizadlo T, Hurtig R, Rezai K, et al. Short term and long term verbal memory: A positron emission tomography study. Proc Natl Acad Sci USA. 1995;92:5111–5.PubMedGoogle Scholar
  84. 84.
    Jetter W, Poser U, Freeman RB, Markowithsch HJ. A verbal long term memory deficit in frontal lobe damaged patients. Cortex. 1986;22:229–42.PubMedGoogle Scholar
  85. 85.
    Wadia NH. A common variety of hereditary ataxia in India. In: Lechtenberg R, editor. Handbook of cerebellar diseases,. pp 373–88, New York: Marcel Dekker, Inc., 1993.Google Scholar
  86. 86.
    Kish SJ, el Awar M, Stuss D, Nobrega J, Currier R, Aita JF, et al. Neuropsychological test performance in patients with dominantly inherited spinocerebellar ataxia: Relationship to ataxia severity. Neurology. 1994;44(9):1738–46.PubMedGoogle Scholar
  87. 87.
    Owen AM, James M, Leigh PN, Summers BA, Marsden CD, Quinn NP, et al. Fronto-striatal cognitive deficits at different stages of Parkinson’s disease. Brain. 1992;115(Pt 6):1727–51.PubMedGoogle Scholar
  88. 88.
    Gilman S, Sima AA, Junck L, Kluin KJ, Koeppe RA, Lohman ME, et al. Spinocerebellar ataxia type 1 with multiple system degeneration and glial cytoplasmic inclusions. Ann Neurol. 1996;39:241–55.PubMedGoogle Scholar
  89. 89.
    Rüb U, de Vos RA, Brunt ER, Sebesteny T, Schöls L, Auburger G, et al. Spinocerebellar ataxia type 3 (SCA3): Thalamic neurodegeneration occurs independently from thalamic ataxin-3 immunopositive neuronal intranuclear inclusions. Brain Pathol. 2006;16(3):218–27.PubMedGoogle Scholar
  90. 90.
    Rüb U, Del Turco D, Bürk K, Diaz GO, Auburger G, Mittelbronn M, et al. Extended pathoanatomical studies point to a consistent affection of the thalamus in spinocerebellar ataxia type 2. Neuropathol Appl Neurobiol. 2005;31(2): 127–40.PubMedGoogle Scholar
  91. 91.
    Schmahmann JD, Pandya DN. Prefrontal cortex projections to the basilar pons in rhesus monkey: Implications for the cerebellar contribution to higher function. Neurosci Lett. 1995;199(3):175–8.PubMedGoogle Scholar
  92. 92.
    Schmahmann JD, Pandya DN. Anatomic organization of the basilar pontine projections from prefrontal cortices in rhesus monkey. J Neurosci. 1997;17(1):438–58.PubMedGoogle Scholar
  93. 93.
    Allen GI, Tsukahara N. Cerebrocerebellar communication systems. [Review]. Physiol Rev. 1974;54:957–1006.PubMedGoogle Scholar
  94. 94.
    Middleton FA, Strick PL. Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science. 1994;266(5184):458–61.PubMedGoogle Scholar
  95. 95.
    Middleton FA, Strick PL. Dentate output channels: motor and cognitive components. Prog Brain Res. 1997;114:553–66.PubMedGoogle Scholar
  96. 96.
    Schmahmann JD, Pandya DN. The cerebrocerebellar system. Int Rev Neurobiol. 1997;41:31–60.PubMedGoogle Scholar
  97. 97.
    Brodai P. The corticopontine projection in the rhesus monkey. Origin and principles of organization. Brain. 1978;101:251–83.Google Scholar
  98. 98.
    Schmahmann JD, Pandya DN. Anatomical investigation of projections to the basis pontis from posterior parietal association cortices in rhesus monkey. J Comp Neurol. 1989;289(1):53–73.PubMedGoogle Scholar
  99. 99.
    De Michele G, Mainenti P, Soricelli A. Cerebral blood flow in spinocerebellar degenerations: A single photon emission tomography study in 28 patients. Eur Neurol. 1998;245:603–08.Google Scholar
  100. 100.
    Campuzano V, Montermini L, Lutz Y, Cova L, Hindelang C, Jiralerspong S, et al. Frataxin is reduced in Friedreich ataxia patients and is associated with mitochondrial membranes. Hum Mol Genet. 1997;6(11):1771–80.PubMedGoogle Scholar
  101. 101.
    Campuzano V, Montermini L, Molto MD, Pianese L, Cossee M, Cavalcanti F, et al. Friedreich’s ataxia: Autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science. 1996;271(5254):1423–7.PubMedGoogle Scholar

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© Springer 2007

Authors and Affiliations

  1. 1.Department of NeurologyUniversity of MarburgGermany
  2. 2.Institute of Brain ResearchUniversity of TübingenTübingenGermany

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