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Spinocerebellar Ataxia Type 2 Neurodegeneration Differentially Affects Error-Based and Strategic-Based Visuomotor Learning

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Abstract

There are different types of visuomotor learning. Among the most studied is motor error-based learning where the sign and magnitude of the error are used to update motor commands. However, there are other instances where individuals show visuomotor learning even if the sign or magnitude of the error is precluded. Studies with patients suggest that the former learning is impaired after cerebellar lesions, while basal ganglia lesions disrupt the latter. Nevertheless, the cerebellar role is not restricted only to error-based learning, but it also contributes to several cognitive processes. Therefore, here, we tested if cerebellar ataxia patients are affected in two tasks, one that depends on error-based learning and the other that prevents the use of error-based learning. Our results showed that cerebellar patients have deficits in both visuomotor tasks; however, while error-based learning tasks deficits correlated with the motor impairments, the motor error-dependent task did not correlate with any motor measure.

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References

  1. Ohlsson S. Learning from performance errors. Psychol Rev. 1996;103:241–62.

    Article  Google Scholar 

  2. Kawato M, Gomi H. The cerebellum and VOR/OKR learning models. Trends Neurosci. 1992;15(11):445–53.

    Article  PubMed  CAS  Google Scholar 

  3. Kornheiser AS. Adaptation to laterally displaced vision: a review. Psychol Bull. 1976;83(5):783–816.

    Article  PubMed  CAS  Google Scholar 

  4. Fernández-Ruiz J, Díaz R. Prism adaptation and aftereffect: specifying the properties of procedural memory system. Learn Mem. 1999;6(1):47–53.

    PubMed  Google Scholar 

  5. Velázquez-Perez L, Díaz R, Pérez-González R, Canales N, Rodríguez-Labrada R, Medrano J, et al. Motor decline in clinically presymptomatic spinocerebellar ataxia type 2 gene carries. PLoS One. 2009;4(4):e5398.

    Article  PubMed  Google Scholar 

  6. Redding GM, Wallace B. Paradigm and generalizations. In: Redding GM, Wallace B, editors. Adaptive spatial alignment. Mahwah: Lawrence Erlbaum Associates, Inc; 1997. p. 53–66.

    Google Scholar 

  7. Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT. Throwing while looking through prism. II. Specificity and storage of multiple gaze-throw calibrations. Brain. 1996;119(Pt 4):1199–211.

    Article  PubMed  Google Scholar 

  8. Fernández-Ruiz J, Velasquez-Perez L, Díaz R, Drucker-Colín R, Pérez-Gonzalez R, Canales N, et al. Prisms adaptation in spinocerebellar ataxia type 2. Neuropsychologia. 2007;45(12):2692–8.

    Article  PubMed  Google Scholar 

  9. Fernández-Ruiz J, Hall-Haro C, Díaz R, Mischner J, Vergara P, Lopez-García JC. Learning motor synergies makes use of information on muscular load. Lern Mem. 2000;7(4):193–8.

    Article  Google Scholar 

  10. Lillicrap T, Moreno-Briseño P, Díaz R, Tweed DB, Troje NF, Fernandez-Ruiz J. Adapting to inversion of the visual field: a new twist on an old problem. Exp Brain Res. 2013;1–13. doi:10.1007/s00221-013-3565-6.

  11. Redding GM, Wallace B. Effects on prism adaptation of duration and timing of visual feedback during pointing. J Mot Behav. 1990;22(2):209–24.

    Article  PubMed  CAS  Google Scholar 

  12. Marotta JJ, Keith GP, Crawford JD. Task-specific sensorimotor adaptation to reversing prisms. J Neurophysiol. 2005;93(2):1104–10.

    Article  PubMed  Google Scholar 

  13. Taylor JA, Ivry RB. The role of strategies in motor learning. Ann N Y Acad Sci. 2012;1251:1–12.

    Article  PubMed  Google Scholar 

  14. Redding GM, Wallace B. Adaptive spatial alignment and strategic perceptual-motor control. J Exp Psychol Hum Percept Perform. 1996;22(2):379–94.

    Article  PubMed  CAS  Google Scholar 

  15. Abdelghani MN, Lillicrap TP, Tweed DB. Sensitivity derivatives for flexible sensorimotor learning. Neural Comput. 2008;20(8):2085–111.

    Article  PubMed  CAS  Google Scholar 

  16. Pisella L, Michel C, Gréa H, Tolikete C, Vighetto A, Rossetti Y. Preserved prism adaptation in bilateral optic ataxia: strategic versus adaptive reaction to prism. Exp Brain Res. 2004;156(4):399–408.

    Article  PubMed  CAS  Google Scholar 

  17. Taylor JA, Klemfuss NM, Ivry RB. An explicit strategy prevail when the cerebellum fail to compute movement errors. Cerebellum. 2010;9(4):580–6.

    Article  PubMed  Google Scholar 

  18. Maschke M, Gomez CM, Ebner TJ, Konczak J. Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. J Neurophysiol. 2004;91(1):230–8.

    Article  PubMed  Google Scholar 

  19. Criscimagna-Hemminger SE, Bastian AJ, Shadmer R. Size of error affects cerebellar contributions to motor learning. J Neurophysiol. 2010;103(4):2275–84.

    Article  PubMed  Google Scholar 

  20. Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT. Throwing while looking through prism. I. Focal olivocerebellar lesions impair adaptation. Brain. 1996;119(Pt4):1183–98.

    Article  PubMed  Google Scholar 

  21. Pulst SM, Nechiporuk A, Nechiporuk T, Gispert S, Chen XN, Lopes-Cendes I, et al. Moderate expansion of normally biallelic trinucleotide repeat in spinocerebellar ataxia type 2. Nat Genet. 1996;14(3):269–76.

    Article  PubMed  CAS  Google Scholar 

  22. Auburger G, Diaz GO, Capote RF, Sanchez SG, Perez MP, del Cueto ME, et al. Autosomal dominant ataxia: genetic evidence for locus heterogeneity from a Cuban founder-effect population. Am J Hum Genet. 1990;46(6):1163–77.

    PubMed  CAS  Google Scholar 

  23. Dueñas AM, Goold R, Giunti P. Molecular pathogenesis of spinocerebellar ataxias. Brain. 2006;129(Pt6):1357–70.

    Article  PubMed  Google Scholar 

  24. Durr A. Autosomal dominant cerebellar ataxias: polyglutamine expansions and beyond. Lancet Neurol. 2010;9(9):885–94.

    Article  PubMed  CAS  Google Scholar 

  25. Estrada R, Galarraga J, Orozco G, Nodarse A, Auburger G. Spinocerebellar ataxia 2 (SCA2): morphometric analyses in 11 autopsies. Acta Neuropathol. 1999;97(3):306–10.

    Article  PubMed  CAS  Google Scholar 

  26. Geschwind DH, Perlman S, Figueroa CP, Treiman LJ, Pulst SM. The prevalence and wide clinical spectrum of the spinocerebellar ataxia type 2 trinucleotide repeat in patients with autosomal dominant cerebellar ataxia. Am J Hum Genet. 1997;60(4):842–50.

    PubMed  CAS  Google Scholar 

  27. Velázquez-Pérez L, Rodriguez-Labrada R, García-Rodríguez JC, Almaguer-Mederos LE, Cruz-Mariño MT, Laffita-Mesa JM. A comprehensive review of spinocerebellar ataxia type 2 in Cuba. Cerebellum. 2011;10(2):184–98.

    Article  PubMed  Google Scholar 

  28. 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(11):1717–20.

    Article  PubMed  Google Scholar 

  29. Folstein MF, Folstein SE, McHugh PR. Mini-mental state. A practical method for grading the cognitive state of patients for the clinicians. J Psychiatr Res. 1975;12(3):189–98.

    Article  PubMed  CAS  Google Scholar 

  30. Council for International Organizations of Medical Sciences. International ethical guidelines for biomedical research involving human subjects. Bull Med Ethics. 2002;182:17–23.

    Google Scholar 

  31. Tseng YW, Diedrichsen J, Krakauer JW, Shadmer R, Bastian AJ. Sensory predictions errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol. 2007;98(1):54–62.

    Article  PubMed  Google Scholar 

  32. Rabe K, Livne O, Gizewski ER, Aurich V, Beck A, Timmann D, et al. Adaptation to visuomotor rotation and force field perturbation is correlated to different brain areas in patients with cerebellar degeneration. J Neurophysiol. 2009;101(4):1961–71.

    Article  PubMed  CAS  Google Scholar 

  33. Donchin O, Rabe K, Diedrichsen J, Lally N, Schoch B, Gizewski ER, et al. Cerebellar regions involved in adaptation to force field and visuomotor perturbation. J Neurophysiol. 2012;107(1):134–47.

    Article  PubMed  Google Scholar 

  34. Della-Maggiore V, Scholz J, Johansen-Berg H, Paus T. The rate of visuomotor adaptation correlates with cerebellar white-matter microstructure. Hum Brain Mapp. 2009;30(12):4048–53.

    Article  PubMed  Google Scholar 

  35. Brenneis C, Bösch SM, Schocke M, Wenning GK, Poewe W. Atrophy patter in SCA2 determined by voxel-based morphometry. Neuroreport. 2003;14(14):1799–802.

    Article  PubMed  Google Scholar 

  36. Della Nave R, Ginestroni A, Tessa C, Cosottini M, Giannelli M, Salvatores E, et al. Brain structural damage in spinocerebellar ataxia type 2. A voxel-based morphometry study. Mov Disord. 2008;23(6):899–903.

    Article  PubMed  Google Scholar 

  37. Goel G, Pal PK, Ravishankar S, Venkatasubramanian G, Jayakumar PN, Krishna N, et al. Gray matter volume deficits in spinocerebellar ataxia: an optimized voxel based morphometric study. Parkinsonism Relat Disord. 2011;7(7):521–7.

    Article  Google Scholar 

  38. Fernández-Ruiz, Díaz R, Hall-Haro C, Vergara P, Mischner J, Nuñes L, et al. Normal prism adaptation but reduced after-effect in basal ganglia disorders using a throwing task. Eur J Neurosci. 2003;18(3):689–94.

    Article  PubMed  Google Scholar 

  39. Drepper J, Timmann D, Kolb FP, Diener HC. Non-motor associative learning in patients with isolated degenerative cerebellar disease. Brain. 1999;122(Pt 1):87–97.

    Article  PubMed  Google Scholar 

  40. Fernandez-Ruiz J, Wong W, Armstrong IT, Flanagan JR. Relation between reaction time and reach errors during visuomotor adaptation. Behav Brain Res. 2011;219(1):8–14.

    Article  PubMed  Google Scholar 

  41. Ramnani N. The primate cortico-cerebellar system anatomy and function. Nat Rev Neurosci. 2006;7(7):511–22.

    Article  PubMed  CAS  Google Scholar 

  42. Mazzoni P, Krakauer JW. An implicit plan overrides an explicit strategy during visuomotor adaptation. J Neurosci. 2006;26(14):3642–5.

    Article  PubMed  CAS  Google Scholar 

  43. Fuster JM. Upper processing stages of the perception action cycle. Trends Cogn Sci. 2004;8(4):143–5.

    Article  PubMed  Google Scholar 

  44. Ramnani N, Behrens TE, Johansen-Berg H, Richter MC, Pinsk MA, Andersson JL, et al. The evolution of prefrontal inputs to the cortico-pontine system: diffusion imaging evidence from Macaque monkeys and humans. Cereb Cortex. 2006;16(6):811–8.

    Article  PubMed  Google Scholar 

  45. Alcauter S, Barrios FA, Díaz R, Fernández-Ruiz J. Gray and white matter alterations in spinocerebellar ataxia type 7: an in vivo DTI and VBM study. NeuroImage. 2011;55(1):1–7.

    Article  PubMed  CAS  Google Scholar 

  46. Barrios FA, Gonzalez L, Favila R, Alonso ME, Salgado PM, Díaz R, et al. Olfaction and neurodegeneration in HD. Neuroreport. 2007;18(1):73–6.

    Article  PubMed  Google Scholar 

  47. Baillieux H, De Smet HJ, Paquier PF, De Deyn PP, Mariën P. Cerebellar neurocognition: insights into the bottom of the brain. Clin Neurol Neurosurg. 2008;110(8):763–73.

    Article  PubMed  Google Scholar 

  48. Strick PL, Dum PL, Fiez JA. Cerebellum and nonmotor function. Annu Rev Neurosci. 2009;32:413–34.

    Article  PubMed  CAS  Google Scholar 

  49. Ito M. Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci. 2008;9(4):304–13.

    Article  PubMed  CAS  Google Scholar 

  50. Schlerf JE, Galea JM, Bastian AJ, Celnik PA. Dynamic modulation of cerebellar excitability for abrupt, but not gradual, visuomotor adaptation. J Neurosci. 2012;32(34):11610–7.

    Article  PubMed  CAS  Google Scholar 

  51. Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121(Pt 4):561–79.

    Article  PubMed  Google Scholar 

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Acknowledgments

We would like to thank patients, patients' families, control participants and the Cuban Ministry of Health for the cooperation given. The research was supported in part by a UNAM grant PAPIIT IN202810 and CONACYT grant 102314. Israel Vaca-Palomares was supported by CONACYT grant 229175.

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The authors on this manuscript do not have any conflicts of interest.

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Authors and Affiliations

  1. Facultad de Psicología, Universidad Nacional Autónoma de México, Mexico City, Distrito Federal, Mexico

    Israel Vaca-Palomares

  2. Laboratorio de Neuropsicología, Departamento de Fisiología, Facultad de Medicina, Universidad Nacional Autónoma de México, Coyoacan, Mexico City, 04510, Distrito Federal, Mexico

    Israel Vaca-Palomares, Rosalinda Díaz & Juan Fernandez-Ruiz

  3. Centro para la Investigación y Rehabilitación de las Ataxias Hereditarias, Holguín, Cuba

    Roberto Rodríguez-Labrada, Jacqeline Medrano-Montero, Yaimé Vázquez-Mojena & Luis Velázquez-Pérez

  4. Facultad de Psicología, Universidad Veracruzana, Xalapa, Veracruz, Mexico

    Juan Fernandez-Ruiz

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  1. Israel Vaca-Palomares
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  2. Rosalinda Díaz
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Correspondence to Luis Velázquez-Pérez or Juan Fernandez-Ruiz.

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Vaca-Palomares, I., Díaz, R., Rodríguez-Labrada, R. et al. Spinocerebellar Ataxia Type 2 Neurodegeneration Differentially Affects Error-Based and Strategic-Based Visuomotor Learning. Cerebellum 12, 848–855 (2013). https://doi.org/10.1007/s12311-013-0496-5

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