Spinocerebellar ataxia type 2 neurodegeneration differentially affects error-based and strategic-based visuomotor learning

Cerebellum

Volumn 12, Issue 6, 2013, Pages 848-855

  Vaca Palomares, Israel ^a   Díaz, Rosalinda ^a   Rodríguez Labrada, Roberto ^b   Medrano Montero, Jacqeline ^b   Vázquez Mojena, Yaimé ^b   Velázquez Pérez, Luis ^b   Fernandez Ruiz, Juan ^a,c  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b Centro para la Investigacion y Rehabilitacion de las Ataxias Hereditarias Cuba   (Cuba)

^c UNIVERSIDAD VERACRUZANA   (Mexico)

Author keywords

Cerebellum; Learning dissociation; Motor impairment; SCA2; Sensorimotor learning; Visuomotor learning

Indexed keywords

ADAPTATION; ADOLESCENT; ADULT; ARTICLE; CEREBELLAR ATAXIA; CLINICAL ARTICLE; CLINICAL FEATURE; CONTROLLED STUDY; DISEASE ASSOCIATION; ERROR BASED VISUOMOTOR LEARNING; FEMALE; HUMAN; LEARNING; MALE; MIDDLE AGED; MOTOR PERFORMANCE; NERVE CELL NETWORK; PRIORITY JOURNAL; PSYCHOLOGIC ASSESSMENT; SPINOCEREBELLAR ATAXIA TYPE 2; STRATEGIC BASED VISUOMOTOR LEARNING; TASK PERFORMANCE; VISUAL FIELD; VISUAL FIELD DISPLACEMENT; VISUAL FIELD INVERSION; VISUAL SYSTEM PARAMETERS; YOUNG ADULT;

ADAPTATION, PHYSIOLOGICAL; ADULT; BASAL GANGLIA; FEMALE; HUMANS; LEARNING DISORDERS; MALE; MIDDLE AGED; MOTOR ACTIVITY; PERCEPTUAL DISORDERS; PSYCHOMOTOR PERFORMANCE; SPINOCEREBELLAR ATAXIAS; VISUAL FIELDS; VISUAL PERCEPTION;

EID: 84892443562     PISSN: 14734222     EISSN: 14734230     Source Type: Journal    
DOI: 10.1007/s12311-013-0496-5     Document Type: Article

References (51)

1. Ohlsson S. Learning from performance errors. Psychol Rev. 1996;103:241-62.
2. Kawato M, Gomi H. The cerebellum and VOR/OKR learning models. Trends Neurosci. 1992;15(11):445-53.
3. Kornheiser AS. Adaptation to laterally displaced vision: a review. Psychol Bull. 1976;83(5):783-816.
4. Fernández-Ruiz J, Díaz R. Prism adaptation and aftereffect: specifying the properties of procedural memory system. Learn Mem. 1999;6(1):47-53.
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.
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.
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.
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.
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.
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.
12. Marotta JJ, Keith GP, Crawford JD. Task-specific sensorimotor adaptation to reversing prisms. J Neurophysiol. 2005;93(2):1104-10.
13. Taylor JA, Ivry RB. The role of strategies in motor learning. Ann N YAcad Sci. 2012;1251:1-12.
14. Redding GM, Wallace B. Adaptive spatial alignment and strategic perceptual-motor control. J Exp Psychol Hum Percept Perform. 1996;22(2):379-94.
15. Abdelghani MN, Lillicrap TP, Tweed DB. Sensitivity derivatives for flexible sensorimotor learning. Neural Comput. 2008;20(8):2085-111.
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.
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.
18. Maschke M, Gomez CM, Ebner TJ, Konczak J. Hereditary cerebellar ataxia progressively impairs force adaptation during goaldirected arm movements. J Neurophysiol. 2004;91(1):230-8.
19. Criscimagna-Hemminger SE, Bastian AJ, Shadmer R. Size of error affects cerebellar contributions to motor learning. J Neurophysiol. 2010;103(4):2275-84.
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 (Pt 4):1183-98.
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.
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.
23. Dueñas AM, Goold R, Giunti P. Molecular pathogenesis of spinocerebellar ataxias. Brain. 2006;129(Pt 6):1357-70.
24. Durr A. Autosomal dominant cerebellar ataxias: polyglutamine expansions and beyond. Lancet Neurol. 2010;9(9):885-94.
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.
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.
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.
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.
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.
30. Council for International Organizations of Medical Sciences. International ethical guidelines for biomedical research involving human subjects. Bull Med Ethics. 2002;182:17-23.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
41. Ramnani N. The primate cortico-cerebellar system anatomy and function. Nat Rev Neurosci. 2006;7(7):511-22.
42. Mazzoni P, Krakauer JW. An implicit plan overrides an explicit strategy during visuomotor adaptation. J Neurosci. 2006;26 (14):3642-5.
43. Fuster JM. Upper processing stages of the perception action cycle. Trends Cogn Sci. 2004;8(4):143-5.
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.
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.
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.
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.
48. Strick PL, Dum PL, Fiez JA. Cerebellum and nonmotor function. Annu Rev Neurosci. 2009;32:413-34.
49. Ito M. Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci. 2008;9(4):304-13.
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.
51. Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121(Pt 4):561-79.