The effect of Parkinson's disease and Huntington's disease on human visuomotor learning

European Journal of Neuroscience

Volumn 38, Issue 6, 2013, Pages 2933-2940

  Gutierrez Garralda, Juan Manuel ^a   Moreno Briseño, Pablo ^a   Boll, Marie Catherine ^b   Morgado Valle, Consuelo ^c   Campos Romo, Aurelio ^a   Diaz, Rosalinda ^a   Fernandez Ruiz, Juan ^a,c  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b NATIONAL INSTITUTE OF NEUROLOGY AND NEUROSURGERY   (Mexico)

^c UNIVERSIDAD VERACRUZANA   (Mexico)

Author keywords

Basal ganglia; Cerebellum; Huntington's disease; Learning dissociation; Parkinson's disease; Sensorimotor learning

Indexed keywords

ADULT; ARTICLE; BASAL GANGLION; CEREBELLUM; CLINICAL ARTICLE; CONTROLLED STUDY; DOVE PRISM; ERROR BASED LEARNING; EXTRAPYRAMIDAL SYNDROME; FEMALE; HUMAN; HUNTINGTON CHOREA; LEARNING; MALE; MOTOR PERFORMANCE; OUTCOME ASSESSMENT; PARKINSON DISEASE; PRIORITY JOURNAL; PRISM; SIGNAL TRANSDUCTION; VISUAL FEEDBACK; VISUOMOTOR COORDINATION; VISUOMOTOR LEARNING; WEDGE PRISM;

EID: 84884704674     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12288     Document Type: Article

References (59)

1. Abdelghani, M.N., Lillicrap, T.P. & Tweed, D.B. (2008) Sensitivity derivatives for flexible sensorimotor learning. Neural Comput., 20, 2085-2111.
2. Alexander, G.E. & Crutcher, M.D. (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci., 13, 266-271.
3. Aretouli, E. & Brandt, J. (2010) Episodic memory in dementia: Characteristics of new learning that differentiate Alzheimer's, Huntington's, and Parkinson's diseases. Arch. Clin. Neuropsych., 25, 396-409.
4. Braak, H., Braak, E., Yilmazer, D., de Vos, R.A., Jansen, E.N. & Bohl, J. (1996) Pattern of brain destruction in Parkinson's and Alzheimer's diseases. J. Neural Transm., 103, 455-490.
5. Contreras-Vidal, J.L. & Buch, E.R. (2003) Effects of Parkinson's disease on visuomotor adaptation. Exp. Brain Res., 150, 25-32.
6. Damier, P., Hirsch, E.C., Agid, Y. & Graybiel, A.M. (1999) The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain, 122, 1437-1448.
7. DeLong, M.R. (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci., 13, 281-285.
8. Dezfouli, A. & Balleine, B.W. (2012) Habits, action sequences and reinforcement learning. Eur. J. Neurosci., 35, 1036-1051.
9. Doya, K. (2000) Complementary roles of basal ganglia and cerebellum in learning and motor control. Curr. Opin. Neurobiol., 10, 732-739.
10. Doya, K. (2007) Reinforcement learning: computational theory and biological mechanisms. HFSP J., 1, 30-40.
11. Doyon, J., Gaudreau, D., Laforce, R. Jr., Castonguay, M., Bedard, P.J., Bedard, F. & Bouchard, J.P. (1997) Role of the striatum, cerebellum, and frontal lobes in the learning of a visuomotor sequence. Brain Cognition, 34, 218-245.
12. Doyon, J., Penhune, V. & Ungerleider, L.G. (2003) Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia, 41, 252-262.
13. Fernandez-Ruiz, J. & Diaz, R. (1999) Prism adaptation and aftereffect: specifying the properties of a procedural memory system. Learn. Memory, 6, 47-53.
14. Fernandez-Ruiz, J., Wang, J., Aigner, T.G. & Mishkin, M. (2001) Visual habit formation in monkeys with neurotoxic lesions of the ventrocaudal neostriatum. Proc. Natl. Acad. Sci. USA, 98, 4196-4201.
15. Fernandez-Ruiz, J., Diaz, R., Hall-Haro, C., Vergara, P., Mischner, J., Nunez, L., Drucker-Colin, R., Ochoa, A. & Alonso, M.E. (2003) Normal prism adaptation but reduced after-effect in basal ganglia disorders using a throwing task. Eur. J. Neurosci., 18, 689-694.
16. Fernandez-Ruiz, J., Velasquez-Perez, L., Diaz, R., Drucker-Colin, R., Perez-Gonzalez, R., Canales, N., Sanchez-Cruz, G., Martinez-Gongora, E., Medrano, Y., Almaguer-Mederos, L., Seifried, C. & Auburger, G. (2007) Prism adaptation in spinocerebellar ataxia type 2. Neuropsychologia, 45, 2692-2698.
17. Fernandez-Ruiz, J., Wong, W., Armstrong, I.T. & Flanagan, J.R. (2011) Relation between reaction time and reach errors during visuomotor adaptation. Behav. Brain Res., 219, 8-14.
18. Fiez, J.A., Petersen, S.E., Cheney, M.K. & Raichle, M.E. (1992) Impaired non-motor learning and error detection associated with cerebellar damage. A single case study. Brain, 115, 155-178.
19. Flanagan, J.R. & Wing, A.M. (1997) The role of internal models in motion planning and control: evidence from grip force adjustments during movements of hand-held loads. J. Neurosci., 17, 1519-1528.
20. Frank, M.J., Seeberger, L.C. & O'Reilly, R.C. (2004) By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science, 306, 1940-1943.
21. Grahn, J.A., Parkinson, J.A. & Owen, A.M. (2009) The role of the basal ganglia in learning and memory: neuropsychological studies. Behav. Brain Res., 199, 53-60.
22. Graybiel, A.M. (2005) The basal ganglia: learning new tricks and loving it. Curr. Opin. Neurobiol., 15, 638-644.
23. Graybiel, A.M., Aosaki, T., Flaherty, A.W. & Kimura, M. (1994) The basal ganglia and adaptive motor control. Science, 265, 1826-1831.
24. Harrington, D.L., Haaland, K.Y., Yeo, R.A. & Marder, E. (1990) Procedural memory in Parkinson's disease: impaired motor but not visuoperceptual learning. J. Clin. Exp. Neuropsyc., 12, 323-339.
25. Haruno, M., Kuroda, T., Doya, K., Toyama, K., Kimura, M., Samejima, K., Imamizu, H. & Kawato, M. (2004) A neural correlate of reward-based behavioral learning in caudate nucleus: a functional magnetic resonance imaging study of a stochastic decision task. J. Neurosci., 24, 1660-1665.
26. Heindel, W.C., Butters, N. & Salmon, D.P. (1988) Impaired learning of a motor skill in patients with Huntington's disease. Behav. Neurosci., 102, 141-147.
27. Heindel, W.C., Salmon, D.P., Shults, C.W., Walicke, P.A. & Butters, N. (1989) Neuropsychological evidence for multiple implicit memory systems: a comparison of Alzheimer's, Huntington's, and Parkinson's disease patients. J. Neurosci., 9, 582-587.
28. Huang, V.S., Haith, A., Mazzoni, P. & Krakauer, J.W. (2011) Rethinking motor learning and savings in adaptation paradigms: model-free memory for successful actions combines with internal models. Neuron, 70, 787-801.
29. Ito, M. & Doya, K. (2011) Multiple representations and algorithms for reinforcement learning in the cortico-basal ganglia circuit. Curr. Opin. Neurobiol., 21, 368-373.
30. Izawa, J. & Shadmehr, R. (2011) Learning from sensory and reward prediction errors during motor adaptation. PLoS Comput. Biol., 7, e1002012.
31. Jenkins, I.H., Brooks, D.J., Nixon, P.D., Frackowiak, R.S. & Passingham, R.E. (1994) Motor sequence learning: a study with positron emission tomography. J. Neurosci., 14, 3775-3790.
32. Jueptner, M., Frith, C.D., Brooks, D.J., Frackowiak, R.S. & Passingham, R.E. (1997) Anatomy of motor learning. II. Subcortical structures and learning by trial and error. J. Neurophysiol., 77, 1325-1337.
33. Krakauer, J.W. (2009) Motor learning and consolidation: the case of visuomotor rotation. Adv. Exp. Med. Biol., 629, 405-421.
34. Lambrecq, V., Langbour, N., Guehl, D., Bioulac, B., Burbaud, P. & Rotge, J.Y. (2013) Evolution of brain gray matter loss in Huntington's disease: a meta-analysis. Eur. J. Neurol., 20, 315-321.
35. Lillicrap, T.P., Moreno-Briseno, P., Diaz, R., Tweed, D.B., Troje, N. & Fernandez-Ruiz, J. (2013) Adapting to inversion of the visual field: a new twist on an old problem. Exp. Brain Res., doi: 10.1007/s00221-013-3565-6 [Epub ahead of print].
36. Litvan, I., Paulsen, J.S., Mega, M.S. & Cummings, J.L. (1998) Neuropsychiatric assessment of patients with hyperkinetic and hypokinetic movement disorders. Arch. Neurol., 55, 1313-1319.
37. Marinelli, L., Crupi, D., Di Rocco, A., Bove, M., Eidelberg, D., Abbruzzese, G. & Ghilardi, M.F. (2009) Learning and consolidation of visuo-motor adaptation in Parkinson's disease. Parkinsonism Relat. D., 15, 6-11.
38. Martin, T.A., Keating, J.G., Goodkin, H.P., Bastian, A.J. & Thach, W.T. (1996a) Throwing while looking through prisms. 2. Specificity and storage of multiple gaze-throw calibrations. Brain, 119, 1199-1211.
39. Martin, T.A., Keating, J.G., Goodkin, H.P., Bastian, A.J. & Thach, W.T. (1996b) Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. Brain, 119, 1183-1198.
40. Moreno-Briseno, P., Diaz, R., Campos-Romo, A. & Fernandez-Ruiz, J. (2010) Sex-related differences in motor learning and performance. Behav. Brain Funct., 6, 74.
41. Murray, E.A., Bussey, T.J. & Wise, S.P. (2000) Role of prefrontal cortex in a network for arbitrary visuomotor mapping. Exp. Brain Res., 133, 114-129.
42. Owen, A.M., James, M., Leigh, P.N., Summers, B.A., Marsden, C.D., Quinn, N.P., Lange, K.W. & Robbins, T.W. (1992) Fronto-striatal cognitive deficits at different stages of parkinsons-disease. Brain, 115, 1727-1751.
43. Packard, M.G. & Knowlton, B.J. (2002) Learning and memory functions of the basal ganglia. Annu. Rev. Neurosci., 25, 563-593.
44. Palminteri, S., Lebreton, M., Worbe, Y., Hartmann, A., Lehericy, S., Vidailhet, M., Grabli, D. & Pessiglione, M. (2011) Dopamine-dependent reinforcement of motor skill learning: evidence from Gilles de la Tourette syndrome. Brain, 134, 2287-2301.
45. Pasupathy, A. & Miller, E.K. (2005) Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature, 433, 873-876.
46. Pereira, J.B., Ibarretxe-Bilbao, N., Marti, M.J., Compta, Y., Junque, C., Bargallo, N. & Tolosa, E. (2012) Assessment of cortical degeneration in patients with Parkinson's disease by voxel-based morphometry, cortical folding, and cortical thickness. Hum. Brain Mapp., 33, 2521-2534.
47. Redgrave, P., Prescott, T.J. & Gurney, K. (1999) The basal ganglia: a vertebrate solution to the selection problem? Neuroscience, 89, 1009-1023.
48. Rosas, H.D., Hevelone, N.D., Zaleta, A.K., Greve, D.N., Salat, D.H. & Fischl, B. (2005) Regional cortical thinning in preclinical Huntington disease and its relationship to cognition. Neurology, 65, 745-747.
49. Schultz, W., Tremblay, L. & Hollerman, J.R. (2000) Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb. Cortex, 10, 272-284.
50. Shadmehr, R., Smith, M.A. & Krakauer, J.W. (2010) Error correction, sensory prediction, and adaptation in motor control. Annu. Rev. Neurosci., 33, 89-108.
51. Shohamy, D., Myers, C.E., Grossman, S., Sage, J., Gluck, M.A. & Poldrack, R.A. (2004) Cortico-striatal contributions to feedback-based learning: converging data from neuroimaging and neuropsychology. Brain, 127, 851-859.
52. Smith, M.A. & Shadmehr, R. (2005) Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degeneration. J. Neurophysiol., 93, 2809-2821.
53. Tam, C.W., Burton, E.J., McKeith, I.G., Burn, D.J. & O'Brien, J.T. (2005) Temporal lobe atrophy on MRI in Parkinson disease with dementia: a comparison with Alzheimer disease and dementia with Lewy bodies. Neurology, 64, 861-865.
54. Taylor, J.A. & Ivry, R.B. (2012) The role of strategies in motor learning. Ann. NY Acad. Sci., 1251, 1-12.
55. Toni, I. & Passingham, R.E. (1999) Prefrontal-basal ganglia pathways are involved in the learning of arbitrary visuomotor associations: a PET study. Exp. Brain Res., 127, 19-32.
56. Vonsattel, J.P., Myers, R.H., Stevens, T.J., Ferrante, R.J., Bird, E.D. & Richardson, E.P. Jr. (1985) Neuropathological classification of Huntington's disease. J. Neuropath. Exp. Neur., 44, 559-577.
57. Weiner, M.J., Hallett, M. & Funkenstein, H.H. (1983) Adaptation to lateral displacement of vision in patients with lesions of the central nervous system. Neurology, 33, 766-772.
58. Wolpert, D.M., Diedrichsen, J. & Flanagan, J.R. (2011) Principles of sensorimotor learning. Nat. Rev. Neurosci., 12, 739-751.
59. Yin, H.H. & Knowlton, B.J. (2006) The role of the basal ganglia in habit formation. Nat. Rev. Neurosci., 7, 464-476.