Learning fast accurate movements requires intact frontostriatal circuits

Frontiers in Human Neuroscience

Volumn , Issue NOV, 2013, Pages

  Shabbott, Britne ^a   Ravindran, Roshni ^a   Schumacher, Joseph W ^a   Wasserman, Paula B ^b,c   Marder, Karen S ^b,c   Mazzoni, Pietro ^a,b  

^a NEUROLOGICAL INSTITUTE   (United States)

^b Department of Medicine   (United States)

^c Vagelos College of Physicians and Surgeons   (United States)

Author keywords

Basal ganglia; Kinematics; Motor skill; Movement disorder; Neurodegenerative; Neurological; Reaching; Striatum

Indexed keywords

ADULT; AGED; ARTICLE; BASAL GANGLION; BRAIN FUNCTION; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DEGENERATIVE DISEASE; DISEASE SEVERITY; ENERGY EXPENDITURE; FEEDBACK SYSTEM; FEMALE; HUMAN; HUNTINGTON CHOREA; KINEMATICS; LEARNING; MALE; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOVEMENT PERCEPTION; RATING SCALE; TASK PERFORMANCE; VELOCITY;

EID: 84888122031     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00752     Document Type: Article

References (87)

1. Abeele, S., and Bock, O. (2001). Sensorimotor adaptation to rotated visual input: different mechanisms for small versus large rotations. Exp. Brain Res. 140, 407-410. doi: 10.1007/s002210100846
2. Akaike, H. (1974). A new look at the statistical model identification. IEEE Trans. Autom. Control 19, 716-723. doi: 10.1109/TAC.1974.1100705
3. Albin, R. L., Young, A. B., and Penney, J. B. (1989). The functional anatomy of basal ganglia disorders. Trends Neurosci. 12, 366-375. doi: 10.1016/0166-2236(89)90074-X
4. Alexander, G. E. (1994). Basal ganglia-thalamocortical circuits: their role in control of movements. J. Clin. Neurophysiol. 11, 420-431. doi: 10.1097/00004691-199407000-00004
5. Bedard, P., and Sanes, J. (2011). Basal ganglia-dependent processes in recalling learned visual-motor adaptations. Exp. Brain. Res. 209, 385-393. doi: 10.1007/s00221-011-2561-y
6. Biglan, K. M., Ross, C. A., Langbehn, D. R., Aylward, E. H., Stout, J. C., Queller, S., et al. (2009). Motor abnormalities in premanifest persons with Huntington's disease: the PREDICT-HD study. Mov. Disord. 24, 1763-1772. doi: 10.1002/mds.22601
7. Bonfiglioli, C., De Berti, G., Nichelli, P., Nicoletti, R., and Castiello, U. (1998). Kinematic analysis of the reach to grasp movement in Parkinson's and Huntington's disease subjects. Neuropsychologia 36, 1203-1208. doi: 10.1016/S0028-3932(97)00171-1
8. Boulet, C., Lemay, M., Bedard, M. A., Chouinard, M. J., Chouinard, S., and Richer, F. (2005). Early Huntington's disease affects movements in transformed sensorimotor mappings. Brain Cogn. 57, 236-243. doi: 10.1016/j.bandc.2004.09.001
9. Bradshaw, J. L., Phillips, J. G., Dennis, C., Mattingley, J. B., Andrewes, D., Chiu, E., et al. (1992). Initiation and execution of movement sequences in those suffering from and at-risk of developing Huntington's disease. J. Clin. Exp. Neuropsychol. 14, 179-192. doi: 10.1080/01688639208402822
10. Churchland, M. M., Afshar, A., and Shenoy, K. V. (2006). A central source of movement variability. Neuron 52, 1085-1096. doi: 10.1016/j.neuron.2006.10.034
11. Contreras-Vidal, J. L., and Buch, E. R. (2003). Effects of Parkinson's disease on visuomotor adaptation. Exp. Brain Res. 150, 25-32. doi: 10.1007/s00221-003-1403-y
12. De Boo, G. M., Tibben, A., Lanser, J. B., Jennekens-Schinkel, A., Hermans, J., Maat-Kievit, A., et al. (1997). Early cognitive and motor symptoms in identified carriers of the gene for Huntington disease. Arch. Neurol. 54, 1353-1357. doi: 10.1001/archneur.1997.00550230030012
13. Doyon, J., Bellec, P., Amsel, R., Penhune, V., Monchi, O., Carrier, J., et al. (2009). Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav. Brain Res. 199, 61-75. doi: 10.1016/j.bbr.2008.11.012
14. Eckart, M. T., Huelse-Matia, M. C., McDonald, R. S., and Schwarting, R. K. (2010). 6-hydroxydopamine lesions in the rat neostriatum impair sequential learning in a serial reaction time task. Neurotox. Res. 17, 287-298. doi: 10.1007/s12640-009-9103-4
15. Farrow, M., Chua, P., Churchyard, A., Bradshaw, J. L., Chiu, E., and Georgiou-Karistianis, N. (2006). Proximity to clinical onset influences motor and cognitive performance in presymptomatic Huntington disease gene carriers. Cogn. Behav. Neurol. 19, 208-216. doi: 10.1097/01.wnn.0000213914.64772.b6
16. Fernandez-Ruiz, J., Diaz, R., Hall-Haro, C., Vergara, P., Mischner, J., Nunez, L., et al. (2003). Normal prism adaptation but reduced after-effect in basal ganglia disorders using a throwing task. Eur. J. Neurosci. 18, 689-694. doi: 10.1046/j.1460-9568.2003.02785.x
17. Ferraro, F. R., Balota, D. A., and Connor, L. T. (1993). Implicit memory and the formation of new associations in nondemented Parkinson's disease individuals and individuals with senile dementia of the Alzheimer type: a serial reaction time (SRT) investigation. Brain Cogn. 21, 163-180. doi: 10.1006/brcg.1993.1013
18. Folstein, M. F., Folstein, S. E., and McHugh, P. R. (1975). "Mini-mental state. " A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12, 189-198. doi: 10.1016/0022-3956(75)90026-6
19. Gabrieli, J. D., Stebbins, G. T., Singh, J., Willingham, D. B., and Goetz, C. G. (1997). Intact mirror-tracing and impaired rotary-pursuit skill learning in patients with Huntington's disease: evidence for dissociable memory systems in skill learning. Neuropsychology 11, 272-281. doi: 10.1037/0894-4105.11.2.272
20. Georgiou, N., Phillips, J. G., Bradshaw, J. L., Cunnington, R., and Chiu, E. (1997). Impairments of movement kinematics in patients with Huntington's disease: a comparison with and without a concurrent task. Mov. Disord. 12, 386-396. doi: 10.1002/mds.870120318
21. Ghilardi, M. F., Silvestri, G., Feigin, A., Mattis, P., Zgaljardic, D., Moisello, C., et al. (2008). Implicit and explicit aspects of sequence learning in pre-symptomatic Huntington's disease. Parkinsonism Relat. Disord. 14, 457-464. doi: 10.1016/j.parkreldis.2007.11.009
22. Guthrie, E. R. (1952). The Psychology of Learning. New York, NY: Harper.
23. Hefter, H., Homberg, V., Lange, H. W., and Freund, H. J. (1987). Impairment of rapid movement in Huntington's disease. Brain 110 (Pt 3), 585-612. doi: 10.1093/brain/110.3.585
24. Heindel, W. C., Butters, N., and Salmon, D. P. (1988). Impaired learning of a motor skill in patients with Huntington's disease. Behav. Neurosci. 102, 141-147. doi: 10.1037/0735-7044.102.1.141
25. Heindel, W. C., Salmon, D. P., Shults, C. W., Walicke, P. A., and 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.
26. Hosp, J. A., Pekanovic, A., Rioult-Pedotti, M. S., and Luft, A. R. (2011). Dopaminergic projections from midbrain to primary motor cortex mediate motor skill learning. J. Neurosci. 31, 2481-2487. doi: 10.1523/JNEUROSCI.5411-10.2011
27. Howe, M. W., Atallah, H. E., McCool, A., Gibson, D. J., and Graybiel, A. M. (2011). Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum. Proc. Natl. Acad. Sci. U.S.A. 108, 16801-16806. doi: 10.1073/pnas.1113158108
28. Huang, V. S., Haith, A., Mazzoni, P., and 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. doi: 10.1016/j.neuron.2011.04.012
29. Huntington Study Group. (1996). Unified huntington's disease rating scale: reliability and consistency. Mov. Disord. 11, 136-142. doi: 10.1002/mds.870110204
30. Jackson, G. M., Jackson, S. R., Harrison, J., Henderson, L., and Kennard, C. (1995). Serial reaction time learning and Parkinson's disease: evidence for a procedural learning deficit. Neuropsychologia 33, 577-593. doi: 10.1016/0028-3932(95)00010-Z
31. Jog, M. S., Kubota, Y., Connolly, C. I., Hillegaart, V., and Graybiel, A. M. (1999). Building neural representations of habits. Science 286, 1745-1749. doi: 10.1126/science.286.5445.1745
32. Kirkwood, S. C., Siemers, E., Bond, C., Conneally, P. M., Christian, J. C., and Foroud, T. (2000). Confirmation of subtle motor changes among presymptomatic carriers of the Huntington disease gene. Arch. Neurol. 57, 1040-1044. doi: 10.1001/archneur.57.7.1040
33. Kirkwood, S. C., Siemers, E., Stout, J. C., Hodes, M. E., Conneally, P. M., Christian, J. C., et al. (1999). Longitudinal cognitive and motor changes among presymptomatic Huntington disease gene carriers. Arch. Neurol. 56, 563-568. doi: 10.1001/archneur.56.5.563
34. Kleim, J. A., Barbay, S., and Nudo, R. J. (1998). Functional reorganization of the rat motor cortex following motor skill learning. J. Neurophysiol. 80, 3321-3325.
35. Knopman, D., and Nissen, M. J. (1991). Procedural learning is impaired in Huntington's disease: evidence from the serial reaction time task. Neuropsychologia 29, 245-254. doi: 10.1016/0028-3932(91)90085-M
36. Knowlton, B. J., Mangels, J. A., and Squire, L. R. (1996). A neostriatal habit learning system in humans. Science 273, 1399-1402. doi: 10.1126/science.273.5280.1399
37. Krakauer, J. W., and Mazzoni, P. (2011). Human sensorimotor learning: adaptation, skill, and beyond. Curr. Opin. Neurobiol. 21, 636-644. doi: 10.1016/j.conb.2011.06.012
38. Langbehn, D. R., Brinkman, R. R., Falush, D., Paulsen, J. S., and Hayden, M. R. (2004). A new model for prediction of the age of onset and penetrance for Huntington's disease based on CAG length. Clin. Genet. 65, 267-277. doi: 10.1111/j.1399-0004.2004.00241.x
39. Liu, Y. T., Mayer-Kress, G., and Newell, K. M. (2006). Qualitative and quantitative change in the dynamics of motor learning. J. Exp. Psychol. Hum. Percept. Perform. 32, 380-393. doi: 10.1037/0096-1523.32.2.380
40. Luft, A. R., and Buitrago, M. M. (2005). Stages of motor skill learning. Mol. Neurobiol. 32, 205-216. doi: 10.1385/MN:32:3:205
41. Marinelli, L., Crupi, D., Di Rocco, A., Bove, M., Eidelberg, D., Abbruzzese, G., et al. (2009). Learning and consolidation of visuo-motor adaptation in Parkinson's disease. Parkinsonism Relat. Disord. 15, 6-11. doi: 10.1016/j.parkreldis.2008.02.012
42. Marr, D. (1982). Vision. New York, NY: Freeman.
43. Marsden, C. D. (1982). The mysterious motor function of the basal ganglia: the Robert Wartenberg Lecture. Neurology 32, 514-539. doi: 10.1212/WNL.32.5.514
44. Mazzoni, P., and Krakauer, J. W. (2006). An implicit plan overrides an explicit strategy during visuomotor adaptation. J. Neurosci. 26, 3642-3645. doi: 10.1523/JNEUROSCI.5317-05.2006
45. Mazzoni, P., Hristova, A., and Krakauer, J. W. (2007). Why don't we move faster? Parkinson's disease, movement vigor, and implicit motivation. J. Neurosci. 27, 7105-7116. doi: 10.1523/JNEUROSCI.0264-07.2007
46. Mazzoni, P., and Wexler, N. S. (2009). Parallel explicit and implicit control of reaching. PLoS ONE 4:e7557. doi: 10.1371/journal.pone.0007557
47. Metz, G. A., Antonow-Schlorke, I., and Witte, O. W. (2005). Motor improvements after focal cortical ischemia in adult rats are mediated by compensatory mechanisms. Behav. Brain Res. 162, 71-82. doi: 10.1016/j.bbr.2005.03.002
48. Miyachi, S., Hikosaka, O., Miyashita, K., Karadi, Z., and Rand, M. K. (1997). Differential roles of monkey striatum in learning of sequential hand movement. Exp. Brain Res. 115, 1-5. doi: 10.1007/PL00005669
49. Monchi, O., Petrides, M., Strafella, A. P., Worsley, K. J., and Doyon, J. (2006). Functional role of the basal ganglia in the planning and execution of actions. Ann. Neurol. 59, 257-264. doi: 10.1002/ana.20742
50. Newell, K. M., and Vaillancourt, D. E. (2001). Dimensional change in motor learning. Hum. Mov. Sci. 20, 695-715. doi: 10.1016/S0167-9457(01)00073-2
51. Nissen, M., and Bullemer, P. (1987). Attentional requirements of learning: evidence from performance measures. Cogn. Psychol. 19, 1-32. doi: 10.1016/0010-0285(87)90002-8
52. Nudo, R. J., Wise, B. M., Sifuentes, F., and Milliken, G. W. (1996). Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 272, 1791-1794. doi: 10.1126/science.272.5269.1791
53. Orban, P., Peigneux, P., Lungu, O., Albouy, G., Breton, E., Laberenne, F., et al. (2010). The multifaceted nature of the relationship between performance and brain activity in motor sequence learning. Neuroimage 49, 694-702. doi: 10.1016/j.neuroimage.2009.08.055
54. Pascual-Leone, A., Grafman, J., Clark, K., Stewart, M., Massaquoi, S., Lou, J. S., et al. (1993). Procedural learning in Parkinson's disease and cerebellar degeneration. Ann. Neurol. 34, 594-602. doi: 10.1002/ana.410340414
55. Paulsen, J. S., Hayden, M., Stout, J. C., Langbehn, D. R., Aylward, E., Ross, C. A., et al. (2006). Preparing for preventive clinical trials: the Predict-HD study. Arch. Neurol. 63, 883-890. doi: 10.1001/archneur.63.6.883
56. Pillai, J. A., Hansen, L. A., Masliah, E., Goldstein, J. L., Edland, S. D., and Corey-Bloom, J. (2012). Clinical severity of Huntington's disease does not always correlate with neuropathologic stage. Mov. Disord. 27, 1099-1103. doi: 10.1002/mds.25026
57. Plamondon, R., and Alimi, A. M. (1997). Speed/accuracy trade-offs in target-directed movements. Behav. Brain Sci. 20, 279-303. discussion: 303-249. doi: 10.1017/S0140525X97001441
58. Quinn, L., Hamel, V., Flanagan, J. R., and Kaminski, T. R. (1997). Coordination of multijoint arm movements in Huntington's disease. J. Neurol. Rehab. 11, 47-60. doi: 10.1177/154596839701100108
59. Quinn, L., Reilmann, R., Marder, K., and Gordon, A. M. (2001). Altered movement trajectories and force control during object transport in Huntington's disease. Mov. Disord. 16, 469-480. doi: 10.1002/mds.1108
60. Rao, A. K., Muratori, L., Louis, E. D., Moskowitz, C. B., and Marder, K. S. (2008). Spectrum of gait impairments in presymptomatic and symptomatic Huntington's disease. Mov. Disord. 23, 1100-1107. doi: 10.1002/mds.21987
61. Reis, J., Schambra, H. M., Cohen, L. G., Buch, E. R., Fritsch, B., Zarahn, E., et al. (2009). Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc. Natl. Acad. Sci. U.S.A. 106, 1590-1595. doi: 10.1073/pnas.0805413106
62. Rosas, H. D., Liu, A. K., Hersch, S., Glessner, M., Ferrante, R. J., Salat, D. H., et al. (2002). Regional and progressive thinning of the cortical ribbon in Huntington's disease. Neurology 58, 695-701. doi: 10.1212/WNL.58.5.695
63. Ross, C. A., and Tabrizi, S. J. (2011). Huntington's disease: from molecular pathogenesis to clinical treatment. Lancet Neurol. 10, 83-98. doi: 10.1016/S1474-4422(10)70245-3
64. Sanes, J. N., Dimitrov, B., and Hallett, M. (1990). Motor learning in patients with cerebellar dysfunction. Brain 113, 103-120. doi: 10.1093/brain/113.1.103
65. Schmidt, R. A., and Lee, T. D. (2005). Motor Control and Learning: A Behavioral Emphasis. Champaign, IL: Human Kinetics.
66. Shadmehr, R., Smith, M. A., and Krakauer, J. W. (2010). Error correction, sensory prediction, and adaptation in motor control. Annu. Rev. Neurosci. 33, 89-108. doi: 10.1146/annurev-neuro-060909-153135
67. Shmuelof, L., and Krakauer, J. W. (2011). Are we ready for a natural history of motor learning? Neuron 72, 469-476. doi: 10.1016/j.neuron.2011.10.017
68. Shmuelof, L., Krakauer, J. W., and Mazzoni, P. (2012). How is a motor skill learned? Change and invariance at the levels of task success and trajectory control. J. Neurophysiol. 108, 578-594. doi: 10.1152/jn.00856.2011
69. Smith, M. A., Brandt, J., and Shadmehr, R. (2000). Motor disorder in Huntington's disease begins as a dysfunction in error feedback control. Nature 403, 544-549. doi: 10.1038/35000576
70. Smith, M. A., and 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. doi: 10.1152/jn.00943.2004
71. Soliveri, P., Brown, R. G., Jahanshahi, M., Caraceni, T., and Marsden, C. D. (1997). Learning manual pursuit tracking skills in patients with Parkinson's disease. Brain 120, 1325-1337. doi: 10.1093/brain/120.8.1325
72. Soliveri, P., Brown, R. G., Jahanshahi, M., and Marsden, C. D. (1992). Effect of practice on performance of a skilled motor task in patients with Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 55, 454-460. doi: 10.1136/jnnp.55.6.454
73. Surmeier, D. J., Ding, J., Day, M., Wang, Z., and Shen, W. (2007). D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci. 30, 228-235. doi: 10.1016/j.tins.2007.03.008
74. Tabrizi, S. J., Langbehn, D. R., Leavitt, B. R., Roos, R. A., Durr, A., Craufurd, D., et al. (2009). Biological and clinical manifestations of Huntington's disease in the longitudinal TRACK-HD study: cross-sectional analysis of baseline data. Lancet Neurol. 8, 791-801. doi: 10.1016/S1474-4422(09)70170-X
75. Thompson, P. D., Berardelli, A., Rothwell, J. C., Day, B. L., Dick, J. P., Benecke, R., et al. (1988). The coexistence of bradykinesia and chorea in Huntington's disease and its implications for theories of basal ganglia control of movement. Brain 111 (Pt 2), 223-244. doi: 10.1093/brain/111.2.223
76. Tseng, Y. W., Diedrichsen, J., Krakauer, J. W., Shadmehr, R., and Bastian, A. J. (2007). Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J. Neurophysiol. 98, 54-62. doi: 10.1152/jn.00266.2007
77. Venkatakrishnan, A., Banquet, J. P., Burnod, Y., and Contreras-Vidal, J. L. (2011). Parkinson's disease differentially affects adaptation to gradual as compared to sudden visuomotor distortions. Hum. Mov. Sci. 30, 760-769. doi: 10.1016/j.humov.2010.08.020
78. Verbessem, P., Op't Eijnde, B., Swinnen, S. P., Vangheluwe, S., Hespel, P., and Dom, R. (2002). Unimanual and bimanual voluntary movement in Huntington's disease. Exp. Brain Res. 147, 529-537. doi: 10.1007/s00221-002-1270-y
79. Vonsattel, J. P., Myers, R. H., Stevens, T. J., Ferrante, R. J., Bird, E. D., and Richardson, E. P. Jr. (1985). Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 44, 559-577. doi: 10.1097/00005072-198511000-00003
80. Welford, A. T. (1968). Fundamentals of Skill. London: Methuen.
81. Whishaw, I. Q., Alaverdashvili, M., and Kolb, B. (2008). The problem of relating plasticity and skilled reaching after motor cortex stroke in the rat. Behav. Brain Res. 192, 124-136. doi: 10.1016/j.bbr.2007.12.026
82. Wickens, J., and Kotter, R. (1995). "Cellular models of reinforcement, " in Models of Information Processing in the Basal Ganglia, eds J. C. Houk, J. L. Davis, and D. G. Beiser (Cambridge, MA: The MIT Press), 187-214.
83. Willingham, D. B. (1998). A neuropsychological theory of motor skill learning. Psychol. Rev. 105, 558-584. doi: 10.1037/0033-295X.105.3.558
84. Willingham, D. B., and Koroshetz, W. J. (1993). Evidence for dissociable motor skills in Huntington's disease patients. Psychobiology 21, 173-182.
85. Willingham, D. B., Koroshetz, W. J., and Peterson, E. W. (1996). Motor skills have diverse neural bases: spared and impaired skill acquisition in Huntington's disease. Neuropsychology 10, 315-321. doi: 10.1037/0894-4105.10.3.315
86. World Health Organization. (2001). International Classification of Functioning, Disability and Health (ICF). Geneva: World Health Organization.
87. Yin, H. H., and Knowlton, B. J. (2006). The role of the basal ganglia in habit formation. Nat. Rev. Neurosci. 7, 464-476. doi: 10.1038/nrn1919