Learning to predict the future: the cerebellum adapts feedforward movement control

Current Opinion in Neurobiology

Volumn 16, Issue 6, 2006, Pages 645-649

  Bastian, Amy J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CEREBELLUM; ERROR; FEEDBACK SYSTEM; HUMAN; LEARNING; POSITIVE FEEDBACK; PREDICTION; PRIORITY JOURNAL; REVIEW; SENSORY SYSTEM; SIGNAL TRANSDUCTION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CEREBELLAR ATAXIA; CEREBELLUM; FEEDBACK; HUMANS; LEARNING; MOVEMENT; NEURAL PATHWAYS; PSYCHOMOTOR PERFORMANCE; VOLITION;

EID: 33751223820     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2006.08.016     Document Type: Review

References (36)

1. Marr D. A theory of cerebellar cortex. J Physiol 202 (1969) 437-470
2. Miall R.C. The cerebellum, predictive control and motor coordination. Novartis Found Symp 218 (1998) 272-284
3. Morton S.M., and Bastian A.J. Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J Neurosci 26 (2006) 9107-9116. This study shows impaired adaptation of predictive control, but normal reactive control, in people with cerebellar damage walking on a split belt treadmill. One important feature is that the predictive and reactive components are normally controlled simultaneously within the same walking task.
4. Maschke M., Gomez C.M., Ebner T.J., and Konczak J. Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. J Neurophysiol 91 (2004) 230-238
5. Smith M.A., and Shadmehr R. Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degeneration. J Neurophysiol 93 (2005) 2809-2821. This study shows that people with cerebellar damage are impaired in adapting predictive control of arm movements to a novel force environment. A particular strength of this study is that the authors show that people with Huntington's disease do not have this impairment.
6. Smith M.A., Brandt J., and Shadmehr R. Motor disorder in Huntington's disease begins as a dysfunction in error feedback control. Nature 403 (2000) 544-549
7. Day B.L., Thompson P.D., Harding A.E., and Marsden C.D. Influence of vision on upper limb reaching movements in patients with cerebellar ataxia. Brain 121 (1998) 357-372
8. Fisher B.E., Boyd L., and Winstein C.J. Contralateral cerebellar damage impairs imperative planning but not updating of aimed arm movements in humans. Exp Brain Res 174 (2006) 453-466
9. Lang C.E., and Bastian A.J. Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol 82 (1999) 2108-2119
10. Nowak D.A., Hermsdorfer J., Rost K., Timmann D., and Topka H. Predictive and reactive finger force control during catching in cerebellar degeneration. Cerebellum 3 (2004) 227-235
11. Horak F.B., and Diener H.C. Cerebellar control of postural scaling and central set in stance. J Neurophysiol 72 (1994) 479-493
12. Lasker A.G., Isotalo E.H., and Zee D.S. Predictive saccades to a regularly alternating target in cerebellar patients. Ann N Y Acad Sci 1039 (2005) 544-547
13. Diedrichsen J., Verstynen T., Lehman S.L., and Ivry R.B. Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements. J Neurophysiol 93 (2005) 801-812. This study shows that people with cerebellar damage can produce appropriate predictive postural adjustments when lifting a load out of one hand with the other, but they cannot make short-term adaptations of this bimanual behavior. Nor can they acquire a novel postural adjustment to a new trigger for lifting the load (e.g. a button press). A strength of this study is that the authors contrast cerebellar subject behavior with that of individuals with a corpus callosum transaction.
14. Beppu H., Suda M., and Tanaka R. Analysis of cerebellar motor disorders by visually guided elbow tracking movement. Brain 107 (1984) 787-809
15. Beppu H., Nagaoka M., and Tanaka R. Analysis of cerebellar motor disorders by visually-guided elbow tracking movement. 2. Contribution of the visual cues on slow ramp pursuit. Brain 110 (1987) 1-18
16. Vilis T., and Hore J. Central neural mechanisms contributing to cerebellar tremor produced by limb perturbations. J Neurophysiol 43 (1980) 279-291
17. Wolpert D.M., Miall R.C., and Kawato M. Internal models in the cerebellum. Trends Cogn Sci 2 (1998) 338-347
18. OhyamaT, Nores W.L., Murphy M., and Mauk M.D. What the cerebellum computes. Trends Neurosci 26 (2003) 222-227
19. Miall R.C., Weir D.J., Wolpert D.M., and Stein J.F. Is the cerebellum a Smith predictor?. J Mot Behav 25 (1993) 203-216
20. Wolpert D.M., Ghahramani Z., and Jordan M.I. An internal model for sensorimotor integration. Science 29 (1995) 1880-1882
21. Angelaki D.E., Shaikh A.G., Green A.M., and Dickman J.D. Neurons compute internal models of the physical laws of motion. Nature 430 (2004) 560-564
22. Blakemore S.J., Wolpert D.M., and Frith C.D. Central cancellation of self-produced tickle sensation. Nat Neurosci 1 (1998) 635-640
23. Shaikh A.G., Green A.M., Ghasia F.F., Newlands S.D., Dickman J.D., and Angelaki D.E. Sensory convergence solves a motion ambiguity problem. Curr Biol 15 (2005) 1657-1662
24. Paulin M.G. Evolution of the cerebellum as a neuronal machine for Bayesian state estimation. J Neural Eng 2 (2005) S219-S234
25. Miall R.C., and Jenkinson E.W. Functional imaging of changes in cerebellar activity related to learning during a novel eye-hand tracking task. Exp Brain Res 166 (2005) 170-183. The authors report on novel eye-hand tracking. The most striking result in this study is that the locus of cerebellar activation switched from an eye-specific site to an arm-specific site, depending on which effector was leading. Thus, the cerebellar contribution seemed to be making a prediction about the leading effector to guide the lagging effector.
26. Shidara M., Kawano K., Gomi H., and Kawato M. Inverse-dynamics model eye movement control by Purkinje cells in the cerebellum. Nature 365 (1993) 50-52
27. Schweighofer N., Arbib M.A., and Kawato M. Role of the cerebellum in reaching movements in humans. I. Distributed inverse dynamics control. Eur J Neurosci 10 (1998) 86-94
28. Spoelstra J., Schweighofer N., and Arbib M.A. Cerebellar learning of accurate predictive control for fast-reaching movements. Biol Cybern 82 (2000) 321-333
29. Wolpert D.M., and Kawato M. Multiple paired forward and inverse models for motor control. Neural Netw 11 (1998) 1317-1329
30. Seidler R.D., Noll D.C., and Thiers G. Feedforward and feedback processes in motor control. Neuroimage 22 (2004) 1775-1783
31. Diedrichsen J., Hashambhoy Y., Rane T., and Shadmehr R. Neural correlates of reach errors. J Neurosci 25 (2005) 9919-9931. This is an important study in which reaching errors were induced through random perturbations of the arm or through random movements of the target. Individuals performing the task appeared to interpret errors from arm perturbations as arising from a faulty motor command. They then made the appropriate feedforward correction on the subsequent reach. By contrast, when error was thought to be due to an external influence (i.e. moving the target), it did not drive feedforward cerebellar learning. This work also showed the surprising result that the locus of cerebellar activation is virtually identical for adaptations to force field and to those for visual rotations.
32. Robertson E.M., Pascual-Leone A., and Miall R.C. Current concepts in procedural consolidation. Nat Rev Neurosci 5 (2004) 576-582
33. Krakauer J.W., and Shadmehr R. Consolidation of motor memory. Trends Neurosci 29 (2006) 58-64
34. Kagerer F.A., Contreras-Vidal J.L., and Stelmach G.E. Adaptation to gradual as compared with sudden visuo-motor distortions. Exp Brain Res 115 (1997) 557-561
35. Malfait N., and Ostry D.J. Is interlimb transfer of force-field adaptation a cognitive response to the sudden introduction of load?. J Neurosci 24 (2004) 8084-8089
36. Yamamoto K, Hoffman DS, Strick PL: Rapid and long-lasting plasticity of input-output mapping. J Neurophysiol 2006, in press.