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Cerebellum Predicts the Future Motor State

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Abstract

Feed forward control and estimates of the future state of the motor system are critical for fast and coordinated movements. One framework for generating these predictive signals is based on the central nervous system implementing internal models. Internal models provide for representations of the input–output properties of the motor apparatus or their inverses. It has been widely hypothesized that the cerebellum acquires and stores internal models of the motor apparatus. The results of psychophysical, functional imaging and transcranial magnetic stimulation studies in normal subjects support this hypothesis. Also, the deficits in patients with cerebellar dysfunction can be attributed to a failure of predictive feed forward control and/or to accurately estimate the consequences of motor commands. Furthermore, the computation performed by the cerebellar-like electrosensory lobes in several groups of fishes is to predict the sensory consequences of motor commands. However, only a few electrophysiological investigations have directly tested whether neurons in the cerebellar cortex have the requisite signals compatible with either an inverse or forward internal model. Our studies in the monkey performing manual pursuit tracking demonstrate that the simple spike discharge of Purkinje cells does not have the dynamics-related signals required to be the output of an inverse dynamics model. However, Purkinje cell firing has several of the characteristics of a forward internal model of the arm. A synthesis of the evidence suggests that the cerebellum is involved in integrating the current state of the motor system with internally generated motor commands to predict the future state.

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References

  1. Bastian AJ (2006) Learning to predict the future: the cerebellum adapts feedforward movement control. Curr Opin Neurobiol 16(6):645–649

    Article  PubMed  CAS  Google Scholar 

  2. Bell CC (1981) An efference copy which is modified by reafferent input. Science 214(4519):450–453

    Article  PubMed  CAS  Google Scholar 

  3. Bell CC (1989) Sensory coding and corollary discharge effects in mormyrid electric fish. J Exp Biol 146:229–253

    PubMed  CAS  Google Scholar 

  4. Bell CC, Han V, Sawtell NB (2008) Cerebellum-like structures and their implications for cerebellar function. Annu Rev Neurosci 31:1–24

    Google Scholar 

  5. Bell CC, Han VZ, Sugawara Y, Grant K (1997) Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387(6630):278–281

    Article  PubMed  CAS  Google Scholar 

  6. Bloedel JR, Courville J (1981) A review of cerebellar afferent systems. In: Brooks VB (ed) Handbook of Physiology, Sect. 1, The Nervous System, Vol. II. Motor Control, Part 2. Williams and Wilkins, Baltimore, pp 735–830

    Google Scholar 

  7. Bodznick D, Montgomery JC, Carey M (1999) Adaptive mechanisms in the elasmobranch hindbrain. J Exp Biol 202(Pt 10):1357–1364

    PubMed  Google Scholar 

  8. Bursztyn LLCD, Ganesh G, Imamizu H, Kawato M, Flanagan JR (2006) Neural correlates of internal-model loading. Current Biology 16(24):2440–2445

    Article  PubMed  CAS  Google Scholar 

  9. Coltz JD, Johnson MT, Ebner TJ (1999) Cerebellar Purkinje cell simple spike discharge encodes movement velocity in primates during visuomotor arm tracking. J Neurosci 19(5):1782–1803

    PubMed  CAS  Google Scholar 

  10. Diedrichsen J, Hashambhoy Y, Rane T, Shadmehr R (2005) Neural correlates of reach errors. J Neurosci 25(43):9919–9931

    Article  PubMed  CAS  Google Scholar 

  11. Flanagan J, Wing AM (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(4):1519–1528

    PubMed  CAS  Google Scholar 

  12. Fu QG, Flament D, Coltz JD, Ebner TJ (1997) Relationship of cerebellar Purkinje cell simple spike discharge to movement kinematics in the monkey. J Neurophysiol 78(1):478–491

    PubMed  CAS  Google Scholar 

  13. Gomi H, Shidara M, Takemura A, Inoue Y, Kawano K, Kawato M (1998) Temporal firing patterns of Purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys I. Simple spikes. J Neurophysiol 80(2):818–831

    CAS  Google Scholar 

  14. Han VZ, Grant K, Bell CC (2000) Reversible associative depression and nonassociative potentiation at a parallel fiber synapse. Neuron 27(3):611–622

    Article  PubMed  CAS  Google Scholar 

  15. Horak FB, Diener HC (1994) Cerebellar control of postural scaling and central set in stance. J Neurophysiol 72(2):479–493

    PubMed  CAS  Google Scholar 

  16. Imamizu H, Miyauchi S, Tamada T, Sasaki Y, Takino R, Putz B, Yoshioka T, Kawato M (2000) Human cerebellar activity reflecting an acquired internal model of a new tool. Nature 403(6766):192–195

    Article  PubMed  CAS  Google Scholar 

  17. Johansson RS, Cole KJ (1992) Sensory-motor coordination during grasping and manipulative actions. Curr Opin Neurobiol 2(6):815–823

    Article  PubMed  CAS  Google Scholar 

  18. Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9(6):718–727

    Article  PubMed  CAS  Google Scholar 

  19. Kawato M, Kuroda T, Imamizu H, Nakano E, Miyauchi S, Yoshioka T (2003) Internal forward models in the cerebellum: fMRI study on grip force and load force coupling. Prog Brain Res 142:171–188

    Article  PubMed  Google Scholar 

  20. Kobayashi Y, Kawano K, Takemura A, Inoue Y, Kitama T, Gomi H, Kawato M (1998) Temporal firing patterns of Purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys II. Complex spikes. J Neurophysiol 80(2):832–848

    PubMed  CAS  Google Scholar 

  21. Lang CE, Bastian AJ (1999) Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol 82(5):2108–2119

    PubMed  CAS  Google Scholar 

  22. Leung HC, Suh M, Kettner RE (2000) Cerebellar flocculus and paraflocculus Purkinje cell activity during circular pursuit in monkey. J Neurophysiol 83(1):13–30

    PubMed  CAS  Google Scholar 

  23. Maschke M, Gomez CM, Ebner TJ, Konczak J (2004) Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. J Neurophysiol 91(1):230–238

    Article  PubMed  Google Scholar 

  24. Medina JF, Lisberger SG (2007) Variation, signal, and noise in cerebellar sensory-motor processing for smooth-pursuit eye movements. J Neurosci 27(25):6832–6842

    Article  PubMed  CAS  Google Scholar 

  25. Miall RC, Christensen LO, Cain O, Stanley J (2007) Disruption of state estimation in the human lateral cerebellum. PLoS Biol 5(11):e316

    Article  PubMed  Google Scholar 

  26. Miall RC, Weir DJ, Wolpert DM, Stein JF (1993) Is the cerebellum a Smith predictor? J Mot Behav 25(3):203–216

    PubMed  Google Scholar 

  27. Morton SM, Bastian AJ (2006) Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J Neurosci 26(36):9107–9116

    Article  PubMed  CAS  Google Scholar 

  28. Nixon PD, Passingham RE (2001) Predicting sensory events. The role of the cerebellum in motor learning. Exp Brain Res 138(2):251–257

    Article  PubMed  CAS  Google Scholar 

  29. Nowak DA, Hermsdorfer J, Rost K, Timmann D, Topka H (2004) Predictive and reactive finger force control during catching in cerebellar degeneration. Cerebellum 3(4):227–235

    Article  PubMed  Google Scholar 

  30. Ostry DJ, Feldman AG (2003) A critical evaluation of the force control hypothesis in motor control. Exp Brain Res 153(3):275–288

    Article  PubMed  Google Scholar 

  31. Pasalar S, Ebner TJ (2007) Invariant prediction of movement kinematics by Purkinje cell simple spike discharge [Abstract]. Soc Neurosci Abstr

  32. Pasalar S, Roitman AV, Durfee WK, Ebner TJ (2006) Force field effects on cerebellar Purkinje cell discharge with implications for internal models. Nat Neurosci 9:1404–1411

    Article  PubMed  CAS  Google Scholar 

  33. Paulin MG (2005) Evolution of the cerebellum as a neuronal machine for Bayesian state estimation. J Neural Eng 2(3):S219–S234

    Article  PubMed  CAS  Google Scholar 

  34. Pollok B, Gross J, Kamp D, Schnitzler A (2008) Evidence for anticipatory motor control within a cerebello-diencephalic-parietal network. J Cogn Neurosci 20(5):828–840

    Article  PubMed  Google Scholar 

  35. Roitman AV, Pasalar S, Johnson MT, Ebner TJ (2005) Position, direction of movement, and speed tuning of cerebellar Purkinje cells during circular manual tracking in monkey. J Neurosci 25(40):9244–9257

    Article  PubMed  CAS  Google Scholar 

  36. Schweighofer N, Arbib MA, Kawato M (1998) Role of the cerebellum in reaching movements in humans. I. Distributed inverse dynamics control. Eur J Neurosci 10(1):86–94

    Article  PubMed  CAS  Google Scholar 

  37. Shadmehr R, Holcomb HH (1997) Neural correlates of motor memory consolidation. Science 277(5327):821–825

    Article  PubMed  CAS  Google Scholar 

  38. Shadmehr R, Mussa-Ivaldi FA (1994) Adaptive representation of dynamics during learning of a motor task. J Neurosci 14:3208–3224

    PubMed  CAS  Google Scholar 

  39. Shidara M, Kawano K, Gomi H, Kawato M (1993) Inverse-dynamics model eye movement control by Purkinje cells in the cerebellum. Nature 365(6441):50–52

    Article  PubMed  CAS  Google Scholar 

  40. Smith MA, Shadmehr R (2005) Intact ability to learn internal models of arm dynamics in Huntington’s disease but not cerebellar degeneration. J Neurophysiol 93(5):2809–2821

    Article  PubMed  Google Scholar 

  41. Stein JF, Glickstein M (1992) Role of the cerebellum in visual guidance of movement. Physiol Rev 72(4):967–1017

    PubMed  CAS  Google Scholar 

  42. Thoroughman KA, Shadmehr R (1999) Electromyographic correlates of learning an internal model of reaching movements. J Neurosci 19(19):8573–8588

    PubMed  CAS  Google Scholar 

  43. Tseng YW, Diedrichsen J, Krakauer JW, Shadmehr R, Bastian AJ (2007) Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol 98:54–62

    Google Scholar 

  44. Wolpert DM, Miall RC, Kawato M (1998) Internal models in the cerebellum. Trends Cogn Sci 2:338–347

    Article  Google Scholar 

  45. Yamamoto K, Kawato M, Kotosaka S, Kitazawa S (2006) Encoding of movement dynamics by Purkinje cell simple spike activity during fast arm movements under resistive and assistive force fields. J Neurophysiol 97:1588–1599

    Article  PubMed  Google Scholar 

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Acknowledgements

We wish to thank Michael McPhee for graphics, and Kris Bettin for preparation of the manuscript. Supported in part by NIH grant R01-NS18338.

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  1. Department of Neuroscience, University of Minnesota, Minneapolis, MN, 55455, USA

    Timothy J. Ebner & Siavash Pasalar

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  1. Timothy J. Ebner
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  2. Siavash Pasalar
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Correspondence to Timothy J. Ebner.

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Ebner, T.J., Pasalar, S. Cerebellum Predicts the Future Motor State. Cerebellum 7, 583–588 (2008). https://doi.org/10.1007/s12311-008-0059-3

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