Skip to main content
SpringerLink
Log in

The role of the cerebellum for predictive control of grasping

  • Original Article
  • Scientific Papers
  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

Predictive control of grasping forces when manipulating objects in the environment is suggested to reflect internal models that capture the causal relationship between actions and their consequences. The anatomical correlate of predictive control of grasping within the central nervous system is not completely understood. One structure which has been related to the neural representation of internal models is the cerebellum. Given its stereotyped cytoarchitecture, the widespread connections with cortical and subcortical sensory-motor structures and the neural activity of cerebellar Purkinje cells during sensory-motor tasks, the cerebellum has long been considered to play a major role in the establishment and maintenance of sensory-motor representations related to voluntary movement. Such representations are necessary to predict the consequences of our own movements. Here we review theoretical concepts, electrophysiological, imaging and behavioural data suggesting the cerebellum to be the anatomical and functional correlate of internal models relevant for predictive control of grasping.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Brooks VB, Thach WT. Cerebellar control of posture and movement. In: Brooks VB, editor. Handbook of physiology, Section 1 : The nervous system, Vol. 2: Motor control, Part 2. Bethesda, MD: American Physiological Society; 1981. pp 877–946.

  2. Gilman S. The cerebellum: Its role in posture and movement. In: Swash M, Kennard C, editors. Scientific basis of clinical neurology. New York: Churchill Livingstone; 1985. pp 36–55.

    Google Scholar 

  3. Glickstein M, Yeo C. The cerebellum and motor learning. J Cogn Neurosci. 1990;2:69–80.

    Article  Google Scholar 

  4. Holmes G. The cerebellum of man. Brain. 1939;62:1–20.

    Article  Google Scholar 

  5. Miall RC, Weir DJ, Wolpert DM, Stein JF. Is the cerebellum a Smith predictor? J Motor Behav. 1993;25:203–16.

    Google Scholar 

  6. Kawato M. Internal models for motor control and trajectory planning. Curr Opin Neurobiol. 1999;9:718–27.

    Article  PubMed  CAS  Google Scholar 

  7. Imamizu H, Miyauchi S, Tamada T, Sasaki Y, Takino R, Putz B, Yoshiaka T, Kawato M. Human cerebellar activity reflecting an acquired internal model of a new tool. Nature. 2000;403:192–5.

    Article  PubMed  CAS  Google Scholar 

  8. Kitazawa S, Kimura T, Yin PB. Cerebellar complex spikes encode both destinations and errors in arm movements. Nature. 1998;392:494–7.

    Article  PubMed  CAS  Google Scholar 

  9. Ghez C, Gordon J. Voluntary movement. In: Kandel ER, Schwartz JH, Jessell TM, editors. Essentials of neural science and behavior. Connecticut: Appleton & Lange; 1995. pp 529–50.

    Google Scholar 

  10. Hoover J, Strick P. The organization of cerebellar and basal ganglia outputs to primary motor cortex as revealed by retrograde transneural transport of herpes simplex virus type I. JNeurosci. 1999;19:1446–63.

    CAS  Google Scholar 

  11. Allen GI, Tsukahara N. Cerebrocerebellar communication systems. Physiol Rev. 1974;54:957–1006.

    PubMed  CAS  Google Scholar 

  12. Gilbert PFC, Thach WT. Purkinje cell activity during motor learning. Brain Res. 1977;128:309–28.

    Article  PubMed  CAS  Google Scholar 

  13. Ito M. The cerebellum and neural control. New York: Raven Press, 1984.

    Google Scholar 

  14. Dugas C, Smith AM. Responses of cerebellar Purkinje cells to slip of a hand-held object. J Neurophysiol. 1992;67: 483–95.

    PubMed  CAS  Google Scholar 

  15. Espinoza E, Smith AM. Purkinje cell simple spike activity during grasping and lifting objects of different textures and weights. J Neurophysiol. 1990;64:698–714.

    PubMed  CAS  Google Scholar 

  16. Smith AM, Dugas C, Fortier P, Kalaska J, Picard N. Comparing cerebellar and motor cortical activity in reaching and grasping. Can J Neurol Sci. 1993;3(Suppl.): S53-S61.

    Google Scholar 

  17. Monzee J, Smith AM. Responses of cerebellar interpositus neurons to predictable perturbations applied to an object held in a precision grip. J Neurophysiol. 2004; 911230–9.

  18. Mason CR, Hendrix CM, Ebner TJ. Purkinje cells signal hand shape and grasp force during reach-to-grasp in the monkey. J Neurophysiol. 2006;95:144–58.

    Article  PubMed  Google Scholar 

  19. Wolpert DM, Miall RC, Kawato M. Internal models in the cerebellum. Trends Cogn Sci. 1998;2:338–47.

    Article  Google Scholar 

  20. Flanagan JR, Johansson RS. Hand movements. In: Ramshandran VS, editor. Encyclopedia of the human brain, Vol 2. San Diego: Academic Press; 2002. pp 399–414.

    Google Scholar 

  21. Kawato M, Kuroda T, Imamizu H, Nakano E, Miyauchi S, Yoshioka T. Internal forward models in the cerebellum: FMRI study on grip force and load force coupling. Progr Brain Res. 2003;142:171–88.

    Article  Google Scholar 

  22. Fellows SJ, Ernst J, Schwarz M, Töpper R, Noth J. Precision grip in cerebellar disorders in man. Clin Neurophysiol. 2001;112:1793–1802.

    Article  PubMed  CAS  Google Scholar 

  23. Blakemore SJ, Frith CD, Wolpert DM. The cerebellum is involved in predicting the sensory consequences of action. Neuroreport. 2001;12:1879–84.

    Article  PubMed  CAS  Google Scholar 

  24. Serrien JD, Wiesendanger M. Grip-load coordination in cerebellar patients. Exp Brain Res. 1999;128:76–80.

    Article  PubMed  CAS  Google Scholar 

  25. Nowak DA, Hermsdörfer J, Marquardt C, Fuchs HH. Grip and load force coupling during discrete vertical movements in cerebellar atrophy. Exp Brain Res. 2002;145: 28–39.

    Article  PubMed  Google Scholar 

  26. Nowak DA, Hermsdörfer J, Rost K, Timmann D, Topka H. Predictive and reactive finger force control during catching in cerebellar degeneration. Cerebellum. 2004;3:227–35.

    Article  PubMed  Google Scholar 

  27. Rost K, Nowak DA, Timmann D, Hermsdörfer J. Preserved and impaired aspects of predictive grip force control in cerebellar patients. Clin Neurophysiol. 2005;1 16:1405–14.

    Article  Google Scholar 

  28. Nowak DA, Hermsdörfer J, Timmann D, Rost K, Topka H. Impaired generalization of weight-related information in cerebellar degeneration. Neuropsychologia. 2005;43: 20–7.

    Article  PubMed  Google Scholar 

  29. Boecker H, Lee A, Mühlau M, Ceballos-Baumann AO, Ritzl A, Spilker M, Marquardt C, Hermsdörfer J. Force level independent representation of predictive grip force-load force coupling: a PET activation study. Neuroimage. 2005.

  30. Hermsdörfer J, Nowak DA, Lee A, Rost K, Timmann D, Mühlau M, Boecker H. The representation of predictive force control and internal forward models: evidence from lesion studies and brain imaging. Cogn Process. 2005;6: 48–58.

    Article  Google Scholar 

  31. Mehta B, Schaal S. Forward models in visuomotor control. J Neurophysiol. 2002;88:942–53.

    PubMed  Google Scholar 

  32. Gribble PL, Ostry DJ. Compensation for loads during arm movements using equilibrium point control. Exp Brain Res. 2000;135:474–82.

    Article  PubMed  CAS  Google Scholar 

  33. Kawato M, Furakawa K, Suzuki R. A hierachical neural network model for the control and learning of voluntary movements. Biol Cybern. 1984;56:1–17.

    Google Scholar 

  34. Gomi H, Shidara M, Takemura A, Inoue Y, Kawano K, Kawato M. Temporal firing patterns of Purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys I. Simple spikes. J Neurophysiol. 1998;80:818–31.

    PubMed  CAS  Google Scholar 

  35. Ostry DJ, Feldman AG. A critical evaluation of the force control hypothesis in motor control. Exp Brain Res. 2003;153:275–88.

    Article  PubMed  Google Scholar 

  36. Sommer MA, Wurtz RH. A pathway in primate brain for internal monitoring of movements. Science. 2002;296: 1480–2.

    Article  PubMed  CAS  Google Scholar 

  37. Johansson RS. Sensory control of dexterous manipulation in humans. In: Wing AM, Haggard P, Flanagan JR, editors. Hand and brain. San Diego: Academic Press; 1996. pp 381–414.

    Google Scholar 

  38. Johansson RS, Westling G. Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip. Exp Brain Res. 1988;71:59–71.

    PubMed  CAS  Google Scholar 

  39. Gordon A, Westling G, Cole K, Johansson R. Memory representation underlying motor commands used during manipulation of common and novel objects. J Neurophysiol. 1993;69:1789–96.

    PubMed  CAS  Google Scholar 

  40. Gordon AM. Visual size cues in the programming of manipulative forces during precision grip. Exp Brain Res. 1991;83:477–82.

    PubMed  CAS  Google Scholar 

  41. Gordon A, Forssberg H, Iwasaki N. Formation and lateralization of internal representations underlying motor commands during precision grip. Neuropsychologia. 1994;32: 555–68.

    Article  PubMed  CAS  Google Scholar 

  42. Wing AM. Anticipatory control of grip force in rapid arm movements. In: Wing AM, Haggard P, Flanagan JR, editors. Hand and brain. The neurophysiology and psychology of hand movements. San Diego: Academic Press; 1996. pp 301–28.

    Google Scholar 

  43. Flanagan JR, Tresilian JR. Grip-load force coupling: a general control strategy for transporting objects. J Exp Psychol Hum Percept Perform. 1994;20:944–57.

    Article  PubMed  CAS  Google Scholar 

  44. Wolpert DM, Flanagan JR. Motor prediction. Curr Biol. 2001;11:R729–32.

    Article  PubMed  CAS  Google Scholar 

  45. Diener HC, Dichgans J. Pathophysiology of cerebellar ataxia. MovDisord. 1992;7:95–102.

    Article  CAS  Google Scholar 

  46. Topka H, Konczak J, Schneider K, Boose A, Dichgans J. Multijoint arm movements in cerebellar ataxia: abnormal control of movement dynamics. Exp Brain Res. 1998;119: 493–503.

    Article  PubMed  CAS  Google Scholar 

  47. Bastian AJ, Martin TA, Keating JG, Thach WT. Cerebellar ataxia: abnormal control of interaction torques across mutiple joints. J Neurophysiol. 1996;76:492–509.

    PubMed  CAS  Google Scholar 

  48. Mason C, Miller L, Baker J, Houk J. Organization of reaching and grasping movements in the primate cerebellar nuclei as revealed by focal muscimol inactivations. J Neurophysiol. 1998;79:537–44.

    PubMed  CAS  Google Scholar 

  49. Johansson RS, Westling G. Programmed and triggered actions to rapid load changes during precision grip. Exp Brain Res. 1988;71:72–86.

    PubMed  CAS  Google Scholar 

  50. Diedrichsen J, Verstynen T, Lehman SL, Ivry RB. Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements. J Neurophysiol. 2005;93:801–12.

    Article  PubMed  Google Scholar 

  51. Rao S, Harrington D, Haaland K, Bobholz J, Cox R, Binder J. Distributed neural systems underlying the timing of movements. J Neurosci. 1997;17:5528–35.

    PubMed  CAS  Google Scholar 

  52. Lang CE, Bastian AJ. Additional somatosensory information does not improve cerebellar adaptation during catching. Clin Neurophysiol. 2001;112:895–907.

    Article  PubMed  CAS  Google Scholar 

  53. Smith AM. Does the cerebellum learn strategies for the optimal time-varying control of joint stiffness? Behav Brain Sci. 1996;19:399–410.

    Google Scholar 

  54. Robertson LT, Grimm RJ. Responses of primate dentate nucleus to different trajectories of the limb. Exp Brain Res. 1975;23:447–62.

    Article  PubMed  CAS  Google Scholar 

  55. Milak M, Shimansky Y, Bracha V, Bloedel J. Effects of inactivating individual cerebellar nuclei on the performance and retention of an operantly conditioned forelimb movement. J Neurophysiol. 1997;78:939–59.

    PubMed  CAS  Google Scholar 

  56. Imamizu H, Kuroda T, Miyauchi S, Yoshioka T, Kawato M. Modular organization of internal models of tools in the human cerebellum. Proc Natl Acad Sci USA. 2003;100:5461–6.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurology, University of Cologne and Institute of Medicine, Research Center Jülich, Germany

    Dennis A. Nowak (Priv.-Doz. Dr)

  2. Department of Neurology, Academic Hospital Bogenhausen, Technical University of Munich, Munich

    Helge Topka

  3. Department of Neurology, University of Duisburg-Essen, Essen

    Dagmar Timmann

  4. Department of Nuclear Medicine, Technical University of Munich, Munich

    Henning Boecker

  5. Neuropsychology Research Group, Department of Neuropsychology, Academic Hospital Bogenhausen, Technical University of Munich, Munich, Germany

    Joachim Hermsdörfer

Authors
  1. Dennis A. Nowak
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Helge Topka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dagmar Timmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Henning Boecker
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joachim Hermsdörfer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dennis A. Nowak.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nowak, D.A., Topka, H., Timmann, D. et al. The role of the cerebellum for predictive control of grasping. Cerebellum 6, 7–17 (2007). https://doi.org/10.1080/14734220600776379

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1080/14734220600776379

Key words

Search

Navigation