Skip to main content
Log in

Predictive and reactive finger force control during catching in cerebellar degeneration

  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

We investigated how patients with cerebellar degeneration control fingertip forces to resist a perturbation imposed on a handheld load. Patients and healthy sex- and age-matched control subjects held an instrumented receptacle between the index finger and thumb. A weight was dropped into the receptacle either unexpectedly from the experimenter’s hand with the subject being blindfolded or expectedly from the subject’s opposite hand. This paradigm allowed us to study predictive and reactive modes of finger force control. Patients generated an overshoot of grip force, irrespective of whether the weight was dropped expectedly or unexpectedly. When the weight was dropped from the experimenter’s hand, grip force lagged behind the load perturbation at impact in patients and controls. When the weight was dropped expectedly from the subject’s opposite hand, healthy subjects started to increase grip force prior to the release of the weight. This observation is indicative for a predictive mode of force control. In contrast, the grip force profile of cerebellar patients was not processed in anticipation of the time of impact when the weight was dropped from the opposite hand. Our data suggest involvement of cerebellar circuits in a predictive, but less in a reactive, mode of fingertip force control during manipulative behavior.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Flanagan JR, Johansson RS. Hand movements. In: VS Ramshan-dran, editor. Encyclopedia of the Human Brain, Vol 2. San Diego,: Academic Press, 2002: 399–414.

    Google Scholar 

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

    Google Scholar 

  3. 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 

  4. Wolpert DM, Flanagan JR. Motor prediction. Curr Biol 2001; 11: R729-R732.

    Article  PubMed  CAS  Google Scholar 

  5. Stein JF, Glickstein M. Role of the cerebellum in visual guidance of movement. Physiol Rev 1992; 72: 967–1017.

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  7. 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 

  8. Hermsdörfer J, Wessel K, Mai N, Marquardt C. Perturbation of precision grip in Friedreich’s ataxia and late-onset cerebellar ataxia. Mov Disord 1994; 9: 650–654.

    Article  PubMed  Google Scholar 

  9. Blakemore SJ, Frith CD, Wolpert DM. The cerebellum is involved in predicting the sensory consequences of action. Neuroreport 2001; 12: 1879–1884.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  11. 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 

  12. Dugas C, Smith AM. Responses of cerebellar Purkinje cells to slip of a hand-held object. J Neurophysiol 1992; 67: 483–495.

    PubMed  CAS  Google Scholar 

  13. 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 

  14. Smith AM, Dugas C, Fortier P, Kalaska J, Picard N. Comparing cerebellar and motor cortical activity in reaching and grasping. Can JNeurol Sci [Suppl] 1993; 3: S53-S61.

    Google Scholar 

  15. Monzee J, Smith AM. Responses of cerebellar interpositus neurons to predictable perturbations applied to an object held in a precision grip. J Neurophysiol 2004; 91: 1230–1239.

    Article  PubMed  Google Scholar 

  16. Trouillas P, Takayanagi T, Hallett M, Currier RD, Subramory SH, Wessel K, Bryer A, Diener HC, Massaquoi S, Gomez CM, Coutinho P, Ben Hamida M, Campanella G, Filla A, Schut L, Timmann D, Honnorat J, Nighoghossian N, Manyam B. Inter-national cooperative ataxia rating scale for pharmacological assessment of the cerebellar syndrome. The Ataxia Neuropharma-cology Committee of the World Federation of Neurology. J Neurol Sci 1997; 145: 205–211.

    Article  PubMed  CAS  Google Scholar 

  17. Nowak DA. Different modes of grip force control: Voluntary and externally guided arm movements with a hand-held load. Clin Neurophysiol 2004; 115: 839–848.

    Article  PubMed  Google Scholar 

  18. Holmes G. The symptoms of acute cerebellar injuries due to gunshot injuries. Brain 1917; 40: 461–535.

    Article  Google Scholar 

  19. Diener HC, Dichgans J. Pathophysiology of cerebellar ataxia. Mov Disord 1992; 7: 95–102.

    Article  PubMed  CAS  Google Scholar 

  20. Matthews PBCThe human stretch reflex and the motor cortex. Trends Neurosci 1991; 14: 87–91.

    Article  PubMed  CAS  Google Scholar 

  21. Jenner JR, Stephens JA. Cutaneous reflex responses and their central nervous pathways studied in man. J Physiol (London) 1982; 333: 405–419.

    CAS  Google Scholar 

  22. Macefield VG, Johansson RS. Loads applied tangential to a fingertip during an object restraint task can trigger short-latency as well as long-latency EMG responses in hand muscles. Exp Brain Res 2003; 152: 143–149.

    Article  PubMed  Google Scholar 

  23. 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 

  24. Topka H, Konczak J, Schneider K, Boose A, Dichgans J. Multijoint arm movements in cerebellar ataxia: Abnormal control of move-ment dynamics. Exp Brain Res 1998; 119: 493–503.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  26. Rao S, Harrington D, Haaland K, Bobholz J, Cox R, Binder J. Distributed neural systems underlying the timing of movements. J Neurosci 1997; 17: 5528–5535.

    PubMed  CAS  Google Scholar 

  27. 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. J Neurosci 1999; 19: 1446–1463.

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  29. Müller F, Dichgans J. Dyscoordination of pinch and lift forces during grasp in patients with cerebellar lesions. Exp Brain Res 1994; 101: 485–492.

    Article  PubMed  Google Scholar 

  30. Robertson LT, Grimm RJ. Responses of primate dentate nucleus to different trajectories of the limb. Exp Brain Res 1975; 23: 447–462.

    Article  PubMed  CAS  Google Scholar 

  31. 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: 939–959.

    PubMed  CAS  Google Scholar 

  32. 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: 537–544.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dennis A. Nowak.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nowak, D.A., Hermsdörfer, J., Rost, K. et al. Predictive and reactive finger force control during catching in cerebellar degeneration. Cerebellum 3, 227–235 (2004). https://doi.org/10.1080/14734220410019057

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1080/14734220410019057

Keywords

Navigation