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The Cerebellum

, Volume 16, Issue 2, pp 427–437 | Cite as

Proprioceptive Localization Deficits in People With Cerebellar Damage

  • Heidi M. Weeks
  • Amanda S. Therrien
  • Amy J. BastianEmail author
Original Paper

Abstract

It has been hypothesized that an important function of the cerebellum is predicting the state of the body during movement. Yet, the extent of cerebellar involvement in perception of limb state (i.e., proprioception, specifically limb position sense) has yet to be determined. Here, we investigated whether patients with cerebellar damage have deficits when trying to locate their hand in space (i.e., proprioceptive localization), which is highly important for everyday movements. By comparing performance during passive robot-controlled and active self-made multi-joint movements, we were able to determine that some cerebellar patients show improved precision during active movement (i.e., active benefit), comparable to controls, whereas other patients have reduced active benefit. Importantly, the differences in patient performance are not explained by patient diagnosis or clinical ratings of impairment. Furthermore, a subsequent experiment confirmed that active deficits in proprioceptive localization occur during both single-joint and multi-joint movements. As such, it is unlikely that localization deficits can be explained by the multi-joint coordination deficits occurring after cerebellar damage. Our results suggest that cerebellar damage may cause varied impairments to different elements of proprioceptive sense. It follows that proprioceptive localization should be adequately accounted for in clinical testing and rehabilitation of people with cerebellar damage.

Keywords

Proprioception Upper extremity Cerebellum Ataxia 

Notes

Acknowledgments

We thank the members of the Center for Movement Studies at the Kennedy Krieger Institute for helping to coordinate experiments and the patients for volunteering their time to participate in these studies. This research was supported by National Institutes of Health grants R01 HD040289 to AJ Bastian, T32 EB003383 to N Thakor, and F31 NS086399 to HM Weeks.

Compliance with Ethical Standards

Ethics Statement

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed consent

This article does not contain any studies with animals performed by any of the authors. Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Ghez C, Sainburg R. Proprioceptive control of interjoint coordination. Can J Physiol Pharmacol. 1995;73:273–84.CrossRefPubMedGoogle Scholar
  2. 2.
    Bosco G, Poppele RE. Proprioception from a spinocerebellar perspective. Physiol Rev. 2001;81:539–68.PubMedGoogle Scholar
  3. 3.
    Proske U, Gandevia SC. The kinaesthetic senses. J Physiol. 2009;587:4139–46.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Proske U, Gandevia SC. The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiol Rev. 2012;92:1651–97.CrossRefPubMedGoogle Scholar
  5. 5.
    Thach WT, Goodkin HP, Keating JG. The cerebellum and the adaptive coordination of movement. Annu Rev Neurosci. 1992;15:403–42.CrossRefPubMedGoogle Scholar
  6. 6.
    Oscarsson O. Functional organization of the spino- and cuneocerebellar tracts. Physiol Rev. 1965;45:495–522.PubMedGoogle Scholar
  7. 7.
    Dum RP, Strick PL. An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J Neurophysiol. 2003;89:634–9.CrossRefPubMedGoogle Scholar
  8. 8.
    Strick PL, Dum RP, Fiez JA. Cerebellum and nonmotor function. Annu Rev Neurosci. 2009;32:413–34.CrossRefPubMedGoogle Scholar
  9. 9.
    Paulin MG. The role of the cerebellum in motor control and perception. Brain Behav Evol. 1993;41:39–50.CrossRefPubMedGoogle Scholar
  10. 10.
    Grill SE, Hallett M, Marcus C, McShane L. Disturbances of kinaesthesia in patients with cerebellar disorders. Brain. 1994;117:1433–47.CrossRefPubMedGoogle Scholar
  11. 11.
    Gao JH, Parsons LM, Bower JM, Xiong J, Li J, Fox PT. Cerebellum implicated in sensory acquisition and discrimination rather than motor control. Science. 1996;272:545–7.CrossRefPubMedGoogle Scholar
  12. 12.
    Hagura N, Oouchida Y, Aramaki Y, Okada T, Matsumura M, Sadato N, et al. Visuokinesthetic perception of hand movement is mediated by cerebro-cerebellar interaction between the left cerebellum and right parietal cortex. Cereb Cortex. 2009;19:176–86.CrossRefPubMedGoogle Scholar
  13. 13.
    Bhanpuri NH, Okamura AM, Bastian AJ. Predictive modeling by the cerebellum improves proprioception. J Neurosci. 2013;33:14301–6.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Bhanpuri NH, Okamura AM, Bastian AJ. Active force perception depends on cerebellar function. J Neurophysiol. 2012;107:1612–20.CrossRefPubMedGoogle Scholar
  15. 15.
    Maschke M, Gomez CM, Tuite PJ, Konczak J. Dysfunction of the basal ganglia, but not the cerebellum, impairs kinaesthesia. Brain. 2003;126:2312–22.CrossRefPubMedGoogle Scholar
  16. 16.
    Wolpert DM, Miall RC, Kawato M. Internal models in the cerebellum. Trends Cogn Sci. 1998;2:338–47.CrossRefPubMedGoogle Scholar
  17. 17.
    Miall RC, Christensen LOD, Cain O, Stanley J. Disruption of state estimation in the human lateral cerebellum. PLoS Biol. 2007;5:e316.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Synofzik M, Lindner A, Thier P. The cerebellum updates predictions about the visual consequences of one’s behavior. Curr Biol. 2008;18:814–8.CrossRefPubMedGoogle Scholar
  19. 19.
    Izawa J, Criscimagna-Hemminger SE, Shadmehr R. Cerebellar contributions to reach adaptation and learning sensory consequences of action. J Neurosci. 2012;32:4230–9.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Block HJ, Bastian AJ. Cerebellar involvement in motor but not sensory adaptation. Neuropsychologia. 2012;50:1766–75.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Paillard J, Brouchon M. Active and passive movements in the calibration of position sense. In: Freedman SJ, editor. The neuropsychology of spatially oriented behavior. Homewood, III: Dorsey Press; 1968. p. 37–55.Google Scholar
  22. 22.
    Adamovich SV, Berkinblit MB, Fookson O, Poizner H. Pointing in 3D space to remembered targets. I. Kinesthetic versus visual target presentation. J Neurophysiol. 1998;79:2833–46.PubMedGoogle Scholar
  23. 23.
    Fuentes CT, Bastian AJ. Where is your arm? Variations in proprioception across space and tasks. J Neurophysiol. 2010;103:164–71.CrossRefPubMedGoogle Scholar
  24. 24.
    Campbell W. DeJong’s the neurologic examination. Baltimore, MD: Lippincott Williams and Wilkins; 2005.Google Scholar
  25. 25.
    Thornbury JM, Mistretta CM. Tactile sensitivity as a function of age. J Gerontol. 1981;36:34–9.CrossRefPubMedGoogle Scholar
  26. 26.
    Trouillas P, Takayanagi T, Hallett M, Currier RD, Subramony SH, Wessel K, et al. International cooperative ataxia rating scale for pharmacological assessment of the cerebellar syndrome. The ataxia neuropharmacology Committee of the World Federation of neurology. J Neurol Sci. 1997;145:205–11.CrossRefPubMedGoogle Scholar
  27. 27.
    Desmurget M, Vindras P, Grea H, Viviani P, Grafton ST. Proprioception does not quickly drift during visual occlusion. Exp Brain Res. 2000;134:363–77.CrossRefPubMedGoogle Scholar
  28. 28.
    Johnson RA, Wichern DW. Applied multivariate statistical analysis. 6th ed. Pearson Prentice Hall: Upper Saddle River, NJ; 2007.Google Scholar
  29. 29.
    DiCiccio TJ, Efron B. Bootstrap confidence intervals. Stat Sci. 1996;11:189–228.CrossRefGoogle Scholar
  30. 30.
    Crowe A, Keessen W, Kuus W, Van Vliet R, Zegeling A. Proprioceptive accuracy in two dimensions. Percept Mot Skills. 1987;64:831–46.CrossRefPubMedGoogle Scholar
  31. 31.
    Wilson ET, Wong J, Gribble PL. Mapping proprioception across a 2D horizontal workspace. PLoS One. 2010;5:e11851.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Bastian AJ, Martin TA, Keating JG, Thach WT. Cerebellar ataxia: abnormal control of interaction torques across multiple joints. J Neurophysiol. 1996;76:492–509.PubMedGoogle Scholar
  33. 33.
    van Beers RJ, Sittig AC, Gon JJ. Integration of proprioceptive and visual position-information: an experimentally supported model. J Neurophysiol. 1999;81:1355–64.PubMedGoogle Scholar
  34. 34.
    van Beers RJ, Wolpert DM, Haggard P. When feeling is more important than seeing in sensorimotor adaptation. Curr Biol. 2002;12:834–7.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Heidi M. Weeks
    • 1
    • 2
  • Amanda S. Therrien
    • 2
    • 3
  • Amy J. Bastian
    • 2
    • 3
    Email author
  1. 1.Department of Biomedical EngineeringThe Johns Hopkins School of MedicineBaltimoreUSA
  2. 2.Kennedy Krieger InstituteBaltimoreUSA
  3. 3.Department of NeuroscienceThe Johns Hopkins School of MedicineBaltimoreUSA

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