Skip to main content
Log in

Reinforcement Signaling Can Be Used to Reduce Elements of Cerebellar Reaching Ataxia

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

Abstract

Damage to the cerebellum causes a disabling movement disorder called ataxia, which is characterized by poorly coordinated movement. Arm ataxia causes dysmetria (over- or under-shooting of targets) with many corrective movements. As a result, people with cerebellar damage exhibit reaching movements with highly irregular and prolonged movement paths. Cerebellar patients are also impaired in error-based motor learning, which may impede rehabilitation interventions. However, we have recently shown that cerebellar patients can learn a simple reaching task using a binary reinforcement paradigm, in which feedback is based on participants’ mean performance. Here, we present a pilot study that examined whether patients with cerebellar damage can use this reinforcement training to learn a more complex motor task—to decrease the path length of their reaches. We compared binary reinforcement training to a control condition of massed practice without reinforcement feedback. In both conditions, participants made target-directed reaches in 3-dimensional space while vision of their movement was occluded. In the reinforcement training condition, reaches with a path length below participants’ mean were reinforced with an auditory stimulus at reach endpoint. We found that patients were able to use reinforcement signaling to significantly reduce their reach paths. Massed practice produced no systematic change in patients’ reach performance. Overall, our results suggest that binary reinforcement training can improve reaching movements in patients with cerebellar damage and the benefit cannot be attributed solely to repetition or reduced visual control.

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.

Fig. 1
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

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

    Article  Google Scholar 

  2. Bastian A, Thach W. Cerebellar outflow lesions: a comparison of movement deficits resulting from lesions at the levels of the cerebellum and thalamus. Ann Neurol. 1995;38:881–92.

    Article  CAS  Google Scholar 

  3. Bastian A, Martin T, Keating J, Thach W. Cerebellar ataxia: abnormal control of interaction torques across multiple joints. J Neurophysiol. 1996;76:492–509.

    Article  CAS  Google Scholar 

  4. Bhanpuri N, Okamura A, Bastian A. Predicting and correcting ataxia using a model of cerebellar function. Brain. 2014;137:1931–44.

    Article  Google Scholar 

  5. Therrien A, Bastian A. The cerebellum as a movement sensor. Neurosci Lett. 2018;688:37–40.

    Article  Google Scholar 

  6. Krakauer J, Pine Z, Ghilardi M, Ghez C. Learning of visuomotor transformations for vectorial planning of reaching trajectories. J Neurosci. 2000;20:8916–24.

    Article  CAS  Google Scholar 

  7. Shadmehr R, Smith M, Krakauer J. Error correction, sensory prediction, and adaptation in motor control. Neuroscience. 2010;33:89–108.

    CAS  Google Scholar 

  8. Weiner MJ, Hallett M, Funkenstein HH. Adaptation to lateral displacement of vision in patients with lesions of the central nervous system. Neurology. 1983;33:766–72.

    Article  CAS  Google Scholar 

  9. Martin T, Keating J, Goodkin H, Bastian A, Thach W. Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. Brain. 1996;119:1183–98.

    Article  Google Scholar 

  10. Maschke M, Gomez C, Ebner T, Konczak J. Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. J Neurophysiol. 2004;91:230–8.

    Article  Google Scholar 

  11. Smith M, Shadmehr R. Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degeneration. J Neurophysiol. 2005;93:2809–21.

    Article  Google Scholar 

  12. Tseng Y, Diedrichsen J, Krakauer J, Shadmehr R, Bastian A. Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol. 2007;98:54–62.

    Article  Google Scholar 

  13. Schlerf J, Xu J, Klemfuss N, Griffiths T, Ivry R. Individuals with cerebellar degeneration show similar adaptation deficits with large and small visuomotor errors. J Neurophysiol. 2013;109:1164–73.

    Article  Google Scholar 

  14. Therrien A, Wolpert D, Bastian A. Effective reinforcement learning following cerebellar damage requires a balance between exploration and motor noise. Brain. 2016. 2016;139:101–14.

    Article  Google Scholar 

  15. Izawa J, Criscimagna-Hemminger S, Shadmehr R. Cerebellar contributions to reach adaptation and learning sensory consequences of action. J Neurosci. 2012;32:4230–9.

    Article  CAS  Google Scholar 

  16. Sutton RS, Barto G. An introduction to reinforcement learning. Cambridge: MIT Press; 1998.

    Book  Google Scholar 

  17. Lee D, Seo H, Jung M. Neural basis of reinforcement learning and decision making. Ann Rev Neurosci. 2012;35:287–308.

    Article  CAS  Google Scholar 

  18. Izawa J, Shadmehr R. Learning from sensory and reward prediction errors during motor adaptation. PLoS Comp Biol. 2011;7:e1002012.

    Article  CAS  Google Scholar 

  19. Trouillas P, Takayanagi T, Hallett M, Currier R, Subramony S, Wessel K, et al. International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome. J Neurol Sci. 1997;145:205–11.

    Article  CAS  Google Scholar 

  20. Bastian A. Learning to predict the future: the cerebellum adapts feedforward movement control. Curr Opin Neurobiol. 2006;16:645–9.

    Article  CAS  Google Scholar 

  21. Zimmet A, Bastian A, Cowan N. Cerebellar patients have intact feedback control that can be leveraged to improve reaching. bioRxiv. 2019.

  22. Ilg W, Bastian A, Boesch S, Burciu R, Celnik P, Claasen J, et al. Consensus paper: management of degenerative cerebellar disorders. Cerebellum. 2014;13:248–68.

    Article  CAS  Google Scholar 

  23. Uehara S, Mawase F, Therrien A, Cherry-Allen K, Celnik P. Interactions between motor exploration and reinforcement learning. J Neurophysiol. 2019;122:797–808.

    Article  Google Scholar 

  24. Cashaback J, McGregor H, Mohatarem A, Gribble P. Dissociating error-based and reinforcement-based loss functions during sensorimotor learning. PLOS Comp Biol. 2017;13:e1005623.

    Article  Google Scholar 

  25. Wong A, Marvel C, Taylor J, Krakauer J. Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits? bioRxiv. 2018.

  26. Beppu H, Suda M, Tanaka R. Analysis of cerebellar motor disorders by visually guided elbow tracking movement. Brain. 1984;107:787–809.

    Article  Google Scholar 

  27. Day B, Thompson P, Harding A, Marsden C. Influence of vision on upper limb reaching movements in patients with cerebellar ataxia. Brain. 1998;121:357–72.

    Article  Google Scholar 

  28. Miall R, Christensen L, Cain O, Stanley J. Disruption of state estimation in the human lateral cerebellum. PLoS Biol. 2007;5:e316.

    Article  Google Scholar 

  29. Mazzoni P, Krakauer J. An implicit plan overrides an explicit strategy during visuomotor adaptation. J Neurosci. 2006;26:3642–5.

    Article  CAS  Google Scholar 

  30. Benson B, Anguera J, Seidler R. A spatial explicit strategy reduces error but interferes with sensorimotor adaptation. J Neurophysiol. 2011;105:2843–51.

    Article  Google Scholar 

  31. Taylor J, Ivry R. Flexible cognitive strategies during motor learning. PLoS Comp Biol. 2011;7:e1001096.

    Article  CAS  Google Scholar 

  32. McDougle S, Bond K, Taylor J. Explicit and implicit processes constitute the fast and slow processes of sensorimotor learning. J Neurosci. 2015;35:9568–79.

    Article  CAS  Google Scholar 

  33. Schween R, McDougle S, Hegele M, Taylor J. Assessing explicit strategies in force field adaptation. J Neurophysiol. 2020;123:1552–65.

    Article  Google Scholar 

  34. Codol O, Holland P, Galea J. The relationship between reinforcement and explicit control during visuomotor adaptation. Sci Rep. 2018;8:9121.

    Article  Google Scholar 

  35. Holland P, Codol O, Galea J. Contribution of explicit processes to reinforcement-based motor learning. J Neurophysiol. 2018;119:2241–55.

    Article  Google Scholar 

  36. Butcher P, Ivry R, Kuo S, Rydz D, Krakauer J, Taylor J. The cerebellum does more than sensory prediction error-based learning in sensorimotor adaptation tasks. J Neurophysiol. 2017;118:1622–36.

    Article  Google Scholar 

  37. McDougle S, Tsay J, Taylor J, Ivry R. Cerebellar degeneration selectively disrupts continuous mental operations in visual cognition. bioRxiv. 2020.

  38. Campbell WW. DeJong’s the neurologic examination. Baltimore: Lippincott Williams and Wilkins; 2005.

    Google Scholar 

Download references

Funding

This work was supported by the National Institute of Child Health and Human Development HD040289 to AJB and a Johns Hopkins Distinguished Science of Learning Fellowship to AST.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Amanda S. Therrien.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Therrien, A.S., Statton, M.A. & Bastian, A.J. Reinforcement Signaling Can Be Used to Reduce Elements of Cerebellar Reaching Ataxia. Cerebellum 20, 62–73 (2021). https://doi.org/10.1007/s12311-020-01183-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12311-020-01183-x

Keywords

Navigation