The cerebellum does more than sensory prediction error-based learning in sensorimotor adaptation tasks

Peter A. Butcher, Richard B. Ivry, Sheng Han Kuo, David Rydz, John W. Krakauer, Jordan A. Taylor

Research output: Contribution to journalArticle

25 Scopus citations

Abstract

Individuals with damage to the cerebellum perform poorly in sensorimotor adaptation paradigms. This deficit has been attributed to impairment in sensory prediction error-based updating of an internal forward model, a form of implicit learning. These individuals can, however, successfully counter a perturbation when instructed with an explicit aiming strategy. This successful use of an instructed aiming strategy presents a paradox: In adaptation tasks, why do individuals with cerebellar damage not come up with an aiming solution on their own to compensate for their implicit learning deficit? To explore this question, we employed a variant of a visuomotor rotation task in which, before executing a movement on each trial, the participants verbally reported their intended aiming location. Compared with healthy control participants, participants with spinocerebellar ataxia displayed impairments in both implicit learning and aiming. This was observed when the visuomotor rotation was introduced abruptly (experiment 1) or gradually (experiment 2). This dual deficit does not appear to be related to the increased movement variance associated with ataxia: Healthy undergraduates showed little change in implicit learning or aiming when their movement feedback was artificially manipulated to produce similar levels of variability (experiment 3). Taken together the results indicate that a consequence of cerebellar dysfunction is not only impaired sensory prediction error-based learning but also a difficulty in developing and/or maintaining an aiming solution in response to a visuomotor perturbation. We suggest that this dual deficit can be explained by the cerebellum forming part of a network that learns and maintains action-outcome associations across trials. NEW & NOTEWORTHY Individuals with cerebellar pathology are impaired in sensorimotor adaptation. This deficit has been attributed to an impairment in error-based learning, specifically, from a deficit in using sensory prediction errors to update an internal model. Here we show that these individuals also have difficulty in discovering an aiming solution to overcome their adaptation deficit, suggesting a new role for the cerebellum in sensorimotor adaptation tasks.

Original languageEnglish (US)
Pages (from-to)1622-1636
Number of pages15
JournalJournal of neurophysiology
Volume118
Issue number3
DOIs
StatePublished - Sep 1 2017

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology

Keywords

  • Aiming
  • Cerebellum
  • Explicit learning
  • Implicit learning
  • Motor learning
  • Visuomotor rotation

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    Butcher, P. A., Ivry, R. B., Kuo, S. H., Rydz, D., Krakauer, J. W., & Taylor, J. A. (2017). The cerebellum does more than sensory prediction error-based learning in sensorimotor adaptation tasks. Journal of neurophysiology, 118(3), 1622-1636. https://doi.org/10.1152/jn.00451.2017