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Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits?

Aaron L. Wong, Cherie L. Marvel, Jordan A. Taylor, John W. Krakauer
doi: https://doi.org/10.1101/386466
Aaron L. Wong
1Moss Rehabilitation Research Institute, Elkins Park, PA 19027
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Cherie L. Marvel
2Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD 21287
3Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, MD 21287
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Jordan A. Taylor
4Department of Psychology, Princeton University, Princeton, NJ, 08544
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John W. Krakauer
2Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD 21287
5Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21287
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ABSTRACT

Systematic perturbations in motor adaptation tasks are primarily countered by learning from sensory-prediction errors, with secondary contributions from other learning processes. Despite the availability of these additional processes, particularly the use of explicit re-aiming to counteract observed target errors, patients with cerebellar degeneration are surprisingly unable to compensate for their sensory-prediction-error deficits by spontaneously switching to another learning mechanism. We hypothesized that if the nature of the task was changed – by allowing vision of the hand, which eliminates sensory-prediction errors – patients could be induced to preferentially adopt aiming strategies to solve visuomotor rotations. To test this, we first developed a novel visuomotor rotation paradigm that provides participants with vision of their hand in addition to the cursor, effectively setting the sensory-prediction-error signal to zero. We demonstrated in younger healthy controls that this promotes a switch to strategic re-aiming based on target errors. We then showed that with vision of the hand, patients with spinocerebellar ataxia could also switch to an aiming strategy in response to visuomotor rotations, performing similarly to age-matched participants (older controls). Moreover, patients could retrieve their learned aiming solution after vision of the hand was removed, and retain it for at least one year. Both patients and older controls, however, exhibited impaired overall adaptation performance compared to younger healthy controls (age, 18-33), likely due to age-related reductions in spatial and working memory. Moreover, patients failed to generalize, i.e., they were unable to adopt analogous aiming strategies in response to novel rotations, nor could they further improve their performance without vision of the hand. Hence, there appears to be an inescapable obligatory dependence on sensory-prediction-error-based learning – even when this system is impaired in patients with cerebellar degeneration. The persistence of sensory-prediction-error-based learning effectively suppresses a switch to target-error-based learning, which perhaps explains the unexpectedly poor performance by patients with spinocerebellar ataxia in visuomotor adaptation tasks.

Abbreviations
SPE
sensory-prediction error
TE
target error
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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted August 24, 2018.
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Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits?
Aaron L. Wong, Cherie L. Marvel, Jordan A. Taylor, John W. Krakauer
bioRxiv 386466; doi: https://doi.org/10.1101/386466
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Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits?
Aaron L. Wong, Cherie L. Marvel, Jordan A. Taylor, John W. Krakauer
bioRxiv 386466; doi: https://doi.org/10.1101/386466

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