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Differential effects of cerebellar degeneration on feedforward versus feedback control across speech and reaching movements

View ORCID ProfileBenjamin Parrell, View ORCID ProfileHyosub Kim, View ORCID ProfileAssaf Breska, Arohi Saxena, View ORCID ProfileRich Ivry
doi: https://doi.org/10.1101/2021.04.05.438454
Benjamin Parrell
1University of Wisconsin–Madison, Department of Communication Sciences & Disorders, Madison, WI, 53706, USA
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  • For correspondence: bparrell@wisc.edu
Hyosub Kim
2University of California, Berkeley, Department of Psychology, Berkeley, CD, 94720
3University of Delaware, Department of Physical Therapy, Newark, DE, 19713
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Assaf Breska
2University of California, Berkeley, Department of Psychology, Berkeley, CD, 94720
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Arohi Saxena
2University of California, Berkeley, Department of Psychology, Berkeley, CD, 94720
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Rich Ivry
2University of California, Berkeley, Department of Psychology, Berkeley, CD, 94720
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Abstract

Errors that result from a mismatch between predicted movement outcomes and sensory afference are used to correct ongoing movements through feedback control and to adapt feedforward control of future movements. The cerebellum has been identified as a critical part of the neural circuit underlying implicit adaptation across a wide variety of movements (reaching, gait, eye movements, and speech). The contribution of this structure to feedback control is less well understood: although it has recently been shown in the speech domain that individuals with cerebellar degeneration produce even larger online corrections for sensory perturbations than control participants, similar behavior has not been observed in other motor domains. Currently, comparisons across domains are limited by different population samples and potential ceiling effects in existing tasks. To assess the relationship between changes in feedforward and feedback control associated with cerebellar degeneration across motor domains, we evaluated adaptive (feedforward) and compensatory (feedback) responses to sensory perturbations in reaching and speech production in individuals with cerebellar degeneration and neurobiologically healthy controls. As expected, the cerebellar group demonstrated impaired adaptation in both reaching and speech. In contrast, the groups did not differ in their compensatory response in either domain. Moreover, compensatory and adaptive responses in the cerebellar group were not correlated within or across motor domains. Together, these results point to a general impairment in feedforward control with spared feedback control in cerebellar degeneration. However, the magnitude of feedforward impairments and potential changes in feedback-based control manifest in a domain-specific manner across individuals.

Significance Statement The cerebellum contributes to feedforward updating of movement in response to sensory errors, but its role in feedback control is less understood. Here, we tested individuals with cerebellar degeneration (CD), using sensory perturbations to assess adaptation of feedforward control and feedback gains during reaching and speech production tasks. The results confirmed that CD leads to reduced adaption in both domains. However, feedback gains were unaffected by CD in either domain. Interestingly, measures of feedforward and feedback control were not correlated across individuals within or across motor domains. Together, these results indicate a general impairment in feedforward control with spared feedback control in CD. However, the magnitude of feedforward impairments manifests in a domain-specific manner across individuals.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Conflict of interests: None of the authors has a conflict of interest to disclose.

Copyright 
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 April 06, 2021.
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Differential effects of cerebellar degeneration on feedforward versus feedback control across speech and reaching movements
Benjamin Parrell, Hyosub Kim, Assaf Breska, Arohi Saxena, Rich Ivry
bioRxiv 2021.04.05.438454; doi: https://doi.org/10.1101/2021.04.05.438454
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Differential effects of cerebellar degeneration on feedforward versus feedback control across speech and reaching movements
Benjamin Parrell, Hyosub Kim, Assaf Breska, Arohi Saxena, Rich Ivry
bioRxiv 2021.04.05.438454; doi: https://doi.org/10.1101/2021.04.05.438454

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