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The Cerebellum and Implicit Sequencing: Evidence from Cerebellar Ataxia

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Abstract

The cerebellum recognizes sequences from prior experiences and uses this information to generate internal models that predict future outcomes in a feedforward manner [Front Hum Neurosci 8: 475, 2014; Cortex 47: 137–44, 2011; Cerebellum 7: 611–5, 2008; J Neurosci 26: 9107–16, 2006]. This process has been well documented in the motor domain, but the cerebellum’s role in cognitive sequencing, within the context of implicit versus explicit processes, is not well characterized. In this study, we tested individuals with cerebellar ataxia and healthy controls to clarify the role of the cerebellum sequencing using variations on implicit versus explicit and motor versus cognitive demands across five experiments. Converging results across these studies suggest that cerebellar feedforward mechanisms may be necessary for sequencing in the implicit domain only. In the ataxia group, rhythmic tapping, rate of motor learning, and implicit sequence learning were impaired. However, for cognitive sequencing that could be accomplished using explicit strategies, the cerebellar group performed normally, as though they shifted to extra-cerebellar mechanisms to compensate. For example, when cognitive and motor functions relied on cerebellar function simultaneously, the ataxia group’s motor function was unaffected, in contrast to that of controls whose motor performance declined as a function of cognitive load. These findings indicated that the cerebellum is not critical for all forms of sequencing per se. Instead, it plays a fundamental role for sequencing within the implicit domain, whether functions are motor or cognitive. Moreover, individuals with cerebellar ataxia are generally able to compensate for cognitive sequencing when explicit strategies are available in order to preserve resources for motor function.

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Acknowledgments

We thank Cyrus Eierud for an initial version of the task that was adapted here for Experiment 1, Leah Rubin for her statistical support of Experiment 2, Erin Hill for her assistance with Experiment 5, and Jason Creighton for his assistance with data collection in all experiments. We are extremely grateful to the National Ataxia Foundation for providing resources for testing at their 2018 and 2019 Annual Ataxia Conferences. Finally, we thank the volunteers, with and without ataxia, who contributed their valuable time and effort to this research.

Funding

Funding for this study was provided by the Gordon and Marilyn Macklin Foundation and the Margaret Q. Landenberger Foundation.

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Authors and Affiliations

  1. Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Owen P. Morgan, Mitchell B. Slapik, Katherine G. Iannuzzelli, Liana S. Rosenthal & Cherie L. Marvel

  2. Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA, USA

    Stephen M. LaConte & Jonathan M. Lisinski

  3. Department of Psychiatry, University of Iowa Carver College of Medicine, Iowa City, IA, USA

    Peg C. Nopoulos & Ashley M. Cochran

  4. Interdepartmental Neuroscience Program and the Department of Neurology, Yale University, New Haven, CT, USA

    Sharif I. Kronemer

  5. Baltimore, MD, 21205, USA

    Cherie L. Marvel

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  1. Owen P. Morgan
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Contributions

All authors contributed to the study conceptualization and design. Material preparation, data collection, and analyses were performed by Owen Morgan, Mitchell Slapik, Katherine Iannuzzelli, Ashley Cochran, Sharif Kronemer, and Cherie Marvel. The first draft of the manuscript was written by Owen Morgan, Mitchell Slapik, Katherine Iannuzzelli, and Cherie Marvel, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. Funding acquisition and resources were provided by Peg Nopoulos, Liana Rosenthal, and Cherie Marvel.

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Correspondence to Cherie L. Marvel.

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Morgan, O.P., Slapik, M.B., Iannuzzelli, K.G. et al. The Cerebellum and Implicit Sequencing: Evidence from Cerebellar Ataxia. Cerebellum 20, 222–245 (2021). https://doi.org/10.1007/s12311-020-01206-7

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