The Cerebellum and Implicit Sequencing: Evidence from Cerebellar Ataxia

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ORIGINAL ARTICLE

The Cerebellum and Implicit Sequencing: Evidence from Cerebellar Ataxia Owen P. Morgan 1 & Mitchell B. Slapik 1 & Katherine G. Iannuzzelli 1 & Stephen M. LaConte 2 & Jonathan M. Lisinski 2 & Peg C. Nopoulos 3 & Ashley M. Cochran 3 & Sharif I. Kronemer 4 & Liana S. Rosenthal 1 & Cherie L. Marvel 1,5 Accepted: 20 October 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020

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. Keywords Ataxia . Cerebellum . Motor . Implicit . Explicit . Sequencing

General Introduction The cerebellum’s role in motor function has been well studied. Notably, it contributes to the timing and coordination of voluntary movements [1]. The cerebellum is uniform in structure, composed of “micro-modules” that include Purkinje cells and parallel fibers throughout the

entire structure. Accordingly, it is believed that the cerebellum is also uniform in its function [2]. Because the cerebellum interconnects with various cortical regions via the thalamus, function is determined by whether a cerebellar region communicates with motor or cognitive cortical regions to support motor or cortical functions, respectively [3–5].

Supplementary Information The online version contains supplementary material available at https: