Anti-Saccades in Cerebellar Ataxias Reveal a Contribution of the Cerebellum in Executive Functions.

Elena Pretegiani,Antonio Federico,Pamela Federighi,Alessandra Rufa,Maria Teresa Dotti,Gemma Tumminelli,Pietro Piu,Valeria Serchi,Francesca Rosini

doi:10.3389/fneur.2018.00274

Elena Pretegiani, Antonio Federico + Show 7 more

Open Access

https://doi.org/10.3389/fneur.2018.00274

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Abstract

Increasing evidence suggests a cerebellar contribution to modulate cognitive aspects of motor behavior and executive functions. Supporting findings come from studies on patients with neurodegenerative diseases, in which however, given the extent of the disease, the specific role of the cerebellum, could not be clearly isolated. Anti-saccades are considered a sensitive tool to test executive functions. The anti-saccade underlying neural network, consisting of different cortical areas and their downstream connections including the lateral cerebellum, has been largely clarified. To separate the role of the cerebellum with respect to other cortical structures in executive control, we compared the anti-saccade performances in two distinct cohorts of patients with cerebellar disorders (with and without cerebral cortical involvement). Eye movements during the execution of anti-saccades were recorded in 12 patients with spinocerebellar ataxia type 2 (a cortical-subcortical neurodegenerative disease), 10 patients with late onset cerebellar ataxia (an isolated cerebellar atrophy), and 34 matched controls. In the anti-saccade task, besides dynamic changes already demonstrated in the pro-saccades of these patients, we found in both groups of cerebellar patients prolonged latency with larger variability than normal and increased directional error rate. Errors, however, were corrected by cerebellar patients as frequently as normal. No significant differences were found in patients with and without cortical involvement. Our results indicate, in a large cohort of cerebellar patients, that the cerebellum plays a critical role in the regulation of executive motor control not only, as well known, by controlling the end of a movement, but also modulating its initiation and reducing reflexive responses that would perturb voluntary actions.

Highlights

The cerebellum plays a well-known role in adapting motor responses by controlling the gain of a movement, its accuracy preservation, and by learning from endpoint errors [1,2,3,4]
To verify the null hypothesis that the latencies of correctly executed anti-saccades were sampled from the same continuous distribution, Kolmogorov–Smirnov tests were set for pairwise comparisons of the latency distributions
In our spinocerebellar ataxia type 2 (SCA2) patients, while abnormality of the cerebral cortex was only qualitatively evaluated, but not quantitatively measured at the brain magnetic resonance imaging (MRI), a cortical functional impairment could not be excluded given the common involvement in this disease

Summary

Introduction

The cerebellum plays a well-known role in adapting motor responses by controlling the gain of a movement, its accuracy preservation, and by learning from endpoint errors [1,2,3,4]. Adaptive behavior is considered the result of cerebellar internal models. A growing number of studies, have suggested that cerebellar internal models might act in the motor and in the sensory, behavioral, and cognitive domains [5,6,7,8,9,10,11]. These observations support the theory that the cerebellum plays a central role in monitoring executive brain performances [12, 13]. To which extent and for which functions this theory is valid, and which cerebellar areas are involved, remains largely unclear

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