Impaired Motor Timing in Tourette Syndrome: Results From a Case-Control Study in Children.

Federica Graziola,Paolo Curatolo,Federico Vigevano,Alessandro Capuano,Chiara Pellorca,Lorena Di Criscio

doi:10.3389/fneur.2020.552701

Federica Graziola, Paolo Curatolo + Show 4 more

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https://doi.org/10.3389/fneur.2020.552701

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Abstract

Tourette syndrome (TS) is a neurodevelopmental disorder characterized by motor and vocal tics. Co-occurrence of attention-deficit/hyperactivity disorder (ADHD) or obsessive–compulsive disorder (OCD) is very frequent in the pediatric population as well as the presence of an impairment of the executive functions. The aim of our study was to investigate motor timing, that is, the temporal organization of motor behavior, in a pediatric population of Tourette patients. Thirty-seven Tourette patients (divided in 22 “pure” Tourette patients and 15 with ADHD) were compared with 22 healthy age- and gender-matched subjects. All subjects underwent a neuropsychiatric screening and were tested for their planning and decision-making abilities by using a standardized test, such as Tower of London (ToL). Two experimental paradigms were adopted: finger-tapping test (FTT), a free motor tapping task, and synchronization–continuation task. An accuracy index was calculated as measure of ability of synchronization. We found that “pure” TS as well as TS+ADHD showed lower scores in the FTT for the dominant and non-dominant hands than controls. Moreover, in the synchronization and continuation test, we observed an overall lack of accuracy in both TS groups in the continuation phase for 2,000 ms (supra-second interval), interestingly, with opposite direction of accuracy index. Thus, “pure” TS patients were classified as “behind the beat,” whereas, TS+ADHD as “ahead of the beat.” The performance in the finger tapping was inversely correlated to ToL total scores and execution time, whereas we did not find any correlation with the accuracy index of the synchronization and continuation test. In conclusion, here, we explored motor timing ability in a childhood cohort of Tourette patients, confirming that patients exhibit an impaired temporal control of motor behavior and these findings may be explained by the common underlying neurobiology of TS and motor timing.

Highlights

Tourette syndrome (TS) is a childhood-onset neurodevelopmental movement disorder clinically characterized by the presence of multiple motor tics and one or more phonic/vocal tics that last for more than 1 year [1]
Ultimate neural mechanisms are far to be completely elucidated, theories, widely accepted, on the psychological and anatomical components of interval timing are based on the neurobiological model of an “internal clock” [12], which consists of an internal pacemaker connected via a decision mechanism to previously important duration codes held in reference memory
In the patients’ group, 60% had a diagnosis of TS without any comorbid condition and 40% with attention-deficit/hyperactivity disorder (ADHD) comorbidity (TS+ADHD, n = 15)

Summary

Introduction

Tourette syndrome (TS) is a childhood-onset neurodevelopmental movement disorder clinically characterized by the presence of multiple motor tics and one or more phonic/vocal tics that last for more than 1 year [1]. Motor Timing in Tourette Syndrome patients with TS without any other comorbid conditions, are relatively uncommon [3]; attention-deficit/hyperactivity disorder (ADHD) or obsessive–compulsive disorder (OCD) is commonly associated [4], but other several clinical and subclinical conditions, such as explosive outbursts, conduct problems, anxiety, self-injurious behavior, and depression, could run the clinical course of the disease [5,6,7]. Cognitive functions, and in particular, executive ones, including inhibition/attention, working memory, planning ability, and problem solving, have been reported to be impaired in TS [8], with conflicting results [9, 10], probably because it is difficult to distinguish the role of comorbid conditions in this framework. Functional imaging studies in humans and lesional studies in animals pointed out the role of basal ganglia nuclei and cortico-striato-thalamo-cortical (CSTC) circuitry [13], as well as it seems that the model crucially depends on the striatal integration of oscillating cortical activity [14]

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