Abnormal lateralization of fine motor actions in Tourette syndrome persists into adulthood.

D Martino,L Avanzino,E Pelosin,A Hartmann,C Delorme,Y Worbe

doi:10.1371/journal.pone.0180812

Abstract

Youth with Tourette syndrome (TS) exhibit, compared to healthy, abnormal ability to lateralize digital sequential tasks. It is unknown whether this trait is related to inter-hemispheric connections, and whether it is preserved or lost in patients with TS persisting through adult life. We studied 13 adult TS patients and 15 age-matched healthy volunteers. All participants undertook: 1) a finger opposition task, performed with the right hand (RH) only or with both hands, using a sensor-engineered glove in synchrony with a metronome at 2 Hz; we calculated a lateralization index [(single RH–bimanual RH)/single RH X 100) for percentage of correct movements (%CORR); 2) MRI-based diffusion tensor imaging and probabilistic tractography of inter-hemispheric corpus callosum (CC) connections between supplementary motor areas (SMA) and primary motor cortices (M1). We confirmed a significant increase in the %CORR in RH in the bimanual vs. single task in TS patients (p<0.001), coupled to an abnormal ability to lateralize finger movements (significantly lower lateralization index for %CORR in TS patients, p = 0.04). The %CORR lateralization index correlated positively with tic severity measured with the Yale Global Tic Severity Scale (R = 0.55;p = 0.04). We detected a significantly higher fractional anisotropy (FA) in both the M1-M1 (p = 0.036) and the SMA-SMA (p = 0.018) callosal fibre tracts in TS patients. In healthy subjects, the %CORR lateralization index correlated positively with fractional anisotropy of SMA-SMA fibre tracts (R = 0.63, p = 0.02); this correlation was not significant in TS patients. TS patients exhibited an abnormal ability to lateralize finger movements in sequential tasks, which increased in accuracy when the task was performed bimanually. This abnormality persists throughout different age periods and appears dissociated from the transcallosal connectivity of motor cortical regions. The altered interhemispheric transfer of motor abilities in TS may be the result of compensatory processes linked to self-regulation of motor control.

Highlights

Tourette syndrome (TS) is a childhood-onset neurodevelopmental disorder defined by persistent motor and vocal tics [1]
We evaluated the following kinematic parameters of the finger motor sequence: touch duration (TD), defined as the contact time between the thumb and another finger; inter-tapping interval (ITI), defined as the time between the end of the contact between the thumb and another finger and the beginning of the contact between thumb and the adjacent finger; and number of correct movements expressed as a percentage of the total number of movements requested by the task (%CORR)
Our adult TS patients exhibited longer touch duration and shorter inter-tapping interval in the dominant hand performance. This executional pattern, which could reflect abnormal processing of sensory information during the motor preparation phase, appears to be constantly present in patients with TS from childhood to adulthood. This pattern was not associated with a reduced accuracy on right hand performance on the single-hand task (%CORR) in TS adults as opposed to TS children, probably because of increased effectiveness of motor control acquired with age in both patients and control subjects

Summary

Introduction

Tourette syndrome (TS) is a childhood-onset neurodevelopmental disorder defined by persistent motor and vocal tics [1]. We previously documented that voluntary finger movements are less lateralized in children with “pure” TS (i.e. without clinically relevant behavioural comorbidities), leading to a better performance during bimanual tasks, which suggests atypical development of sensorimotor integration, movement lateralization and bimanual coordination of fine motion in this patient population [4]. Some aspects of this abnormal ability to lateralize fine manual tasks remain poorly understood. In young and older adults, bimanual coordination was significantly related to the microstructural properties of the more anterior sub-regions of the CC, including the premotor/supplementary and primary motor [8,9]

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