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

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.

Fig 1. Experimental paradigm.

Subject performed with eyes closed a finger opposition movement task (opposition of thumb to index, medium, ring and little fingers), following an acoustic cue set at 2 Hz. The task was executed with right hand only (single hand task; RH-S) or both the right (RH-B) and left (LH-B) hands simultaneously (bimanual task). The analysis was planned to study for movement lateralization and bimanual coordination.

Fig 2. Regions of interest-seeded tractography.

Fig 2A shows the callosal fibre tracts interconnecting the primary motor area (M1) of the two hemispheres, whereas Fig 2B shows the callosal fibre tracts interconnecting of the supplementary motor area (SMA) of the two hemispheres.

Fig 3. Motor behaviour parameters in healthy subjects (HS) and patients with Gilles de la Tourette syndrome (TS) during the execution of single- hand finger sequence with the right hand (RH-S) and during bimanual finger sequence with the right (RH-B) hand.

A–B: ordinate, value of TD and ITI in milliseconds; C: ordinate, % of CORRECT MOVEMENTS in percentage on total movements. Means ± standard errors of mean (SEM) of data are shown. Asterisks indicate when statistical analysis showed a significant difference (* p < 0.05, ** p < 0.01).

Fig 4. Fig 4A shows the lateralization index of the % CORRECT MOVEMENTS in healthy subjects (HS) and patients with Gilles de la Tourette syndrome (TS), calculated as [% CORR MOV RH-B–% CORR MOV RH-S / % CORR MOV RH-S x 100].

Means ± standard errors of mean (SEM) of data are shown. Asterisks indicate when statistical analysis showed a significant difference (* p < 0.05, ** p < 0.01). Fig 4B shows the correlation between the lateralization index of the % CORRECT MOVEMENTS (X-axis) and the YGTSS/50 score (Y-axis) in patients with Gilles de la Tourette syndrome (TS).

Fig 5

Correlation between the lateralization index of the % CORRECT MOVEMENTS (X-axis) and the FA SMA-SMA tract (Y-axis) in patients with Gilles de la Tourette syndrome (TS) (Fig 5A) and healthy subjects (HS) (Fig 5B).