Structure-function abnormalities in cortical sensory projections in embouchure dystonia

Abstract

Background: Embouchure dystonia (ED) is a task-specific focal dystonia in professional brass players leading to abnormal orofacial muscle posturing/spasms during performance. Previous studies have outlined abnormal cortical sensorimotor function during sensory/motor tasks and in the resting state as well as abnormal cortical sensorimotor structure. Yet, potentially underlying white-matter tract abnormalities in this network disease are unknown.

Objective: To delineate structure-function abnormalities within cerebral sensorimotor trajectories in ED.

Method: Probabilistic tractography and seed-based functional connectivity analysis were performed in 16/16 ED patients/healthy brass players within a simple literature-informed network model of cortical sensorimotor processing encompassing supplementary motor, superior parietal, primary somatosensory and motor cortex as well as the putamen. Post-hoc grey matter volumetry was performed within cortices of abnormal trajectories.

Results: ED patients showed average axial diffusivity reduction within projections between the primary somatosensory cortex and putamen, with converse increases within projections between supplementary motor and superior parietal cortex in both hemispheres. Increase in the mode of anisotropy in patients was accompanying the latter left-hemispheric projection, as well as in the supplementary motor area's projection to the left primary motor cortex. Patient's left primary somatosensory functional connectivity with the putamen was abnormally reduced and significantly associated with the axial diffusivity reduction. Left primary somatosensory grey matter volume was increased in patients.

Conclusion: Correlates of abnormal tract integrity within primary somatosensory cortico-subcortical projections and higher-order sensorimotor projections support the key role of dysfunctional sensory information propagation in ED pathophysiology. Differential directionality of cortico-cortical and cortico-subcortical abnormalities hints at non-uniform sensory system changes.

Keywords: Basal Ganglia; Diffusion Tractography; Dystonia, Focal, Task-Specific; Musician’s Dystonia; Sensorimotor Cortex.

Fig. 1

Upper panel: Averaged probable trajectories from all participants and for all investigated projections shown in neurological display convention. Probable trajectories involving primary cortices are shown on the left, and trajectories involving higher-order cortices are shown on the right side of the panel. All probable trajectories are displayed at a tract probability threshold of 5%, allowing for visualisation of trajectory-associated variability, with intensities illustrating the percentage of subject overlay at the given threshold (group-wise overlay across probability thresholds is detailed in figure s-2). Warm colors represent tracts in the left, and cold colors represent tracts in the right hemisphere. Lower panel: Centroids representing the spatially most likely tract termination in the putamen in each group. Tract terminations followed the known topographic anterior-posterior distribution in the putamen (central column), patients being shown in dark and controls in light colors (centroid coordinates given in table s-5). Tract terminations were further in line with their respective topographic label in the striatal connectivity atlas (Tziortzi et al., 2014) visualized in the lateral columns (centroids projected on the 25% probability maps of striatal connectivity atlas labels: red = rostral motor; orange = caudal motor; blue = parietal). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

(A) Results of the FC analysis showing reduced left S1_FACE FC (in blue) with the putamen (highlighted in green). The area of altered FC within the putamen was spatially located beneath the terminations of the cortico-subcortical tract from S1 to the putamen (visualized through the overlaid averaged tract from Fig. 1, shown in red). (B) Results of post hoc analyses. The left panels depict the results of the regression analysis for both groups showing moderate significant positive association of the average axial diffusivity in the trajectory between S1_FACE and the putamen with the average FC with the putamen (extracted from a 10 mm sphere around the significant cluster’s peak coordinate). The right panel illustrated the result of the post-hoc GM volume analysis in the S1 ROI in patients (filled circles) and controls (filled diamonds). Error bars depict the double standard error of mean. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)