Functional and structural neural bases of task specificity in isolated focal dystonia

Abstract

Background: Task-specific focal dystonias selectively affect movements during the production of highly learned and complex motor behaviors. Manifestation of some task-specific focal dystonias, such as musician's dystonia, has been associated with excessive practice and overuse, whereas the etiology of others remains largely unknown.

Objectives: In this study, we aimed to examine the neural correlates of task-specific dystonias in order to determine their disorder-specific pathophysiological traits.

Methods: Using multimodal neuroimaging analyses of resting-state functional connectivity, voxel-based morphometry and tract-based spatial statistics, we examined functional and structural abnormalities that are both common to and distinct between four different forms of task-specific focal dystonias.

Results: Compared to the normal state, all task-specific focal dystonias were characterized by abnormal recruitment of parietal and premotor cortices that are necessary for both modality-specific and heteromodal control of the sensorimotor network. Contrasting the laryngeal and hand forms of focal dystonia revealed distinct patterns of sensorimotor integration and planning, again involving parietal cortex in addition to inferior frontal gyrus and anterior insula. On the other hand, musician's dystonia compared to nonmusician's dystonia was shaped by alterations in primary and secondary sensorimotor cortices together with middle frontal gyrus, pointing to impairments of sensorimotor guidance and executive control.

Conclusion: Collectively, this study outlines a specialized footprint of functional and structural alterations in different forms of task-specific focal dystonia, all of which also share a common pathophysiological framework involving premotor-parietal aberrations. © 2019 International Parkinson and Movement Disorder Society.

Keywords: functional connectivity; gray matter volume; musician's focal hand dystonia; singer's laryngeal dystonia; spasmodic dysphonia; white matter integrity; writer's cramp.

FIG. 1.

Common and distinct functional and structural neural abnormalities in TSFD. Resting-state functional connectivity (A), gray matter volume (B), and white matter integrity (C) are depicted across all examined forms of task-specific focal dystonia compared to healthy controls (I); between task-specific focal dystonias contingent upon the affected body region in focal laryngeal dystonia compared to focal hand dystonia (II); and between task-specific focal dystonias based on the affected motor behavior in musician’s dystonia compared to nonmusician’s dystonia (III). The colors bar indicates the t statistics; the corresponding cluster peaks and P values are provided in Table 2. HC, healthy controls; FLD, focal laryngeal dystonia; FHD, focal hand dystonia; MD, musician’s dystonia; NMD, nonmusician’s dystonia; IPL, inferior parietal lobule; PreCG, precentral gyrus; PreCu, precuneus; IFG, inferior frontal gyrus; aIns, anterior insula; MGH, middle temporal gyrus; SMA, supplementary motor area; SPL, superior parietal lobule; S1, primary somatosensory cortex; OP, parietal operculum; MFG, middle frontal gyrus; CST, corticospinal tract; CBT, corticobulbar tract; SLF, superior longitudinal fasciculus.

FIG. 2.

Schematic representation of main findings and their interpretation. Diagram depicts a visual summary of functional and structural abnormalities in TSFDs.