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Task-specificity in focal dystonia is shaped by aberrant diversity of a functional network kernel.

ABSTRACT: OBJECTIVES:Task-specific focal dystonia selectively affects the motor control during skilled and highly learned behaviors. Recent data suggest the role of neural network abnormalities in the development of the pathophysiological dystonic cascade. METHODS:We used resting-state functional MRI and analytic techniques rooted in network science and graph theory to examine the formation of abnormal subnetwork of highly influential brain regions, the functional network kernel, and its influence on aberrant dystonic connectivity specific to affected body region and skilled motor behavior. RESULTS:We found abnormal embedding of sensorimotor cortex and prefrontal thalamus in dystonic network kernel as a hallmark of task-specific focal dystonia. Dependent on the affected body region, aberrant functional specialization of the network kernel included regions of motor control management in focal hand dystonia (writer's cramp, musician's focal hand dystonia) and sensorimotor processing in laryngeal dystonia (spasmodic dysphonia, singer's laryngeal dystonia). Dependent on skilled motor behavior, the network kernel featured altered connectivity between sensory and motor execution circuits in musician's dystonia (musician's focal hand dystonia, singer's laryngeal dystonia) and abnormal integration of sensory feedback into motor planning and executive circuits in non-musician's dystonia (writer's cramp, spasmodic dysphonia). CONCLUSIONS:Our study identified specific traits in disorganization of large-scale neural connectivity that underlie the common pathophysiology of task-specific focal dystonia while reflecting distinct symptomatology of its different forms. Identification of specialized regions of information transfer that influence dystonic network activity is an important step for future delineation of targets for neuromodulation as a potential therapeutic option of task-specific focal dystonia. © 2018 International Parkinson and Movement Disorder Society.

SUBMITTER: Fuertinger S

PROVIDER: S-EPMC6309584 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Task-specificity in focal dystonia is shaped by aberrant diversity of a functional network kernel.

Fuertinger Stefan S Simonyan Kristina K

Movement disorders : official journal of the Movement Disorder Society 20180927 12

<h4>Objectives</h4>Task-specific focal dystonia selectively affects the motor control during skilled and highly learned behaviors. Recent data suggest the role of neural network abnormalities in the development of the pathophysiological dystonic cascade.<h4>Methods</h4>We used resting-state functional MRI and analytic techniques rooted in network science and graph theory to examine the formation of abnormal subnetwork of highly influential brain regions, the functional network kernel, and its in ...[more]

PMID: 30264427

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Project description:BackgroundFocal dystonias are severe and disabling movement disorders of a still unclear origin. The structural brain networks associated with focal dystonia have not been well characterized. Here, we investigated structural brain network fingerprints in patients with blepharospasm (BSP) compared with those with hemifacial spasm (HFS), and healthy controls (HC). The patients were also examined following treatment with botulinum neurotoxin (BoNT).MethodsThis study included matched groups of 13 BSP patients, 13 HFS patients, and 13 HC. We measured patients using structural-magnetic resonance imaging (MRI) at baseline and after one month BoNT treatment, at time points of maximal and minimal clinical symptom representation, and HC at baseline. Group regional cross-correlation matrices calculated based on grey matter volume were included in graph-based network analysis. We used these to quantify global network measures of segregation and integration, and also looked at local connectivity properties of different brain regions.ResultsThe networks in patients with BSP were more segregated than in patients with HFS and HC (p < 0.001). BSP patients had increased connectivity in frontal and temporal cortices, including sensorimotor cortex, and reduced connectivity in the cerebellum, relative to both HFS patients and HC (p < 0.05). Compared with HC, HFS patients showed increased connectivity in temporal and parietal cortices and a decreased connectivity in the frontal cortex (p < 0.05). In BSP patients, the connectivity of the frontal cortex diminished after BoNT treatment (p < 0.05). In contrast, HFS patients showed increased connectivity in the temporal cortex and reduced connectivity in cerebellum after BoNT treatment (p < 0.05).ConclusionsOur results show that BSP patients display alterations in both segregation and integration in the brain at the network level. The regional differences identified in the sensorimotor cortex and cerebellum of these patients may play a role in the pathophysiology of focal dystonia. Moreover, symptomatic reduction of hyperkinesia by BoNT treatment was associated with different brain network fingerprints in both BSP and HFS patients.

Project description:Cervical dystonia is characterized by involuntary, abnormal movements and postures of the head and neck. Current views on its pathophysiology, such as faulty sensorimotor integration and impaired motor planning, are largely based on studies of focal hand dystonia. Using resting state fMRI, we explored whether cervical dystonia patients have altered functional brain connectivity compared to healthy controls, by investigating 10 resting state networks. Scans were repeated immediately before and some weeks after botulinum toxin injections to see whether connectivity abnormalities were restored. We here show that cervical dystonia patients have reduced connectivity in selected regions of the prefrontal cortex, premotor cortex and superior parietal lobule within a distributed network that comprises the premotor cortex, supplementary motor area, primary sensorimotor cortex, and secondary somatosensory cortex (sensorimotor network). With regard to a network originating from the occipital cortex (primary visual network), selected regions in the prefrontal and premotor cortex, superior parietal lobule, and middle temporal gyrus areas have reduced connectivity. In selected regions of the prefrontal, premotor, primary motor and early visual cortex increased connectivity was found within a network that comprises the prefrontal cortex including the anterior cingulate cortex and parietal cortex (executive control network). Botulinum toxin treatment resulted in a partial restoration of connectivity abnormalities in the sensorimotor and primary visual network. These findings demonstrate the involvement of multiple neural networks in cervical dystonia. The reduced connectivity within the sensorimotor and primary visual networks may provide the neural substrate to expect defective motor planning and disturbed spatial cognition. Increased connectivity within the executive control network suggests excessive attentional control and while this may be a primary trait, perhaps contributing to abnormal motor control, this may alternatively serve a compensatory function in order to reduce the consequences of the motor planning defect inflicted by the other network abnormalities.

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Task-specificity in focal dystonia is shaped by aberrant diversity of a functional network kernel.

Publications

Task-specificity in focal dystonia is shaped by aberrant diversity of a functional network kernel.

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