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Functional MRI connectivity of the primary motor cortex in functional dystonia patients

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Abstract

Background

Functional movement disorders include a wide spectrum of clinically documented movement disorders without an apparent organic substrate.

Objective

To explore the functional connectivity (FC) of the primary motor (M1) cortex in functional dystonia (FD) patients relative to healthy controls, with a focus on different clinical phenotypes.

Methods

Forty FD patients (12 fixed [FixFD]; 28 mobile [MobFD]) and 43 healthy controls (14 young FixFD-age-matched [yHC]; 29 old MobFD-age-matched [oHC]) underwent resting state fMRI. A seed-based FC analysis was performed using bilateral M1 as regions of interest.

Results

Compared to controls, FD patients showed reduced FC between left M1 and left dorsal anterior cingulate cortex, and between right M1 and left M1, premotor/supplementary motor area (SMA), dorsal posterior cingulate cortex (PCC), and bilateral precuneus. Relative to yHC, FixFD patients showed reduced FC between M1 and precuneus bilaterally. Compared to oHC, MobFD patients revealed reduced FC between right M1 and left M1, premotor/SMA, dorsal-PCC, bilateral primary sensory cortices and parieto-occipital areas, and increased FC of right M1 with right associative visual cortex and bilateral ventral-PCC. FixFD patients, relative to MobFD, showed lower FC between the right M1 and right associative visual area, and bilateral precuneus and ventral-PCC.

Conclusions

This study suggests an altered brain FC of the motor circuit with areas involved in emotional processes and sense of agency in FD. FixFD patients showed FC abnormalities mainly in areas related to sense of agency, while MobFD in regions involved in sensorimotor functions (reduced FC) and emotional processing (increased FC).

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Acknowledgements

The authors thank the patients and their families for the time and effort they dedicated to the research.

Funding

Ministry of Education and Science Republic of Serbia (Grant #175090).

Author information

Authors and Affiliations

  1. Neuroimaging Research Unit, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Via Olgettina, 60, 20132, Milan, Italy

    Noemi Piramide, Elisabetta Sarasso, Elisa Canu, Silvia Basaia, Massimo Filippi & Federica Agosta

  2. Neurology Unit, IRCCS San Raffaele Scientific Institute, Via Olgettina, 60, 20132, Milan, Italy

    Massimo Filippi & Federica Agosta

  3. Neurorehabilitation Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy

    Massimo Filippi

  4. Neurophysiology Service, IRCCS San Raffaele Scientific Institute, Milan, Italy

    Massimo Filippi

  5. Vita-Salute San Raffaele University, Via Olgettina, 60, 20132, Milan, Italy

    Noemi Piramide, Massimo Filippi & Federica Agosta

  6. Clinic of Neurology, Faculty of Medicine, University of Belgrade, Belgrade, Serbia

    Aleksandra Tomic, Igor N. Petrovic, Marina Svetel, Natasa Dragasevic Miskovic & Vladimir S. Kostic

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  1. Noemi Piramide
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Contributions

NP: design and conceptualization of study; acquisition, analysis and interpretation of data; drafting and revision of the manuscript. ES: design and conceptualization of study; acquisition, analysis and interpretation of data; drafting and revision of the manuscript. AT: acquisition, analysis and interpretation of data; revision of the manuscript for intellectual content. EC: acquisition, analysis and interpretation of data; revision of the manuscript for intellectual content. IP: acquisition, analysis and interpretation of data; revision of the manuscript for intellectual content. SB: acquisition, analysis and interpretation of data; revision of the manuscript for intellectual content. MS: acquisition, analysis and interpretation of data; revision of the manuscript for intellectual content. NDM: acquisition, analysis and interpretation of data; revision of the manuscript for intellectual content. VSK: design and conceptualization of study; interpretation of data; revision of the manuscript for intellectual content; obtaining funding. MF: design and conceptualization of study; interpretation of data; revision of the manuscript for intellectual content. FA: design and conceptualization of study; interpretation of data; revision of the manuscript for intellectual content.

Corresponding author

Correspondence to Federica Agosta.

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Conflicts of interest

N. Piramide reports no disclosures; E. Sarasso reports no disclosures; A. Tomic reports no disclosures; M. Svetel reports no disclosures; S. Basaia reports no disclosures; D. Miskovic reports no disclosures; E. Canu has received research supports from the Italian Ministry of Health; I. Petrović has received speaker honoraria from Actavis and Salveo; V. Kostić has received speaker honoraria from Roche and Alkaloid; and receives research supports from the Swiss Pharm and Serbian Ministry of Education, Science and Development and Serbian Academy of Sciences and Art; M. Filippi is Editor-in-Chief of the Journal of Neurology, Associate Editor of Human Brain Mapping, Associate Editor of Radiology, and Associate Editor of Neurological Sciences; received compensation for consulting services and/or speaking activities from Alexion, Almirall, Bayer, Biogen, Celgene, Eli Lilly, Genzyme, Merck-Serono, Novartis, Roche, Sanofi, Takeda, and Teva Pharmaceutical Industries; and receives research support from Biogen Idec, Merck-Serono, Novartis, Roche, Teva Pharmaceutical Industries, Italian Ministry of Health, Fondazione Italiana Sclerosi Multipla, and ARiSLA (Fondazione Italiana di Ricerca per la SLA); F. Agosta is Section Editor of NeuroImage: Clinical, has received speaker honoraria from Biogen Idec, Novartis, Philips and Roche, and receives or has received research supports from the Italian Ministry of Health, AriSLA (Fondazione Italiana di Ricerca per la SLA), and the European Research Council.

Ethical standards

This study was performed in line with the principles of the Declaration of Helsinki. Local ethical standards committee on human experimentation approved the study protocol and all participants provided written informed consent prior to study inclusion.

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Piramide, N., Sarasso, E., Tomic, A. et al. Functional MRI connectivity of the primary motor cortex in functional dystonia patients. J Neurol 269, 2961–2971 (2022). https://doi.org/10.1007/s00415-021-10879-x

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