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Sensory trick phenomenon in cervical dystonia: a functional MRI study

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Abstract

Sensory trick may relieve dystonic symptoms in patients with idiopathic cervical dystonia (CD). We investigated the patterns of brain functional MRI (fMRI) during resting state, sensory trick simulation and sensory trick imagination in CD patients both with and without an effective sensory trick. We recruited 17 CD patients and 15 healthy controls. Nine patients (CD-trick) had an effective sensory trick, while 8 patients (CD-no-trick) did not. Cervical range of motion validated instrument assessed dystonic posture and sensory trick effect. Participants underwent resting state fMRI, which was repeated by patients while executing the sensory trick. Patients also performed an fMRI task in which they were asked to imagine a sensory trick execution. CD-trick and CD-no-trick patients were comparable in terms of CD severity. Applying the sensory trick, CD-trick patients significantly improved dystonic posture. CD-no-trick patients showed an increased functional connectivity of sensorimotor network relative to controls during classic resting state fMRI. During resting state fMRI with sensory trick, CD-trick patients showed a decrease of sensorimotor network connectivity. During the sensory trick imagination fMRI task, CD-trick relative to CD-no-trick patients increased the recruitment of cerebellum bilaterally. This study suggests a hyper-connectivity of sensorimotor areas during resting state in CD-no-trick subjects. In CD-trick patients, the sensory trick performance was associated with a decreased connectivity of the sensorimotor network. The increased activation of cerebellum in CD-trick patients during the sensory trick imagination suggests a possible role of this area in modulating cortical activity.

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Authors and Affiliations

  1. Neuroimaging Research Unit, Division of Neuroscience, Institute of Experimental Neurology, IRCCS San Raffaele Scientific Institute, Milan, Italy

    Elisabetta Sarasso, Federica Agosta, Noemi Piramide & Massimo Filippi

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

    Massimo Filippi

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

    Francesca Bianchi, Carla Butera, Stefano Amadio, Ubaldo Del Carro & Massimo Filippi

  4. Vita-Salute San Raffaele University, Milan, Italy

    Federica Agosta & Massimo Filippi

  5. Laboratory of Movement Analysis, IRCCS San Raffaele Scientific Institute, Milan, Italy

    Elisabetta Sarasso

  6. Physiotherapy Unit, Humanitas Clinical and Research Center, Rozzano, Milan, Italy

    Roberto Gatti

  7. Humanitas University, Pieve Emanuele, Milan, Italy

    Roberto Gatti

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  1. Elisabetta Sarasso
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  2. Federica Agosta
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  6. Roberto Gatti
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  8. Ubaldo Del Carro
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Contributions

ES: substantial contributions to the conception of the work. Acquisition, analysis and interpretation of data. Drafting the work and revising it critically for important intellectual content. Final approval of the version published. Agreement to be accountable for all aspects of the work. FA: substantial contributions to the conception and design of the work. Interpretation of data. Revising the work critically for important intellectual content. Final approval of the version published. Agreement to be accountable for all aspects of the work. NP: substantial contributions to the conception of the work. Analysis of data. Revising the work critically for important intellectual content. Final approval of the version published. Agreement to be accountable for all aspects of the work. FB and CB: substantial contributions to the conception of the work. Acquisition of data. Revising the work critically for important intellectual content. Final approval of the version published. Agreement to be accountable for all aspects of the work. RG: substantial contributions to the conception of the work. Revising the work for important intellectual content. Final approval of the version published. Agreement to be accountable for all aspects of the work. SA: substantial contributions to the conception of the work. Acquisition of data. Revising the work critically for important intellectual content. Final approval of the version published. Agreement to be accountable for all aspects of the work. UDC substantial contributions to the conception of the work. Acquisition of data. Revising the work critically for important intellectual content. Final approval of the version published. Agreement to be accountable for all aspects of the work. MF: substantial contributions to the conception and design of the work. Interpretation of data. Revising the work critically for important intellectual content. Final approval of the version published. Agreement to be accountable for all aspects of the work.

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Correspondence to Massimo Filippi.

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Conflicts of interest

E. Sarasso, N. Piramide, F. Bianchi, C. Butera, R. Gatti, S. Amadio, U. Del Carro report no disclosures. F. Agosta is Section Editor of NeuroImage: Clinical; has received speaker honoraria from Philips, Novartis and Biogen Idec; 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. Prof. Filippi is Editor-in-Chief of the Journal of Neurology; received compensation for consulting services and/or speaking activities from Biogen Idec, Merck-Serono, Novartis, Teva Pharmaceutical Industries; and receives research support from Biogen Idec, Merck-Serono, Novartis, Teva Pharmaceutical Industries, Roche, Italian Ministry of Health, Fondazione Italiana Sclerosi Multipla, and ARiSLA (Fondazione Italiana di Ricerca per la SLA).

Ethical standards

All procedures performed in the study involving human participants are in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. All participants provided written informed consent prior to study inclusion.

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Sarasso, E., Agosta, F., Piramide, N. et al. Sensory trick phenomenon in cervical dystonia: a functional MRI study. J Neurol 267, 1103–1115 (2020). https://doi.org/10.1007/s00415-019-09683-5

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  • DOI: https://doi.org/10.1007/s00415-019-09683-5

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