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Acta Neurochirurgica

, Volume 160, Issue 3, pp 611–624 | Cite as

Clinical response to Vim’s thalamic stereotactic radiosurgery for essential tremor is associated with distinctive functional connectivity patterns

  • Constantin Tuleasca
  • Elena Najdenovska
  • Jean Régis
  • Tatiana Witjas
  • Nadine Girard
  • Jérôme Champoudry
  • Mohamed Faouzi
  • Jean-Philippe Thiran
  • Meritxell Bach Cuadra
  • Marc Levivier
  • Dimitri Van De Ville
Original Article - Functional

Abstract

Introduction

Essential tremor (ET) is the most common movement disorder. Drug-resistant ET can benefit from standard surgical stereotactic procedures (deep brain stimulation, thalamotomy) or minimally invasive high-intensity focused ultrasound (HIFU) or stereotactic radiosurgical thalamotomy (SRS-T). Resting-state fMRI (rs-fMRI) is a non-invasive imaging method acquired in absence of a task. We examined whether rs-fMRI correlates with tremor score on the treated hand (TSTH) improvement 1 year after SRS-T.

Methods

We included 17 consecutive patients treated with left unilateral SRS-T in Marseille, France. Tremor score evaluation and rs-fMRI were acquired at baseline and 1 year after SRS-T. Resting-state data (34 scans) were analyzed without a priori hypothesis, in Lausanne, Switzerland. Based on degree of improvement in TSTH, to consider SRS-T at least as effective as medication, we separated two groups: 1, ≤ 50% (n = 6, 35.3%); 2, > 50% (n = 11, 64.7%). They did not differ statistically by age (p = 0.86), duration of symptoms (p = 0.41), or lesion volume at 1 year (p = 0.06).

Results

We report TSTH improvement correlated with interconnectivity strength between salience network with the left claustrum and putamen, as well as between bilateral motor cortices, frontal eye fields and left cerebellum lobule VI with right visual association area (the former also with lesion volume). Longitudinal changes showed additional associations in interconnectivity strength between right dorsal attention network with ventro-lateral prefrontal cortex and a reminiscent salience network with fusiform gyrus.

Conclusions

Brain connectivity measured by resting-state fMRI relates to clinical response after SRS-T. Relevant networks are visual, motor, and attention. Interconnectivity between visual and motor areas is a novel finding, revealing implication in movement sensory guidance.

Keywords

Resting-state fMRI Essential tremor Ventro-intermediate nucleus Radiosurgery Independent component analysis Thalamotomy 

Notes

Acknowledgments

We acknowledge the contribution of Axelle Cretol, from Marseille University Hospital (CHU Timone), France, who, as a research assistant, kept the database up-to-date.

Funding

The work was supported by the Swiss National Science Foundation (SNSF-205321-157040) and by the Centre d’Imagerie BioMédicale (CIBM) of the University of Lausanne (UNIL), the Swiss Federal Institute of Technology Lausanne (EPFL), the University of Geneva (UniGe), the Centre Hospitalier Universitaire Vaudois (CHUV), the CHU Timone, Marseille, France, the Hôpitaux Universitaires de Genève (HUG), and the Leenaards and Jeantet Foundations.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

The Ethical Committee of the Marseille University Hospital (CPPRB1) approved our study.

Supplementary material

701_2017_3456_MOESM1_ESM.pdf (2.7 mb)
Supplementary figure 1: Illustration of the effect of group on component 5, 6 and 11; for component 5, the corresponding clusters are left dentate (A), vermis (B) and right thalamus (pulvinar) (C) with axial (upper), coronal (middle) and sagittal reconstruction (lower); furthermore, illustration of the right pulvinar (C), with the respective boxplots and median values at baseline and 1 year, separated by groups, to show the effect; for component 6, the corresponding cluster is right parietal area (BA 7), with axial (left)), coronal (middle) and sagittal (right) reconstruction; the respective boxplots and median values at baseline and 1 year, separated by groups, to show the effect (below); for component 11, the corresponding clusters are right putamen (A), right thalamus (B) and left thalamus (C) with axial (upper), coronal (middle) and sagittal reconstruction (lower); further illustration of the right putamen and left thalamus FC values with the respective boxplots and median values at baseline and 1 year, separated by groups, to show the effect (below); with axial (upper), coronal (middle) and sagittal reconstruction (lower); (PDF 2769 kb)
701_2017_3456_MOESM2_ESM.pdf (4 mb)
Supplementary figure 2: Illustration of the effect of group on component 13, 15 and 16; for component 13, the corresponding clusters are left frontal eye-fields (A), left dorso-lateral prefrontal (B), right (C) and left (D) supramarginal gyrus, with axial (upper), coronal (middle) and sagittal reconstruction (lower); furthermore, illustration of FC values for the left dorso-lateral, left frontal-eye fields and right supramarginal gyrus, with the respective boxplots and median values at baseline and 1 year, separated by groups, to show the effect (below); for component 15, the corresponding clusters are left retro-spenial cortex (A) and left angular gyrus (B), with axial (left), coronal (middle) and sagittal reconstruction (right); furthermore, illustration of FC values for both clusters, with the respective boxplots and median values at baseline and 1 year, separated by groups, to show the effect (below); for component 16, the corresponding clusters are right posterior cingulate (A), middle temporal area (B) and supramarginal gyrus (C), with axial (upper), coronal (middle) and sagittal reconstruction (lower); furthermore, illustration of FC values for posterior cingulate and left middle temporal area, with the respective boxplots and median values at baseline and 1 year, separated by groups, to show the effect (below); (PDF 4128 kb)
701_2017_3456_MOESM3_ESM.pdf (6.3 mb)
Supplementary figure 3: Illustration of the effect of group on component 12, 18 and 19; for component 12, the corresponding clusters are left middle temporal area (A), left fusiform gyrus (B), left cerebellar (C), left angular gyrus (D), right supramarginal gyrus (E), right superior parietal lobule (F); for all of them, illustration of FC values, with the respective boxplots and median values at baseline and 1 year, separated by groups, to show the effect (below); for component 18, the corresponding clusters are left angular gyrus (A), left BA 7 parietal (B), left cerebellar (C), right anterior dorsal cingulate (D), right angular gyrus (E) and right ventral anterior cingulate (F); furthermore, illustration of FC values for left cerebellar and right anterior dorsal cingulate area, with the respective boxplots and median values at baseline and 1 year, separated by groups, to show the effect (below); for component 19, the corresponding clusters are left angular gyrus (A), left parietal (B), left anterior dorsal cingulate (C), right posterior parietal (D), right angular gyrus (E) and right frontal eye fields (F); furthermore, illustration of FC values for left anterior dorsal cingulate and frontal eye fields, with the respective boxplots and median values at baseline and 1 year, separated by groups, to show the effect (below) (PDF 6461 kb)

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Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Constantin Tuleasca
    • 1
    • 2
    • 3
    • 4
  • Elena Najdenovska
    • 2
    • 4
  • Jean Régis
    • 5
  • Tatiana Witjas
    • 6
  • Nadine Girard
    • 7
  • Jérôme Champoudry
    • 5
  • Mohamed Faouzi
    • 8
  • Jean-Philippe Thiran
    • 3
    • 4
    • 9
  • Meritxell Bach Cuadra
    • 2
    • 3
    • 4
  • Marc Levivier
    • 1
    • 4
  • Dimitri Van De Ville
    • 10
    • 11
  1. 1.Neurosurgery Service and Gamma Knife CenterCentre Hospitalier Universitaire Vaudois (CHUV)LausanneSwitzerland
  2. 2.Medical Image Analysis Laboratory (MIAL) and Department of Radiology-Center of Biomedical Imaging (CIBM)Centre Hospitalier Universitaire VaudoisLausanneSwitzerland
  3. 3.Signal Processing Laboratory (LTS 5)Ecole Polytechnique Fédérale de Lausanne (EPFL)LausanneSwitzerland
  4. 4.Faculty of Biology and MedicineUniversity of LausanneLausanneSwitzerland
  5. 5.Stereotactic and Functional Neurosurgery Service and Gamma Knife UnitCHU TimoneMarseilleFrance
  6. 6.Neurology DepartmentCHU TimoneMarseilleFrance
  7. 7.Department of Diagnostic and Interventionnal NeuroradiologyAMU, CRMBM UMR CNRS 7339, Faculté de Médecine et APHM, Hopital TimoneMarseilleFrance
  8. 8.Institute of Social and Preventive MedicineLausanneSwitzerland
  9. 9.Department of RadiologyCentre Hospitalier Universitaire VaudoisLausanneSwitzerland
  10. 10.Faculty of MedicineUniversity of GenevaGenevaSwitzerland
  11. 11.Medical Image Processing LaboratoryEcole Polytechnique Fédérale de Lausanne (EPFL)LausanneSwitzerland

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