Ventrolateral Motor Thalamus Abnormal Connectivity in Essential Tremor Before and After Thalamotomy: A Resting-State Functional Magnetic Resonance Imaging Study

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

doi:10.1016/j.wneu.2018.02.055

Ventrolateral Motor Thalamus Abnormal Connectivity in Essential Tremor Before and After Thalamotomy: A Resting-State Functional Magnetic Resonance Imaging Study

World Neurosurg. 2018 May:113:e453-e464. doi: 10.1016/j.wneu.2018.02.055. Epub 2018 Feb 21.

Affiliations

¹ Neurosurgery Service and Gamma Knife Center, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland; Medical Image Analysis Laboratory (MIAL) and Department of Radiology-Center of Biomedical Imaging (CIBM), Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland; Signal Processing Laboratory (LTS 5), Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland; Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland. Electronic address: constantin.tuleasca@gmail.com.
² Medical Image Analysis Laboratory (MIAL) and Department of Radiology-Center of Biomedical Imaging (CIBM), Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland.
³ Stereotactic and Functional Neurosurgery Service and Gamma Knife Unit, CHU Timone, Marseille, France.
⁴ Neurology Department, CHU Timone, Marseille, France.
⁵ AMU, CRMBM UMR CNRS 7339, Faculté de Médecine and APHM, Hopital Timone, Department of Diagnostic and Interventional Neuroradiology, Marseille, France.
⁶ Centre for Clinical Epidemiology, Institute of Social and Preventive Medicine, Lausanne, Switzerland.
⁷ Department of Radiology, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland; Signal Processing Laboratory (LTS 5), Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland; Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland.
⁸ Medical Image Analysis Laboratory (MIAL) and Department of Radiology-Center of Biomedical Imaging (CIBM), Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland; Signal Processing Laboratory (LTS 5), Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland.
⁹ Neurosurgery Service and Gamma Knife Center, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland; Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland.
¹⁰ Faculty of Medicine, University of Geneva, Geneva, Switzerland; Medical Image Processing Laboratory, Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland. Electronic address: dimitri.vandeville@epfl.ch.

PMID: 29475059
DOI: 10.1016/j.wneu.2018.02.055

Abstract

Objective: To evaluate functional connectivity (FC) of the ventrolateral thalamus, a common target for drug-resistant essential tremor (ET), resting-state data were analyzed before and 1 year after stereotactic radiosurgical thalamotomy and compared against healthy controls (HCs).

Methods: In total, 17 consecutive patients with ET and 10 HCs were enrolled. Tremor network was investigated using the ventrolateral ventral (VLV) thalamic nucleus as the region of interest, extracted with automated segmentation from pretherapeutic diffusion magnetic resonance imaging. Temporal correlations of VLV at whole brain level were evaluated by comparing drug-naïve patients with ET with HCs, and longitudinally, 1 year after stereotactic radiosurgical thalamotomy. 1 year thalamotomy MR signature was always located inside VLV and did not correlate with any of FC measures (P > 0.05). This suggested presence of longitudinal changes in VLV FC independently of the MR signature volume.

Results: Pretherapeutic ET displayed altered VLV FC with left primary sensory-motor cortex, pedunculopontine nucleus, dorsal anterior cingulate, left visual association, and left superior parietal areas. Pretherapeutic negative FC with primary somatosensory cortex and pedunculopontine nucleus correlated with poorer baseline tremor scores (Spearman = 0.04 and 0.01). Longitudinal study displayed changes within right dorsal attention (frontal eye-fields and posterior parietal) and salience (anterior insula) networks, as well as areas involved in hand movement planning or language production.

Conclusions: Our results demonstrated that patients with ET and HCs differ in their left VLV FC to primary somatosensory and supplementary motor, visual association, or brainstem areas (pedunculopontine nucleus). Longitudinal changes display reorganization of dorsal attention and salience networks after thalamotomy. Beside attentional gateway, they are also known for their major role in facilitating a rapid access to the motor system.

Keywords: Essential tremor; Motor thalamus; Resting state; Stereotactic radiosurgery; Thalamotomy; Ventrointermediate nucleus; fMRI.

MeSH terms

Aged
Aged, 80 and over
Attention
Brain Mapping / methods*
Diffusion Magnetic Resonance Imaging / methods*
Essential Tremor / physiopathology
Essential Tremor / surgery*
Female
Follow-Up Studies
Humans
Magnetic Resonance Imaging*
Male
Middle Aged
Nerve Net / physiopathology
Neuroimaging*
Pedunculopontine Tegmental Nucleus / physiopathology
Radiosurgery*
Thalamus / surgery*
Ventral Thalamic Nuclei / physiopathology*