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J Neurosurg. 2019 May 10:1-10. doi: 10.3171/2019.2.JNS183454. [Epub ahead of print]

Normalization of aberrant pretherapeutic dynamic functional connectivity of extrastriate visual system in patients who underwent thalamotomy with stereotactic radiosurgery for essential tremor: a resting-state functional MRI study.

Author information

1
1Service de Neurochirurgie, Assistance Publique-Hôpitaux de Paris, Hôpitaux Universitaires Paris-Sud, Centre Hospitalier Universitaire de Bicêtre, Paris.
2
2Faculté de Médecine, Sorbonne Université, Paris, France.
3
3Neurosurgery Service and Gamma Knife Center, Centre Hospitalier Universitaire Vaudois, Lausanne.
4
4Medical Image Analysis Laboratory and Department of Radiology-Center of Biomedical Imaging, Centre Hospitalier Universitaire Vaudois, Lausanne.
5
5Signal Processing Laboratory (LTS 5), École Polytechnique Fédérale de Lausanne.
6
6Faculty of Biology and Medicine University of Lausanne.
7
7Medical Image Processing Laboratory, École Polytechnique Fédérale de Lausanne, Switzerland.
8
8Department of Radiology and Medical Informatics, University of Geneva, Switzerland.
9
9Stereotactic and Functional Neurosurgery Service and Gamma Knife Unit, CHU Timone, Marseille.
10
10Neurology Department, CHU Timone, Marseille.
11
11Department of Diagnostic and Interventional Neuroradiology, Centre de Résonance Magnétique Biologique et Médicale, Unité Mixte de Recherche, Centre National de la Recherche Scientifique, Faculté de Médecine et Assistance Publique-Hôpitaux de Marseille, Hôpital Timone, Marseille, France.
12
12Institute of Social and Preventive Medicine, Lausanne; and.
13
13Department of Radiology, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland.

Abstract

OBJECTIVEThe tremor circuitry has commonly been hypothesized to be driven by one or multiple pacemakers within the cerebello-thalamo-cortical pathway, including the cerebellum, contralateral motor thalamus, and primary motor cortex. However, previous studies, using multiple methodologies, have advocated that tremor could be influenced by changes within the right extrastriate cortex, at both the structural and functional level. The purpose of this work was to evaluate the role of the extrastriate cortex in tremor generation and further arrest after left unilateral stereotactic radiosurgery thalamotomy (SRS-T).METHODSThe authors considered 12 healthy controls (HCs, group 1); 15 patients with essential tremor (ET, right-sided, drug-resistant; group 2) before left unilateral SRS-T; and the same 15 patients (group 3) 1 year after the intervention, to account for delayed effects. Blood oxygenation level-dependent functional MRI during resting state was used to characterize the dynamic interactions of the right extrastriate cortex, comparing HC subjects against patients with ET before and 1 year after SRS-T. In particular, the authors applied coactivation pattern analysis to extract recurring whole-brain spatial patterns of brain activity over time.RESULTSThe authors found 3 different sets of coactivating regions within the right extrastriate cortex in HCs and patients with pretherapeutic ET, reminiscent of the "cerebello-visuo-motor," "thalamo-visuo-motor" (including the targeted thalamus), and "basal ganglia and extrastriate" networks. The occurrence of the first pattern was decreased in pretherapeutic ET compared to HCs, whereas the other two patterns showed increased occurrences. This suggests a misbalance between the more prominent cerebellar circuitry and the thalamo-visuo-motor and basal ganglia networks. Multiple regression analysis showed that pretherapeutic standard tremor scores negatively correlated with the increased occurrence of the thalamo-visuo-motor network, suggesting a compensatory pathophysiological trait. Clinical improvement after SRS-T was related to changes in occurrences of the basal ganglia and extrastriate cortex circuitry, which returned to HC values after the intervention, suggesting that the dynamics of the extrastriate cortex had a role in tremor generation and further arrest after the intervention.CONCLUSIONSThe data in this study point to a broader implication of the visual system in tremor generation, and not only through visual feedback, given its connections to the dorsal visual stream pathway and the cerebello-thalamo-cortical circuitry, with which its dynamic balance seems to be a crucial feature for reduced tremor. Furthermore, SRS-T seems to bring abnormal pretherapeutic connectivity of the extrastriate cortex to levels comparable to those of HC subjects.

KEYWORDS:

ADL = activities of daily living; BA = Brodmann area; BOLD = blood oxygenation level–dependent; CAP = coactivation pattern; CHU = Centre Hospitalier Universitaire; DMN = default mode network; DTI = diffusion tensor imaging; ET = essential tremor; GMD = gray matter density; HC = healthy control; PCC = posterior cingulate cortex; QUEST = Quality of Life in Essential Tremor; ROI = region of interest; SRS-T = stereotactic radiosurgery thalamotomy; TSTH = tremor score on the treated hand; Vim = ventral intermediate nucleus; coactivation pattern analysis; dFC = dynamic functional connectivity; extrastriate; fMRI = functional MRI; functional magnetic resonance imaging; functional neurosurgery; radiosurgery; resting state; thalamotomy; ventral intermediate nucleus; visual

PMID:
31075777
DOI:
10.3171/2019.2.JNS183454

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