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The reorganization of motor network in hemidystonia from the perspective of deep brain stimulation

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Abstract

Hemidystonia is usually ‘secondary’ to structural lesions within the cortico-striato-pallido-thalamic or the cerebello-thalamo-cortical loops. Globus pallidus internus Deep Brain Stimulation (GPi DBS) is a validated technique in the treatment of primary dystonia and still under assessment for secondary dystonia. Results of DBS in hemidystonia are limited and heterogeneous. Further knowledge concerning motor network organization after focal brain lesions might contribute to the understanding of this mitigated response to DBS and to the refinement of DBS indications and techniques in secondary dystonia. This study aimed to identify movement-related functional magnetic resonance imaging (fMRI) activation patterns in a group of hemidystonic patients in comparison to healthy controls (HC). Further analysis assessed recruitment pattern in different patient subgroups defined according to clinical and radiological criteria relevant to GPi DBS eligibility (hyperkinetic/hypokinetic and prepallidal/postpallidal). Eleven patients and nine HC underwent fMRI with a block-design alternating active and rest conditions. The motor paradigm consisted of self-paced elbow flexion-extension movements. The main results were as follows: single-subject studies revealed several activation patterns involving motor-related network regions; both ipsilesional and contralesional hemispheres showed abnormal patterns of activity; compared with HC, hemidystonic patients showed decreased brain activity in ipsilesional thalamus, pallidal and temporal areas during affected arm task execution; ‘hypokinetic’ subgroup was commonly related to widespread bilateral overactivity. This study provides additional arguments for case-by-case assessment of DBS surgery indication and target selection in hemidystonia. Single-lead approach might be unable to modulate a highly disorganized network activity in certain patients with this clinical syndrome.

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Acknowledgments

The authors thank also the patients and the families who participated in the study.

Conflict of interest

Financial disclosure related to research covered in this article: No conflict of interest related to this work is reported by the authors.

Full financial disclosure: V. Gonzalez, L. Cif and P. Coubes received lecture fees from Medtronic Company. E. Le Bars, L. EH van Dokkum, I. Laffont, N. Menjot de Champfleur, A. Bonafé and M. Zanca: report no disclosures.

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This research has been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. Informed written consent was provided by all subjects participating in the study.

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Correspondence to Victoria Gonzalez.

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Emmanuelle Le Bars and Laura Cif equally contributed to this study

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Table 4 and 5 Within-subject studies: anatomic MNI coordinates of significant clusters with dystonic and non-dystonic movements (DOCX 43.3 kb)

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Table 6 One-sample t tests Group analysis within healthy control and hemidystonic groups: anatomic MNI coordinates of significant clusters with dystonic and non-dystonic movements (DOCX 32.4 kb)

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Fig. 3 Task-related activity patterns in single-subject studies (P FWE-corr<0.05) with dystonic (right) arm movements: a) healthy control (contralateral SMC activity); b) hyperkinetic subgroup patient (contralateral lobule VII cerebellar activity); c) hyperkinetic subgroup (contralateral SMC, SMA, lobule VII cerebellar activity); d, e, f) Hypokinetic subgroup patients (bilateral activity observed in three patients) (JPEG 19 kb)

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Gonzalez, V., Le Bars, E., Cif, L. et al. The reorganization of motor network in hemidystonia from the perspective of deep brain stimulation. Brain Imaging and Behavior 9, 223–235 (2015). https://doi.org/10.1007/s11682-014-9300-5

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