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Frontal Lobe Connectivity and Network Community Characteristics are Associated with the Outcome of Subthalamic Nucleus Deep Brain Stimulation in Patients with Parkinson’s Disease

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Abstract

Deep brain stimulation (DBS) of the subthalamic nucleus (STN) is nowadays an evidence-based state of the art therapy option for motor and non-motor symptoms in patients with Parkinson’s disease (PD). However, the exact anatomical regions of the cerebral network that are targeted by STN–DBS have not been precisely described and no definitive pre-intervention predictors of the clinical response exist. In this study, we test the hypothesis that the clinical effectiveness of STN–DBS depends on the connectivity profile of the targeted brain networks. Therefore, we used diffusion-weighted imaging (DWI) and probabilistic tractography to reconstruct the anatomical networks and the graph theoretical framework to quantify the connectivity profile. DWI was obtained pre-operatively from 15 PD patients who underwent DBS (mean age = 67.87 ± 7.88, 11 males, H&Y score = 3.5 ± 0.8) using a 3T MRI scanner (Philips Achieva). The pre-operative connectivity properties of a network encompassing frontal, prefrontal cortex and cingulate gyrus were directly linked to the postoperative clinical outcome. Eccentricity as a topological-characteristic of the network defining how cerebral regions are embedded in relation to distant sites correlated inversely with the applied voltage at the active electrode for optimal clinical response. We found that network topology and pre-operative connectivity patterns have direct influence on the clinical response to DBS and may serve as important and independent predictors of the postoperative clinical outcome.

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Abbreviations

AAL:

Automated anatomical labeling

AUC:

Area under the curve

BCT:

Brain connectivity toolbox

COG:

Center of gravity

DBS:

Deep brain stimulation

DWI:

Diffusion-weighted imaging

FWHM:

Full width at half maximum

H & Y:

Hoehn and Yahr

MED OFF/ON:

Medication off/on

MPRAGE:

Magnetization-prepared rapid gradient-echo

ROC:

Receiver operating characteristic

ROI:

Region of interest

SMA:

Supplementary motor area

STN:

Subthalamic nucleus

UPDRS:

Unified Parkinson’s disease rating scale

VTA:

Volume of tissue activation

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Acknowledgements

This work was supported by the German Research Foundation (DFG; CRC-TR-128).

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    Authors and Affiliations

    1. Department of Neurology, Johannes Gutenberg University, 55131, Mainz, Germany

      Nabin Koirala, Vinzenz Fleischer, Muthuraman Muthuraman & Sergiu Groppa

    2. Department of Neurosurgery, Johannes Gutenberg University, 55131, Mainz, Germany

      Martin Glaser

    3. Department of Neurology, University of Kiel, 24105, Kiel, Germany

      Kirsten E. Zeuner & Günther Deuschl

    4. Department of Neurology, University of Würzburg, 97080, Würzburg, Germany

      Jens Volkmann

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    1. Nabin Koirala
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    Correspondence to Sergiu Groppa.

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    Muthuraman Muthuraman and Sergiu Groppa have contributed equally.

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    Koirala, N., Fleischer, V., Glaser, M. et al. Frontal Lobe Connectivity and Network Community Characteristics are Associated with the Outcome of Subthalamic Nucleus Deep Brain Stimulation in Patients with Parkinson’s Disease. Brain Topogr 31, 311–321 (2018). https://doi.org/10.1007/s10548-017-0597-4

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