Normative vs. patient-specific brain connectivity in deep brain stimulation

Brain connectivity profiles seeding from deep brain stimulation (DBS) electrodes have emerged as informative tools to estimate outcome variability across DBS patients. Given the limitations of acquiring and processing patient-specific diffusion-weighted imaging data, a number of studies have employe...

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Main Authors: Qiang Wang, Harith Akram, Muthuraman Muthuraman, Gabriel Gonzalez-Escamilla, Sameer A. Sheth, Simón Oxenford, Fang-Cheng Yeh, Sergiu Groppa, Nora Vanegas-Arroyave, Ludvic Zrinzo, Ningfei Li, Andrea Kühn, Andreas Horn
Format: Article
Language:English
Published: Elsevier 2021-01-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S105381192030793X
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author Qiang Wang
Harith Akram
Muthuraman Muthuraman
Gabriel Gonzalez-Escamilla
Sameer A. Sheth
Simón Oxenford
Fang-Cheng Yeh
Sergiu Groppa
Nora Vanegas-Arroyave
Ludvic Zrinzo
Ningfei Li
Andrea Kühn
Andreas Horn
spellingShingle Qiang Wang
Harith Akram
Muthuraman Muthuraman
Gabriel Gonzalez-Escamilla
Sameer A. Sheth
Simón Oxenford
Fang-Cheng Yeh
Sergiu Groppa
Nora Vanegas-Arroyave
Ludvic Zrinzo
Ningfei Li
Andrea Kühn
Andreas Horn
Normative vs. patient-specific brain connectivity in deep brain stimulation
NeuroImage
Deep brain stimulation
Subthalamic nucleus
Parkinson's disease
Human connectome
Tractography
author_facet Qiang Wang
Harith Akram
Muthuraman Muthuraman
Gabriel Gonzalez-Escamilla
Sameer A. Sheth
Simón Oxenford
Fang-Cheng Yeh
Sergiu Groppa
Nora Vanegas-Arroyave
Ludvic Zrinzo
Ningfei Li
Andrea Kühn
Andreas Horn
author_sort Qiang Wang
title Normative vs. patient-specific brain connectivity in deep brain stimulation
title_short Normative vs. patient-specific brain connectivity in deep brain stimulation
title_full Normative vs. patient-specific brain connectivity in deep brain stimulation
title_fullStr Normative vs. patient-specific brain connectivity in deep brain stimulation
title_full_unstemmed Normative vs. patient-specific brain connectivity in deep brain stimulation
title_sort normative vs. patient-specific brain connectivity in deep brain stimulation
publisher Elsevier
series NeuroImage
issn 1095-9572
publishDate 2021-01-01
description Brain connectivity profiles seeding from deep brain stimulation (DBS) electrodes have emerged as informative tools to estimate outcome variability across DBS patients. Given the limitations of acquiring and processing patient-specific diffusion-weighted imaging data, a number of studies have employed normative atlases of the human connectome. To date, it remains unclear whether patient-specific connectivity information would strengthen the accuracy of such analyses. Here, we compared similarities and differences between patient-specific, disease-matched and normative structural connectivity data and their ability to predict clinical improvement.Data from 33 patients suffering from Parkinson's Disease who underwent surgery at three different centers were retrospectively collected. Stimulation-dependent connectivity profiles seeding from active contacts were estimated using three modalities, namely patient-specific diffusion-MRI data, age- and disease-matched or normative group connectome data (acquired in healthy young subjects). Based on these profiles, models of optimal connectivity were calculated and used to estimate clinical improvement in out of sample data.All three modalities resulted in highly similar optimal connectivity profiles that could largely reproduce findings from prior research based on this present novel multi-center cohort. In a data-driven approach that estimated optimal whole-brain connectivity profiles, out-of-sample predictions of clinical improvements were calculated. Using either patient-specific connectivity (R = 0.43 at p = 0.001), an age- and disease-matched group connectome (R = 0.25, p = 0.048) and a normative connectome based on healthy/young subjects (R = 0.31 at p = 0.028), significant predictions could be made.Our results of patient-specific connectivity and normative connectomes lead to similar main conclusions about which brain areas are associated with clinical improvement. Still, although results were not significantly different, they hint at the fact that patient-specific connectivity may bear the potential of explaining slightly more variance than group connectomes. Furthermore, use of normative connectomes involves datasets with high signal-to-noise acquired on specialized MRI hardware, while clinical datasets as the ones used here may not exactly match their quality. Our findings support the role of DBS electrode connectivity profiles as a promising method to investigate DBS effects and to potentially guide DBS programming.
topic Deep brain stimulation
Subthalamic nucleus
Parkinson's disease
Human connectome
Tractography
url http://www.sciencedirect.com/science/article/pii/S105381192030793X
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spelling doaj-a5652688ae574eab95719858fcd8a2e72020-12-17T04:46:56ZengElsevierNeuroImage1095-95722021-01-01224117307Normative vs. patient-specific brain connectivity in deep brain stimulationQiang Wang0Harith Akram1Muthuraman Muthuraman2Gabriel Gonzalez-Escamilla3Sameer A. Sheth4Simón Oxenford5Fang-Cheng Yeh6Sergiu Groppa7Nora Vanegas-Arroyave8Ludvic Zrinzo9Ningfei Li10Andrea Kühn11Andreas Horn12Movement Disorders & Neuromodulation Unit, Department for Neurology, Charité – University Medicine Berlin, Germany; Corresponding author.Unit of Functional Neurosurgery, UCL Queen Square Institute of Neurology, Queen Square, London WC1N 3BG, UK; Victor Horsley Department of Neurosurgery, National Hospital for Neurology and Neurosurgery, UCLH, Queen Square, London WC1N 3BG, UKMovement Disorders and Neurostimulation, Biomedical Statistics and Mulitmodal Signal Processing Unit, Department of Neurology, University Medical Center of the Johannes Gutenberg University, Mainz, GermanyMovement Disorders and Neurostimulation, Biomedical Statistics and Mulitmodal Signal Processing Unit, Department of Neurology, University Medical Center of the Johannes Gutenberg University, Mainz, GermanyDepartment of Neurosurgery, Baylor College of Medicine, Houston, TX, USAMovement Disorders & Neuromodulation Unit, Department for Neurology, Charité – University Medicine Berlin, GermanyDepartment of Neurological Surgery, University of Pittsburgh Medical Center, Pittsburgh, PA, USAMovement Disorders and Neurostimulation, Biomedical Statistics and Mulitmodal Signal Processing Unit, Department of Neurology, University Medical Center of the Johannes Gutenberg University, Mainz, GermanyDepartment of Neurology, Columbia University College of Physicians and Surgeons, New York, NY, USAUnit of Functional Neurosurgery, UCL Queen Square Institute of Neurology, Queen Square, London WC1N 3BG, UK; Victor Horsley Department of Neurosurgery, National Hospital for Neurology and Neurosurgery, UCLH, Queen Square, London WC1N 3BG, UKMovement Disorders & Neuromodulation Unit, Department for Neurology, Charité – University Medicine Berlin, GermanyMovement Disorders & Neuromodulation Unit, Department for Neurology, Charité – University Medicine Berlin, GermanyMovement Disorders & Neuromodulation Unit, Department for Neurology, Charité – University Medicine Berlin, GermanyBrain connectivity profiles seeding from deep brain stimulation (DBS) electrodes have emerged as informative tools to estimate outcome variability across DBS patients. Given the limitations of acquiring and processing patient-specific diffusion-weighted imaging data, a number of studies have employed normative atlases of the human connectome. To date, it remains unclear whether patient-specific connectivity information would strengthen the accuracy of such analyses. Here, we compared similarities and differences between patient-specific, disease-matched and normative structural connectivity data and their ability to predict clinical improvement.Data from 33 patients suffering from Parkinson's Disease who underwent surgery at three different centers were retrospectively collected. Stimulation-dependent connectivity profiles seeding from active contacts were estimated using three modalities, namely patient-specific diffusion-MRI data, age- and disease-matched or normative group connectome data (acquired in healthy young subjects). Based on these profiles, models of optimal connectivity were calculated and used to estimate clinical improvement in out of sample data.All three modalities resulted in highly similar optimal connectivity profiles that could largely reproduce findings from prior research based on this present novel multi-center cohort. In a data-driven approach that estimated optimal whole-brain connectivity profiles, out-of-sample predictions of clinical improvements were calculated. Using either patient-specific connectivity (R = 0.43 at p = 0.001), an age- and disease-matched group connectome (R = 0.25, p = 0.048) and a normative connectome based on healthy/young subjects (R = 0.31 at p = 0.028), significant predictions could be made.Our results of patient-specific connectivity and normative connectomes lead to similar main conclusions about which brain areas are associated with clinical improvement. Still, although results were not significantly different, they hint at the fact that patient-specific connectivity may bear the potential of explaining slightly more variance than group connectomes. Furthermore, use of normative connectomes involves datasets with high signal-to-noise acquired on specialized MRI hardware, while clinical datasets as the ones used here may not exactly match their quality. Our findings support the role of DBS electrode connectivity profiles as a promising method to investigate DBS effects and to potentially guide DBS programming.http://www.sciencedirect.com/science/article/pii/S105381192030793XDeep brain stimulationSubthalamic nucleusParkinson's diseaseHuman connectomeTractography