Structural connectivity of the ANT region based on human ex-vivo and HCP data.: Relevance for DBS in ANT for epilepsy

Milan Majtanik; Frans Gielen; Volker Arnd Coenen; Kai Lehtimäki; Jürgen Konrad Mai

doi:10.1016/j.neuroimage.2022.119551

Structural connectivity of the ANT region based on human ex-vivo and HCP data. Relevance for DBS in ANT for epilepsy

Milan Majtanik
, Frans Gielen
, Volker Arnd Coenen
, Kai Lehtimäki
, Jürgen Konrad Mai^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Scientific › peer-review

20 Citations (Scopus)

24 Downloads (Pure)

Abstract

Objective: Deep Brain Stimulation (DBS) in the Anterior Nucleus of the Thalamus (ANT) has been shown to be a safe and efficacious treatment option for patients with Drug-Resitant focal Epilepsy (DRE). The ANT has been selected frequently in open and controlled studies for bilateral DBS. There is a substantial variability in ANT-DBS outcomes which is not fully understood. These outcomes might not be explained by the target location alone but potentially depend on the connectivity of the mere stimulation site with the epilepsy onset-associated brain regions. The likely sub-components of this anatomy are fiber pathways which penetrate or touch the ANT region and constitute a complex and dense fiber network which has not been described so far. A detailed characterization of this ANT associated fiber anatomy may therefore help to identify which areas are associated with positive or negative outcomes of ANT-DBS. Furthermore, prediction properties in individual ANT-DBS cases might be tested. In this work we aim to generate an anatomically detailed map of candidate fiber structures which might in the future lead to a holistic image of structural connectivity of the ANT region. Methods: To resolve the various components of the complex fiber network connected to the ANT we used a synthetic pathway reconstruction method that combines anatomical fiber tracking with dMRI-based tractography and iteratively created an anatomical high-resolution fiber map representing the most important bundles related to the ANT. Results: The anatomically detailed 3D representation of the fibers in the ANT region generated with the synthetic pathway reconstruction method incorporates multiple anatomically defined fiber bundles with their course, orientation, connectivity and relative strength. Distinctive positions within the ANT region have a different hierarchical profile with respect to the stimulation-activated fiber bundles. This detailed connectivity map, which is embedded into the topographic map of the MNI brain, provides novel opportunities to analyze the outcomes of the ANT-DBS studies. Conclusion: Our synthetic reconstruction method provides the first anatomically realistic fiber pathway map in the human ANT region incorporating histological and structural MRI data. We propose that this complex ANT fiber network can be used for detailed analysis of the outcomes of DBS studies and potentially for visualization during the stimulation planning procedures. The connectivity map might also facilitate surgical planning and will help to simulate the complex ANT connectivity. Possible activation patterns that may be elicited by electrodes in different positions in the ANT region will help to understand clinically diverse outcomes based on this new dense fiber network map. As a consequence this work might in the future help to improve individual outcomes in ANT-DBS.

Original language	English
Article number	119551
Journal	NeuroImage
Volume	262
DOIs	https://doi.org/10.1016/j.neuroimage.2022.119551
Publication status	Published - 15 Nov 2022
Publication type	A1 Journal article-refereed

Funding

In the preparation of this work we used data obtained from the MGH-USC Human Connectome Project (HCP) database (https://ida.loni.usc.edu/login.jsp); from Prof. Dr. Marc Tittgemeyer, MPI Cologne; Translational Neurocircuitry Group; from Prof. Alard Roebroek, Faculty of Psychology and Neuroscience, Computational Brain Connectivity lab (CBClab) EV Maastricht. Data were provided by the Human Connectome Project (HCP); the Washington University, University of Minnesota, and Oxford University Consortium (Principal Investigators David Van Essen and Kamil Ugurbil; Grant No. 1U54MH091657) funded by 16 NIH institutes and centers that support the NIH Blueprint for Neuroscience Research; and the McDonnell Center for Systems Neuroscience at Washington University.

Publication forum classification

Publication forum level 2

ASJC Scopus subject areas

Neurology
Cognitive Neuroscience

Access to Document

10.1016/j.neuroimage.2022.119551Licence: CC BY-NC-ND

1-s2.0-S1053811922006668-mainFinal published version, 5.31 MBLicence: CC BY-NC-ND

https://urn.fi/URN:NBN:fi:tuni-202209137000Licence: CC BY-NC-ND

Cite this

@article{f90a6c7da53e48b2bf287b9d7dd3d094,

title = "Structural connectivity of the ANT region based on human ex-vivo and HCP data.: Relevance for DBS in ANT for epilepsy",

abstract = "Objective: Deep Brain Stimulation (DBS) in the Anterior Nucleus of the Thalamus (ANT) has been shown to be a safe and efficacious treatment option for patients with Drug-Resitant focal Epilepsy (DRE). The ANT has been selected frequently in open and controlled studies for bilateral DBS. There is a substantial variability in ANT-DBS outcomes which is not fully understood. These outcomes might not be explained by the target location alone but potentially depend on the connectivity of the mere stimulation site with the epilepsy onset-associated brain regions. The likely sub-components of this anatomy are fiber pathways which penetrate or touch the ANT region and constitute a complex and dense fiber network which has not been described so far. A detailed characterization of this ANT associated fiber anatomy may therefore help to identify which areas are associated with positive or negative outcomes of ANT-DBS. Furthermore, prediction properties in individual ANT-DBS cases might be tested. In this work we aim to generate an anatomically detailed map of candidate fiber structures which might in the future lead to a holistic image of structural connectivity of the ANT region. Methods: To resolve the various components of the complex fiber network connected to the ANT we used a synthetic pathway reconstruction method that combines anatomical fiber tracking with dMRI-based tractography and iteratively created an anatomical high-resolution fiber map representing the most important bundles related to the ANT. Results: The anatomically detailed 3D representation of the fibers in the ANT region generated with the synthetic pathway reconstruction method incorporates multiple anatomically defined fiber bundles with their course, orientation, connectivity and relative strength. Distinctive positions within the ANT region have a different hierarchical profile with respect to the stimulation-activated fiber bundles. This detailed connectivity map, which is embedded into the topographic map of the MNI brain, provides novel opportunities to analyze the outcomes of the ANT-DBS studies. Conclusion: Our synthetic reconstruction method provides the first anatomically realistic fiber pathway map in the human ANT region incorporating histological and structural MRI data. We propose that this complex ANT fiber network can be used for detailed analysis of the outcomes of DBS studies and potentially for visualization during the stimulation planning procedures. The connectivity map might also facilitate surgical planning and will help to simulate the complex ANT connectivity. Possible activation patterns that may be elicited by electrodes in different positions in the ANT region will help to understand clinically diverse outcomes based on this new dense fiber network map. As a consequence this work might in the future help to improve individual outcomes in ANT-DBS.",

author = "Milan Majtanik and Frans Gielen and Coenen, \{Volker Arnd\} and Kai Lehtim{\"a}ki and Mai, \{J{\"u}rgen Konrad\}",

note = "Funding Information: In the preparation of this work we used data obtained from the MGH-USC Human Connectome Project (HCP) database (https://ida.loni.usc.edu/login.jsp); from Prof. Dr. Marc Tittgemeyer, MPI Cologne; Translational Neurocircuitry Group; from Prof. Alard Roebroek, Faculty of Psychology and Neuroscience, Computational Brain Connectivity lab (CBClab) EV Maastricht. Funding Information: Data were provided by the Human Connectome Project (HCP); the Washington University, University of Minnesota, and Oxford University Consortium (Principal Investigators David Van Essen and Kamil Ugurbil; Grant No. 1U54MH091657) funded by 16 NIH institutes and centers that support the NIH Blueprint for Neuroscience Research; and the McDonnell Center for Systems Neuroscience at Washington University. Publisher Copyright: {\textcopyright} 2022",

year = "2022",

month = nov,

day = "15",

doi = "10.1016/j.neuroimage.2022.119551",

language = "English",

volume = "262",

journal = "NeuroImage",

issn = "1053-8119",

publisher = "Academic Press",

}

TY - JOUR

T1 - Structural connectivity of the ANT region based on human ex-vivo and HCP data.

T2 - Relevance for DBS in ANT for epilepsy

AU - Majtanik, Milan

AU - Gielen, Frans

AU - Coenen, Volker Arnd

AU - Lehtimäki, Kai

AU - Mai, Jürgen Konrad

N1 - Funding Information: In the preparation of this work we used data obtained from the MGH-USC Human Connectome Project (HCP) database (https://ida.loni.usc.edu/login.jsp); from Prof. Dr. Marc Tittgemeyer, MPI Cologne; Translational Neurocircuitry Group; from Prof. Alard Roebroek, Faculty of Psychology and Neuroscience, Computational Brain Connectivity lab (CBClab) EV Maastricht. Funding Information: Data were provided by the Human Connectome Project (HCP); the Washington University, University of Minnesota, and Oxford University Consortium (Principal Investigators David Van Essen and Kamil Ugurbil; Grant No. 1U54MH091657) funded by 16 NIH institutes and centers that support the NIH Blueprint for Neuroscience Research; and the McDonnell Center for Systems Neuroscience at Washington University. Publisher Copyright: © 2022

PY - 2022/11/15

Y1 - 2022/11/15

N2 - Objective: Deep Brain Stimulation (DBS) in the Anterior Nucleus of the Thalamus (ANT) has been shown to be a safe and efficacious treatment option for patients with Drug-Resitant focal Epilepsy (DRE). The ANT has been selected frequently in open and controlled studies for bilateral DBS. There is a substantial variability in ANT-DBS outcomes which is not fully understood. These outcomes might not be explained by the target location alone but potentially depend on the connectivity of the mere stimulation site with the epilepsy onset-associated brain regions. The likely sub-components of this anatomy are fiber pathways which penetrate or touch the ANT region and constitute a complex and dense fiber network which has not been described so far. A detailed characterization of this ANT associated fiber anatomy may therefore help to identify which areas are associated with positive or negative outcomes of ANT-DBS. Furthermore, prediction properties in individual ANT-DBS cases might be tested. In this work we aim to generate an anatomically detailed map of candidate fiber structures which might in the future lead to a holistic image of structural connectivity of the ANT region. Methods: To resolve the various components of the complex fiber network connected to the ANT we used a synthetic pathway reconstruction method that combines anatomical fiber tracking with dMRI-based tractography and iteratively created an anatomical high-resolution fiber map representing the most important bundles related to the ANT. Results: The anatomically detailed 3D representation of the fibers in the ANT region generated with the synthetic pathway reconstruction method incorporates multiple anatomically defined fiber bundles with their course, orientation, connectivity and relative strength. Distinctive positions within the ANT region have a different hierarchical profile with respect to the stimulation-activated fiber bundles. This detailed connectivity map, which is embedded into the topographic map of the MNI brain, provides novel opportunities to analyze the outcomes of the ANT-DBS studies. Conclusion: Our synthetic reconstruction method provides the first anatomically realistic fiber pathway map in the human ANT region incorporating histological and structural MRI data. We propose that this complex ANT fiber network can be used for detailed analysis of the outcomes of DBS studies and potentially for visualization during the stimulation planning procedures. The connectivity map might also facilitate surgical planning and will help to simulate the complex ANT connectivity. Possible activation patterns that may be elicited by electrodes in different positions in the ANT region will help to understand clinically diverse outcomes based on this new dense fiber network map. As a consequence this work might in the future help to improve individual outcomes in ANT-DBS.

AB - Objective: Deep Brain Stimulation (DBS) in the Anterior Nucleus of the Thalamus (ANT) has been shown to be a safe and efficacious treatment option for patients with Drug-Resitant focal Epilepsy (DRE). The ANT has been selected frequently in open and controlled studies for bilateral DBS. There is a substantial variability in ANT-DBS outcomes which is not fully understood. These outcomes might not be explained by the target location alone but potentially depend on the connectivity of the mere stimulation site with the epilepsy onset-associated brain regions. The likely sub-components of this anatomy are fiber pathways which penetrate or touch the ANT region and constitute a complex and dense fiber network which has not been described so far. A detailed characterization of this ANT associated fiber anatomy may therefore help to identify which areas are associated with positive or negative outcomes of ANT-DBS. Furthermore, prediction properties in individual ANT-DBS cases might be tested. In this work we aim to generate an anatomically detailed map of candidate fiber structures which might in the future lead to a holistic image of structural connectivity of the ANT region. Methods: To resolve the various components of the complex fiber network connected to the ANT we used a synthetic pathway reconstruction method that combines anatomical fiber tracking with dMRI-based tractography and iteratively created an anatomical high-resolution fiber map representing the most important bundles related to the ANT. Results: The anatomically detailed 3D representation of the fibers in the ANT region generated with the synthetic pathway reconstruction method incorporates multiple anatomically defined fiber bundles with their course, orientation, connectivity and relative strength. Distinctive positions within the ANT region have a different hierarchical profile with respect to the stimulation-activated fiber bundles. This detailed connectivity map, which is embedded into the topographic map of the MNI brain, provides novel opportunities to analyze the outcomes of the ANT-DBS studies. Conclusion: Our synthetic reconstruction method provides the first anatomically realistic fiber pathway map in the human ANT region incorporating histological and structural MRI data. We propose that this complex ANT fiber network can be used for detailed analysis of the outcomes of DBS studies and potentially for visualization during the stimulation planning procedures. The connectivity map might also facilitate surgical planning and will help to simulate the complex ANT connectivity. Possible activation patterns that may be elicited by electrodes in different positions in the ANT region will help to understand clinically diverse outcomes based on this new dense fiber network map. As a consequence this work might in the future help to improve individual outcomes in ANT-DBS.

U2 - 10.1016/j.neuroimage.2022.119551

DO - 10.1016/j.neuroimage.2022.119551

M3 - Article

C2 - 35948264

AN - SCOPUS:85136538451

SN - 1053-8119

VL - 262

JO - NeuroImage

JF - NeuroImage

M1 - 119551

ER -