High angular resolution diffusion-weighted imaging and higher order tractography of the white matter tracts in the anterior thalamic area: Insights into deep brain stimulation targeting

Background: Deep brain stimulation of the anterior nucleus of the thalamus (ANT) is emerging EU/US-approved form of therapy for drug-resistant focal epilepsy. Its mechanism of action is not yet fully understood, and the patient outcomes in epilepsy appear less consistent compared to for instance mov...

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Main Authors: Ruhunur Özdemir, Kai Lehtimäki, Eetu Siitama, Timo Möttönen, Joonas Haapasalo, Soila Järvenpää, Hannu Eskola, Jukka Peltola
Format: Article
Language:English
Published: Elsevier 2024-09-01
Series:NeuroImage: Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2666956024000163
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author Ruhunur Özdemir
Kai Lehtimäki
Eetu Siitama
Timo Möttönen
Joonas Haapasalo
Soila Järvenpää
Hannu Eskola
Jukka Peltola
author_facet Ruhunur Özdemir
Kai Lehtimäki
Eetu Siitama
Timo Möttönen
Joonas Haapasalo
Soila Järvenpää
Hannu Eskola
Jukka Peltola
author_sort Ruhunur Özdemir
collection DOAJ
description Background: Deep brain stimulation of the anterior nucleus of the thalamus (ANT) is emerging EU/US-approved form of therapy for drug-resistant focal epilepsy. Its mechanism of action is not yet fully understood, and the patient outcomes in epilepsy appear less consistent compared to for instance movement disorders. Furthermore, very little anatomy-based information, such as tractography of relevant fiber systems, exists guiding DBS therapy at present. Objective: To demonstrate ANT-related fiber systems based on histology in vivo employing multi-shell/multi-tissue constrained spherical deconvolution (MSMT-CSD) based deterministic and probabilistic tractography using a sophisticated scanning protocol of 3T high angular resolution diffusion-weighted imaging (HARDI) data in healthy volunteers. Method: HARDI data was acquired from five healthy volunteers in a 3T Siemens MAGNETOM Skyra Magnetic resonance imaging (MRI) machine using multiple b-values (1000, 2000, and 3000), 64 directions, and further preprocessed for tractography. MSMT-CSD-based deterministic and probabilistic tractography was performed from selected fiber systems based on existing literature. Results: Multiple fiber systems were identified: The anterior thalamic radiation (ANT), the thalamo-cingulate tract, the inferior thalamic peduncle (with remote termination areas in the amygdala, the ventral tegmental area, and the occipital cortex), and the mammillothalamic tract. In addition, we observed three parallel connections to the hippocampus (via the cingulum bundle, the fornix, and the temporo-pulvinar pathway). Interestingly, different seed areas in ANT complex mimicking DBS contact locations resulted in visualization of different fiber systems. Discussion: The connections of the ANT are complex and different stimulation sites are likely to affect different networks depending on lead locations and the selection of the active contact. Conclusions: In-depth understanding of the network of anatomical structures related to the ANT is likely to influence therapy outcomes. A hypothetical model of neuronal networks affected by different DBS lead contact locations is proposed. A more profound understanding of neuroanatomic characteristics may guide stereotactic implantation and subsequent programming to optimize outcomes.
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spelling doaj-art-4b481ffccdda4639bd11419f50de5e942025-08-20T03:36:26ZengElsevierNeuroImage: Reports2666-95602024-09-014310021010.1016/j.ynirp.2024.100210High angular resolution diffusion-weighted imaging and higher order tractography of the white matter tracts in the anterior thalamic area: Insights into deep brain stimulation targetingRuhunur Özdemir0Kai Lehtimäki1Eetu Siitama2Timo Möttönen3Joonas Haapasalo4Soila Järvenpää5Hannu Eskola6Jukka Peltola7Faculty of Medicine and Health Technology, University of Tampere, Arvo Ylpön Katu 34, 33520, Tampere, Finland; Corresponding author.Department of Neurosurgery, Tampere University Hospital, Wellbeing Services County of Pirkanmaa, PL 272, 33101, Tampere, FinlandFaculty of Medicine and Health Technology, University of Tampere, Arvo Ylpön Katu 34, 33520, Tampere, Finland; Department of Medical Physics, Medical Imaging Center, Tampere University Hospital, Tampere, Finland; Wellbeing County Service of Pirkanmaa, PL 272, 33101, Tampere, FinlandDepartment of Neurosurgery, Tampere University Hospital, Wellbeing Services County of Pirkanmaa, PL 272, 33101, Tampere, FinlandDepartment of Neurosurgery, Tampere University Hospital, Wellbeing Services County of Pirkanmaa, PL 272, 33101, Tampere, FinlandDepartment of Neurology, Tampere University Hospital, Wellbeing Services County of Pirkanmaa, PL 272, 33101, Tampere, FinlandFaculty of Medicine and Health Technology, University of Tampere, Arvo Ylpön Katu 34, 33520, Tampere, FinlandFaculty of Medicine and Health Technology, University of Tampere, Arvo Ylpön Katu 34, 33520, Tampere, Finland; Department of Neurology, Tampere University Hospital, Wellbeing Services County of Pirkanmaa, PL 272, 33101, Tampere, FinlandBackground: Deep brain stimulation of the anterior nucleus of the thalamus (ANT) is emerging EU/US-approved form of therapy for drug-resistant focal epilepsy. Its mechanism of action is not yet fully understood, and the patient outcomes in epilepsy appear less consistent compared to for instance movement disorders. Furthermore, very little anatomy-based information, such as tractography of relevant fiber systems, exists guiding DBS therapy at present. Objective: To demonstrate ANT-related fiber systems based on histology in vivo employing multi-shell/multi-tissue constrained spherical deconvolution (MSMT-CSD) based deterministic and probabilistic tractography using a sophisticated scanning protocol of 3T high angular resolution diffusion-weighted imaging (HARDI) data in healthy volunteers. Method: HARDI data was acquired from five healthy volunteers in a 3T Siemens MAGNETOM Skyra Magnetic resonance imaging (MRI) machine using multiple b-values (1000, 2000, and 3000), 64 directions, and further preprocessed for tractography. MSMT-CSD-based deterministic and probabilistic tractography was performed from selected fiber systems based on existing literature. Results: Multiple fiber systems were identified: The anterior thalamic radiation (ANT), the thalamo-cingulate tract, the inferior thalamic peduncle (with remote termination areas in the amygdala, the ventral tegmental area, and the occipital cortex), and the mammillothalamic tract. In addition, we observed three parallel connections to the hippocampus (via the cingulum bundle, the fornix, and the temporo-pulvinar pathway). Interestingly, different seed areas in ANT complex mimicking DBS contact locations resulted in visualization of different fiber systems. Discussion: The connections of the ANT are complex and different stimulation sites are likely to affect different networks depending on lead locations and the selection of the active contact. Conclusions: In-depth understanding of the network of anatomical structures related to the ANT is likely to influence therapy outcomes. A hypothetical model of neuronal networks affected by different DBS lead contact locations is proposed. A more profound understanding of neuroanatomic characteristics may guide stereotactic implantation and subsequent programming to optimize outcomes.http://www.sciencedirect.com/science/article/pii/S2666956024000163High angular resolution diffusion-weighted imaging (HARDI)TractographyMulti-shell multi-tissue constrained spherical deconvolution (MSMT-CSD)EpilepsyDeep brain stimulationAnterior nucleus of thalamus
spellingShingle Ruhunur Özdemir
Kai Lehtimäki
Eetu Siitama
Timo Möttönen
Joonas Haapasalo
Soila Järvenpää
Hannu Eskola
Jukka Peltola
High angular resolution diffusion-weighted imaging and higher order tractography of the white matter tracts in the anterior thalamic area: Insights into deep brain stimulation targeting
NeuroImage: Reports
High angular resolution diffusion-weighted imaging (HARDI)
Tractography
Multi-shell multi-tissue constrained spherical deconvolution (MSMT-CSD)
Epilepsy
Deep brain stimulation
Anterior nucleus of thalamus
title High angular resolution diffusion-weighted imaging and higher order tractography of the white matter tracts in the anterior thalamic area: Insights into deep brain stimulation targeting
title_full High angular resolution diffusion-weighted imaging and higher order tractography of the white matter tracts in the anterior thalamic area: Insights into deep brain stimulation targeting
title_fullStr High angular resolution diffusion-weighted imaging and higher order tractography of the white matter tracts in the anterior thalamic area: Insights into deep brain stimulation targeting
title_full_unstemmed High angular resolution diffusion-weighted imaging and higher order tractography of the white matter tracts in the anterior thalamic area: Insights into deep brain stimulation targeting
title_short High angular resolution diffusion-weighted imaging and higher order tractography of the white matter tracts in the anterior thalamic area: Insights into deep brain stimulation targeting
title_sort high angular resolution diffusion weighted imaging and higher order tractography of the white matter tracts in the anterior thalamic area insights into deep brain stimulation targeting
topic High angular resolution diffusion-weighted imaging (HARDI)
Tractography
Multi-shell multi-tissue constrained spherical deconvolution (MSMT-CSD)
Epilepsy
Deep brain stimulation
Anterior nucleus of thalamus
url http://www.sciencedirect.com/science/article/pii/S2666956024000163
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