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Somatotopic Organization of Hyperdirect Pathway Projections From the Primary Motor Cortex in the Human Brain

BACKGROUND: The subthalamic nucleus (STN) is an effective neurosurgical target to improve motor symptoms in Parkinson's Disease (PD) patients. MR-guided Focused Ultrasound (MRgFUS) subthalamotomy is being explored as a therapeutic alternative to Deep Brain Stimulation (DBS) of the STN. The hype...

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Autores principales: Pujol, Sonia, Cabeen, Ryan P., Yelnik, Jérôme, François, Chantal, Fernandez Vidal, Sara, Karachi, Carine, Bardinet, Eric, Cosgrove, G. Rees, Kikinis, Ron
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9081715/
https://www.ncbi.nlm.nih.gov/pubmed/35547388
http://dx.doi.org/10.3389/fneur.2022.791092
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author Pujol, Sonia
Cabeen, Ryan P.
Yelnik, Jérôme
François, Chantal
Fernandez Vidal, Sara
Karachi, Carine
Bardinet, Eric
Cosgrove, G. Rees
Kikinis, Ron
author_facet Pujol, Sonia
Cabeen, Ryan P.
Yelnik, Jérôme
François, Chantal
Fernandez Vidal, Sara
Karachi, Carine
Bardinet, Eric
Cosgrove, G. Rees
Kikinis, Ron
author_sort Pujol, Sonia
collection PubMed
description BACKGROUND: The subthalamic nucleus (STN) is an effective neurosurgical target to improve motor symptoms in Parkinson's Disease (PD) patients. MR-guided Focused Ultrasound (MRgFUS) subthalamotomy is being explored as a therapeutic alternative to Deep Brain Stimulation (DBS) of the STN. The hyperdirect pathway provides a direct connection between the cortex and the STN and is likely to play a key role in the therapeutic effects of MRgFUS intervention in PD patients. OBJECTIVE: This study aims to investigate the topography and somatotopy of hyperdirect pathway projections from the primary motor cortex (M1). METHODS: We used advanced multi-fiber tractography and high-resolution diffusion MRI data acquired on five subjects of the Human Connectome Project (HCP) to reconstruct hyperdirect pathway projections from M1. Two neuroanatomy experts reviewed the anatomical accuracy of the tracts. We extracted the fascicles arising from the trunk, arm, hand, face and tongue area from the reconstructed pathways. We assessed the variability among subjects based on the fractional anisotropy (FA) and mean diffusivity (MD) of the fibers. We evaluated the spatial arrangement of the different fascicles using the Dice Similarity Coefficient (DSC) of spatial overlap and the centroids of the bundles. RESULTS: We successfully reconstructed hyperdirect pathway projections from M1 in all five subjects. The tracts were in agreement with the expected anatomy. We identified hyperdirect pathway fascicles projecting from the trunk, arm, hand, face and tongue area in all subjects. Tract-derived measurements showed low variability among subjects, and similar distributions of FA and MD values among the fascicles projecting from different M1 areas. We found an anterolateral somatotopic arrangement of the fascicles in the corona radiata, and an average overlap of 0.63 in the internal capsule and 0.65 in the zona incerta. CONCLUSION: Multi-fiber tractography combined with high-resolution diffusion MRI data enables the identification of the somatotopic organization of the hyperdirect pathway. Our preliminary results suggest that the subdivisions of the hyperdirect pathway projecting from the trunk, arm, hand, face, and tongue motor area are intermixed at the level of the zona incerta and posterior limb of the internal capsule, with a predominantly overlapping topographical organization in both regions. Subject-specific knowledge of the hyperdirect pathway somatotopy could help optimize target definition in MRgFUS intervention.
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spelling pubmed-90817152022-05-10 Somatotopic Organization of Hyperdirect Pathway Projections From the Primary Motor Cortex in the Human Brain Pujol, Sonia Cabeen, Ryan P. Yelnik, Jérôme François, Chantal Fernandez Vidal, Sara Karachi, Carine Bardinet, Eric Cosgrove, G. Rees Kikinis, Ron Front Neurol Neurology BACKGROUND: The subthalamic nucleus (STN) is an effective neurosurgical target to improve motor symptoms in Parkinson's Disease (PD) patients. MR-guided Focused Ultrasound (MRgFUS) subthalamotomy is being explored as a therapeutic alternative to Deep Brain Stimulation (DBS) of the STN. The hyperdirect pathway provides a direct connection between the cortex and the STN and is likely to play a key role in the therapeutic effects of MRgFUS intervention in PD patients. OBJECTIVE: This study aims to investigate the topography and somatotopy of hyperdirect pathway projections from the primary motor cortex (M1). METHODS: We used advanced multi-fiber tractography and high-resolution diffusion MRI data acquired on five subjects of the Human Connectome Project (HCP) to reconstruct hyperdirect pathway projections from M1. Two neuroanatomy experts reviewed the anatomical accuracy of the tracts. We extracted the fascicles arising from the trunk, arm, hand, face and tongue area from the reconstructed pathways. We assessed the variability among subjects based on the fractional anisotropy (FA) and mean diffusivity (MD) of the fibers. We evaluated the spatial arrangement of the different fascicles using the Dice Similarity Coefficient (DSC) of spatial overlap and the centroids of the bundles. RESULTS: We successfully reconstructed hyperdirect pathway projections from M1 in all five subjects. The tracts were in agreement with the expected anatomy. We identified hyperdirect pathway fascicles projecting from the trunk, arm, hand, face and tongue area in all subjects. Tract-derived measurements showed low variability among subjects, and similar distributions of FA and MD values among the fascicles projecting from different M1 areas. We found an anterolateral somatotopic arrangement of the fascicles in the corona radiata, and an average overlap of 0.63 in the internal capsule and 0.65 in the zona incerta. CONCLUSION: Multi-fiber tractography combined with high-resolution diffusion MRI data enables the identification of the somatotopic organization of the hyperdirect pathway. Our preliminary results suggest that the subdivisions of the hyperdirect pathway projecting from the trunk, arm, hand, face, and tongue motor area are intermixed at the level of the zona incerta and posterior limb of the internal capsule, with a predominantly overlapping topographical organization in both regions. Subject-specific knowledge of the hyperdirect pathway somatotopy could help optimize target definition in MRgFUS intervention. Frontiers Media S.A. 2022-04-25 /pmc/articles/PMC9081715/ /pubmed/35547388 http://dx.doi.org/10.3389/fneur.2022.791092 Text en Copyright © 2022 Pujol, Cabeen, Yelnik, François, Fernandez Vidal, Karachi, Bardinet, Cosgrove and Kikinis. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neurology
Pujol, Sonia
Cabeen, Ryan P.
Yelnik, Jérôme
François, Chantal
Fernandez Vidal, Sara
Karachi, Carine
Bardinet, Eric
Cosgrove, G. Rees
Kikinis, Ron
Somatotopic Organization of Hyperdirect Pathway Projections From the Primary Motor Cortex in the Human Brain
title Somatotopic Organization of Hyperdirect Pathway Projections From the Primary Motor Cortex in the Human Brain
title_full Somatotopic Organization of Hyperdirect Pathway Projections From the Primary Motor Cortex in the Human Brain
title_fullStr Somatotopic Organization of Hyperdirect Pathway Projections From the Primary Motor Cortex in the Human Brain
title_full_unstemmed Somatotopic Organization of Hyperdirect Pathway Projections From the Primary Motor Cortex in the Human Brain
title_short Somatotopic Organization of Hyperdirect Pathway Projections From the Primary Motor Cortex in the Human Brain
title_sort somatotopic organization of hyperdirect pathway projections from the primary motor cortex in the human brain
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9081715/
https://www.ncbi.nlm.nih.gov/pubmed/35547388
http://dx.doi.org/10.3389/fneur.2022.791092
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