Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease

Objectives Firstly, to identify subthalamic region stimulation clusters that predict maximum improvement in rigidity, bradykinesia and tremor, or emergence of side-effects; and secondly, to map-out the cortical fingerprint, mediated by the hyperdirect pathways which predict maximum efficacy. Metho...

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Main Authors: Akram, Harith, Sotiropoulos, Stamatios N., Jbabdi, Saad, Georgiev, Dejan, Mahlknecht, Philipp, Hyam, Jonathan, Foltynie, Thomas, Limousin, Patricia, De Vita, Enrico, Jahanshahi, Marjan, Hariz, Marwan, Ashburner, John, Behrens, Timothy, Zrinzo, Ludvic
Format: Article
Published: Elsevier 2017
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Online Access:https://eprints.nottingham.ac.uk/44103/
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author Akram, Harith
Sotiropoulos, Stamatios N.
Jbabdi, Saad
Georgiev, Dejan
Mahlknecht, Philipp
Hyam, Jonathan
Foltynie, Thomas
Limousin, Patricia
De Vita, Enrico
Jahanshahi, Marjan
Hariz, Marwan
Ashburner, John
Behrens, Timothy
Zrinzo, Ludvic
author_facet Akram, Harith
Sotiropoulos, Stamatios N.
Jbabdi, Saad
Georgiev, Dejan
Mahlknecht, Philipp
Hyam, Jonathan
Foltynie, Thomas
Limousin, Patricia
De Vita, Enrico
Jahanshahi, Marjan
Hariz, Marwan
Ashburner, John
Behrens, Timothy
Zrinzo, Ludvic
author_sort Akram, Harith
building Nottingham Research Data Repository
collection Online Access
description Objectives Firstly, to identify subthalamic region stimulation clusters that predict maximum improvement in rigidity, bradykinesia and tremor, or emergence of side-effects; and secondly, to map-out the cortical fingerprint, mediated by the hyperdirect pathways which predict maximum efficacy. Methods High angular resolution diffusion imaging in twenty patients with advanced Parkinson’s disease was acquired prior to bilateral subthalamic nucleus deep brain stimulation. All contacts were screened one-year from surgery for efficacy and side-effects at different amplitudes. Voxel-based statistical analysis of volumes of tissue activated models was used to identify significant treatment clusters. Probabilistic tractography was employed to identify cortical connectivity patterns associated with treatment efficacy. Results All patients responded well to treatment (46% mean improvement off medication UPDRS-III [p<0.0001]) without significant adverse events. Cluster corresponding to maximum improvement in tremor was in the posterior, superior and lateral portion of the nucleus. Clusters corresponding to improvement in bradykinesia and rigidity were nearer the superior border in a further medial and posterior location. The rigidity cluster extended beyond the superior border to the area of the zona incerta and Forel-H2 field. When the clusters where averaged, the coordinates of the area with maximum overall efficacy was X=-10(-9.5), Y=-13(-1) and Z=-7(-3) in MNI(AC-PC) space. Cortical connectivity to primary motor area was predictive of higher improvement in tremor; whilst that to supplementary motor area was predictive of improvement in bradykinesia and rigidity; and connectivity to prefrontal cortex was predictive of improvement in rigidity. Interpretation These findings support the presence of overlapping stimulation sites within the subthalamic nucleus and its superior border, with different cortical connectivity patterns, associated with maximum improvement in tremor, rigidity and bradykinesia.
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spelling nottingham-441032024-08-15T15:31:28Z https://eprints.nottingham.ac.uk/44103/ Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease Akram, Harith Sotiropoulos, Stamatios N. Jbabdi, Saad Georgiev, Dejan Mahlknecht, Philipp Hyam, Jonathan Foltynie, Thomas Limousin, Patricia De Vita, Enrico Jahanshahi, Marjan Hariz, Marwan Ashburner, John Behrens, Timothy Zrinzo, Ludvic Objectives Firstly, to identify subthalamic region stimulation clusters that predict maximum improvement in rigidity, bradykinesia and tremor, or emergence of side-effects; and secondly, to map-out the cortical fingerprint, mediated by the hyperdirect pathways which predict maximum efficacy. Methods High angular resolution diffusion imaging in twenty patients with advanced Parkinson’s disease was acquired prior to bilateral subthalamic nucleus deep brain stimulation. All contacts were screened one-year from surgery for efficacy and side-effects at different amplitudes. Voxel-based statistical analysis of volumes of tissue activated models was used to identify significant treatment clusters. Probabilistic tractography was employed to identify cortical connectivity patterns associated with treatment efficacy. Results All patients responded well to treatment (46% mean improvement off medication UPDRS-III [p<0.0001]) without significant adverse events. Cluster corresponding to maximum improvement in tremor was in the posterior, superior and lateral portion of the nucleus. Clusters corresponding to improvement in bradykinesia and rigidity were nearer the superior border in a further medial and posterior location. The rigidity cluster extended beyond the superior border to the area of the zona incerta and Forel-H2 field. When the clusters where averaged, the coordinates of the area with maximum overall efficacy was X=-10(-9.5), Y=-13(-1) and Z=-7(-3) in MNI(AC-PC) space. Cortical connectivity to primary motor area was predictive of higher improvement in tremor; whilst that to supplementary motor area was predictive of improvement in bradykinesia and rigidity; and connectivity to prefrontal cortex was predictive of improvement in rigidity. Interpretation These findings support the presence of overlapping stimulation sites within the subthalamic nucleus and its superior border, with different cortical connectivity patterns, associated with maximum improvement in tremor, rigidity and bradykinesia. Elsevier 2017-09 Article PeerReviewed Akram, Harith, Sotiropoulos, Stamatios N., Jbabdi, Saad, Georgiev, Dejan, Mahlknecht, Philipp, Hyam, Jonathan, Foltynie, Thomas, Limousin, Patricia, De Vita, Enrico, Jahanshahi, Marjan, Hariz, Marwan, Ashburner, John, Behrens, Timothy and Zrinzo, Ludvic (2017) Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease. NeuroImage, 158 . pp. 332-345. ISSN 1095-9572 Diffusion weighted imaging (DWI) connectivity Parkinson’s disease (PD) subthalamic nucleus (STN) volume of tissue activated (VTA) hyperdirect pathway http://www.sciencedirect.com/science/article/pii/S1053811917305803 doi:10.1016/j.neuroimage.2017.07.012 doi:10.1016/j.neuroimage.2017.07.012
spellingShingle Diffusion weighted imaging (DWI)
connectivity
Parkinson’s disease (PD)
subthalamic nucleus (STN)
volume of tissue activated (VTA)
hyperdirect pathway
Akram, Harith
Sotiropoulos, Stamatios N.
Jbabdi, Saad
Georgiev, Dejan
Mahlknecht, Philipp
Hyam, Jonathan
Foltynie, Thomas
Limousin, Patricia
De Vita, Enrico
Jahanshahi, Marjan
Hariz, Marwan
Ashburner, John
Behrens, Timothy
Zrinzo, Ludvic
Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease
title Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease
title_full Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease
title_fullStr Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease
title_full_unstemmed Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease
title_short Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease
title_sort subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in parkinson’s disease
topic Diffusion weighted imaging (DWI)
connectivity
Parkinson’s disease (PD)
subthalamic nucleus (STN)
volume of tissue activated (VTA)
hyperdirect pathway
url https://eprints.nottingham.ac.uk/44103/
https://eprints.nottingham.ac.uk/44103/
https://eprints.nottingham.ac.uk/44103/