Whole-brain network transitions within the framework of ignition and transfer entropy following VIM-MRgFUS in essential tremor patients

Magnetic resonance-guided focused ultrasound (MRgFUS) lesioning of the ventralis intermedius nucleus (VIM) has shown promise in treating drug-refractory essential tremor (ET). It remains unknown whether focal VIM lesions by MRgFUS have broader restorative effects on information flow within the whole...

Full description

Bibliographic Details
Main Authors: Julia M. Lueckel, Neeraj Upadhyay, Veronika Purrer, Angelika Maurer, Valeri Borger, Alexander Radbruch, Ulrike Attenberger, Ullrich Wuellner, Rajanikant Panda, Henning Boecker
Format: Article
Language:English
Published: Elsevier 2023-05-01
Series:Brain Stimulation
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1935861X23017734
_version_ 1797798081969782784
author Julia M. Lueckel
Neeraj Upadhyay
Veronika Purrer
Angelika Maurer
Valeri Borger
Alexander Radbruch
Ulrike Attenberger
Ullrich Wuellner
Rajanikant Panda
Henning Boecker
author_facet Julia M. Lueckel
Neeraj Upadhyay
Veronika Purrer
Angelika Maurer
Valeri Borger
Alexander Radbruch
Ulrike Attenberger
Ullrich Wuellner
Rajanikant Panda
Henning Boecker
author_sort Julia M. Lueckel
collection DOAJ
description Magnetic resonance-guided focused ultrasound (MRgFUS) lesioning of the ventralis intermedius nucleus (VIM) has shown promise in treating drug-refractory essential tremor (ET). It remains unknown whether focal VIM lesions by MRgFUS have broader restorative effects on information flow within the whole-brain network of ET patients. We applied an information-theoretical approach based on intrinsic ignition and the concept of transfer entropy (TE) to assess the spatiotemporal dynamics after VIM-MRgFUS. Eighteen ET patients (mean age 71.44 years) underwent repeated 3T resting-state functional magnetic resonance imaging combined with Clinical Rating Scale for Tremor (CRST) assessments one day before (T0) and one month (T1) and six months (T2) post-MRgFUS, respectively. We observed increased whole brain ignition-driven mean integration (IDMI) at T1 (p < 0.05), along with trend increases at T2. Further, constraining to motor network nodes, we identified significant increases in information-broadcasting (bilateral supplementary motor area (SMA) and left cerebellar lobule III) and information-receiving (right precentral gyrus) at T1. Remarkably, increased information-broadcasting in bilateral SMA was correlated with relative improvement of the CRST in the treated hand. In addition, causal TE-based effective connectivity (EC) at T1 showed an increase from right SMA to left cerebellar lobule crus II and from left cerebellar lobule III to right thalamus. In conclusion, results suggest a change in information transmission capacity in ET after MRgFUS and a shift towards a more integrated functional state with increased levels of global and directional information flow.
first_indexed 2024-03-13T03:59:06Z
format Article
id doaj.art-83fef3480b4b4f5ba1fae8f91f6593a1
institution Directory Open Access Journal
issn 1935-861X
language English
last_indexed 2024-03-13T03:59:06Z
publishDate 2023-05-01
publisher Elsevier
record_format Article
series Brain Stimulation
spelling doaj.art-83fef3480b4b4f5ba1fae8f91f6593a12023-06-22T05:02:45ZengElsevierBrain Stimulation1935-861X2023-05-01163879888Whole-brain network transitions within the framework of ignition and transfer entropy following VIM-MRgFUS in essential tremor patientsJulia M. Lueckel0Neeraj Upadhyay1Veronika Purrer2Angelika Maurer3Valeri Borger4Alexander Radbruch5Ulrike Attenberger6Ullrich Wuellner7Rajanikant Panda8Henning Boecker9Clinical Functional Imaging Group, Department of Diagnostic and Interventional Radiology, University Hospital Bonn, Bonn, GermanyClinical Functional Imaging Group, Department of Diagnostic and Interventional Radiology, University Hospital Bonn, Bonn, GermanyGerman Center for Neurodegenerative Diseases, Bonn, Germany; Department of Neurology, University Hospital Bonn, Bonn, GermanyClinical Functional Imaging Group, Department of Diagnostic and Interventional Radiology, University Hospital Bonn, Bonn, GermanyDepartment of Neurosurgery, University Hospital Bonn, Bonn, GermanyDepartment of Neuroradiology, University Hospital Bonn, Bonn, Germany; German Center for Neurodegenerative Diseases, Bonn, GermanyDepartment of Diagnostic and Interventional Radiology, University Hospital Bonn, Bonn, GermanyGerman Center for Neurodegenerative Diseases, Bonn, Germany; Department of Neurology, University Hospital Bonn, Bonn, GermanyComa Science Group, GIGA-Consciousness, University of Liège, Liège, BelgiumClinical Functional Imaging Group, Department of Diagnostic and Interventional Radiology, University Hospital Bonn, Bonn, Germany; German Center for Neurodegenerative Diseases, Bonn, Germany; Corresponding author. Clinical Functional Imaging Group, Department of Diagnostic and Interventional Radiology, University Hospital Bonn, Bonn, Germany.Magnetic resonance-guided focused ultrasound (MRgFUS) lesioning of the ventralis intermedius nucleus (VIM) has shown promise in treating drug-refractory essential tremor (ET). It remains unknown whether focal VIM lesions by MRgFUS have broader restorative effects on information flow within the whole-brain network of ET patients. We applied an information-theoretical approach based on intrinsic ignition and the concept of transfer entropy (TE) to assess the spatiotemporal dynamics after VIM-MRgFUS. Eighteen ET patients (mean age 71.44 years) underwent repeated 3T resting-state functional magnetic resonance imaging combined with Clinical Rating Scale for Tremor (CRST) assessments one day before (T0) and one month (T1) and six months (T2) post-MRgFUS, respectively. We observed increased whole brain ignition-driven mean integration (IDMI) at T1 (p < 0.05), along with trend increases at T2. Further, constraining to motor network nodes, we identified significant increases in information-broadcasting (bilateral supplementary motor area (SMA) and left cerebellar lobule III) and information-receiving (right precentral gyrus) at T1. Remarkably, increased information-broadcasting in bilateral SMA was correlated with relative improvement of the CRST in the treated hand. In addition, causal TE-based effective connectivity (EC) at T1 showed an increase from right SMA to left cerebellar lobule crus II and from left cerebellar lobule III to right thalamus. In conclusion, results suggest a change in information transmission capacity in ET after MRgFUS and a shift towards a more integrated functional state with increased levels of global and directional information flow.http://www.sciencedirect.com/science/article/pii/S1935861X23017734Essential tremorMR-Guided focused ultrasoundVentral intermediate nucleusInformation theoryIntrinsic ignition frameworkTransfer entropy
spellingShingle Julia M. Lueckel
Neeraj Upadhyay
Veronika Purrer
Angelika Maurer
Valeri Borger
Alexander Radbruch
Ulrike Attenberger
Ullrich Wuellner
Rajanikant Panda
Henning Boecker
Whole-brain network transitions within the framework of ignition and transfer entropy following VIM-MRgFUS in essential tremor patients
Brain Stimulation
Essential tremor
MR-Guided focused ultrasound
Ventral intermediate nucleus
Information theory
Intrinsic ignition framework
Transfer entropy
title Whole-brain network transitions within the framework of ignition and transfer entropy following VIM-MRgFUS in essential tremor patients
title_full Whole-brain network transitions within the framework of ignition and transfer entropy following VIM-MRgFUS in essential tremor patients
title_fullStr Whole-brain network transitions within the framework of ignition and transfer entropy following VIM-MRgFUS in essential tremor patients
title_full_unstemmed Whole-brain network transitions within the framework of ignition and transfer entropy following VIM-MRgFUS in essential tremor patients
title_short Whole-brain network transitions within the framework of ignition and transfer entropy following VIM-MRgFUS in essential tremor patients
title_sort whole brain network transitions within the framework of ignition and transfer entropy following vim mrgfus in essential tremor patients
topic Essential tremor
MR-Guided focused ultrasound
Ventral intermediate nucleus
Information theory
Intrinsic ignition framework
Transfer entropy
url http://www.sciencedirect.com/science/article/pii/S1935861X23017734
work_keys_str_mv AT juliamlueckel wholebrainnetworktransitionswithintheframeworkofignitionandtransferentropyfollowingvimmrgfusinessentialtremorpatients
AT neerajupadhyay wholebrainnetworktransitionswithintheframeworkofignitionandtransferentropyfollowingvimmrgfusinessentialtremorpatients
AT veronikapurrer wholebrainnetworktransitionswithintheframeworkofignitionandtransferentropyfollowingvimmrgfusinessentialtremorpatients
AT angelikamaurer wholebrainnetworktransitionswithintheframeworkofignitionandtransferentropyfollowingvimmrgfusinessentialtremorpatients
AT valeriborger wholebrainnetworktransitionswithintheframeworkofignitionandtransferentropyfollowingvimmrgfusinessentialtremorpatients
AT alexanderradbruch wholebrainnetworktransitionswithintheframeworkofignitionandtransferentropyfollowingvimmrgfusinessentialtremorpatients
AT ulrikeattenberger wholebrainnetworktransitionswithintheframeworkofignitionandtransferentropyfollowingvimmrgfusinessentialtremorpatients
AT ullrichwuellner wholebrainnetworktransitionswithintheframeworkofignitionandtransferentropyfollowingvimmrgfusinessentialtremorpatients
AT rajanikantpanda wholebrainnetworktransitionswithintheframeworkofignitionandtransferentropyfollowingvimmrgfusinessentialtremorpatients
AT henningboecker wholebrainnetworktransitionswithintheframeworkofignitionandtransferentropyfollowingvimmrgfusinessentialtremorpatients