A novel local field potential-based functional approach for targeting the centromedian-parafascicular complex for deep brain stimulation

Background: The centromedian-parafascicular (Cm-Pf) complex of the thalamus is a common deep brain stimulation (DBS) target for treatment of Tourette syndrome (TS). Currently, there are no standardized functional intraoperative neurosurgical targeting approaches. Collectively, these issues have led...

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Main Authors: Jackson N. Cagle, Robert S. Eisinger, Marshall T. Holland, Kelly D. Foote, Michael S. Okun, Aysegul Gunduz
Format: Article
Language:English
Published: Elsevier 2021-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158221000887
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author Jackson N. Cagle
Robert S. Eisinger
Marshall T. Holland
Kelly D. Foote
Michael S. Okun
Aysegul Gunduz
author_facet Jackson N. Cagle
Robert S. Eisinger
Marshall T. Holland
Kelly D. Foote
Michael S. Okun
Aysegul Gunduz
author_sort Jackson N. Cagle
collection DOAJ
description Background: The centromedian-parafascicular (Cm-Pf) complex of the thalamus is a common deep brain stimulation (DBS) target for treatment of Tourette syndrome (TS). Currently, there are no standardized functional intraoperative neurosurgical targeting approaches. Collectively, these issues have led to variability in DBS lead placement. Therefore, more defined methods are needed to improve targeting accuracy. Objective: The objective of this observational study was to develop and to verify a functional mapping task capable of differentiating the Cm-Pf region from the nearby ventral intermediate (Vim) nucleus region of the thalamus. The overarching goal was to improve the reproducibility of DBS targeting in the Cm-Pf region. Methods: Seven TS patients completed a modified Go/NoGo task (five in the post-operative setting and two in the intra-operative setting). Post-operative neural signals from Cm-Pf region were collected using sensing-enabled implanted neural stimulators, and intraoperative neural signals from the Cm-Pf region were collected using an external amplifier. Event-related potential (ERP) features were identified by using the grand-average of stimulus onset signals derived from the postoperative participants. These features were correlated with anatomical locations for the specific electrode recordings. The same features were extracted from the intraoperative patients in order to verify electrode positions in the operating room environment. Results: Two features – a positive and a negative deflection – were identified in the average ERP from the post-operative participants. The peak amplitudes of both features were significantly correlated with the electrode depth position (p = 0.025 for positive deflection and p = 0.039 for negative deflection). The same result was reproduced intra-operatively in the two most recent patients, where more ventral electrode contacts revealed stronger peak amplitudes in comparison to the dorsal electrode contacts. Conclusion: This process was used to physiologically confirm accurate lead placement in the operating room setting. The modified Go/NoGo task elicited robust neural responses in the Cm-Pf region however the signal was not present in the Vim nucleus region of thalamus along the DBS electrode trajectory. We conclude that the differences in ERP responses may be a potentially novel LFP based functional approach for future targeting of the Cm-Pf complex for TS DBS.
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spelling doaj.art-32bbc48ceee44f549c68605326f9b8cf2022-12-21T18:44:02ZengElsevierNeuroImage: Clinical2213-15822021-01-0130102644A novel local field potential-based functional approach for targeting the centromedian-parafascicular complex for deep brain stimulationJackson N. Cagle0Robert S. Eisinger1Marshall T. Holland2Kelly D. Foote3Michael S. Okun4Aysegul Gunduz5J. Crayton Pruitt Department of Biomedical Engineering, University of Florida, Gainesville FL, United StatesDepartment of Neuroscience, University of Florida, Gainesville, FL, United StatesDepartment of Neurosurgery, University of Florida Norman Fixel Institute for Neurological Diseases, Gainesville, FL, United States; Department of Neurosurgery, University of Iowa, Iowa City, IA, United StatesDepartment of Neurosurgery, University of Florida Norman Fixel Institute for Neurological Diseases, Gainesville, FL, United StatesDepartment of Neuroscience, University of Florida, Gainesville, FL, United States; Department of Neurology, University of Florida Norman Fixel Institute for Neurological Diseases, Gainesville, FL, United StatesJ. Crayton Pruitt Department of Biomedical Engineering, University of Florida, Gainesville FL, United States; Corresponding authors at: University of Florida, PO Box 116131, Gainesville, FL 32611, United States.Background: The centromedian-parafascicular (Cm-Pf) complex of the thalamus is a common deep brain stimulation (DBS) target for treatment of Tourette syndrome (TS). Currently, there are no standardized functional intraoperative neurosurgical targeting approaches. Collectively, these issues have led to variability in DBS lead placement. Therefore, more defined methods are needed to improve targeting accuracy. Objective: The objective of this observational study was to develop and to verify a functional mapping task capable of differentiating the Cm-Pf region from the nearby ventral intermediate (Vim) nucleus region of the thalamus. The overarching goal was to improve the reproducibility of DBS targeting in the Cm-Pf region. Methods: Seven TS patients completed a modified Go/NoGo task (five in the post-operative setting and two in the intra-operative setting). Post-operative neural signals from Cm-Pf region were collected using sensing-enabled implanted neural stimulators, and intraoperative neural signals from the Cm-Pf region were collected using an external amplifier. Event-related potential (ERP) features were identified by using the grand-average of stimulus onset signals derived from the postoperative participants. These features were correlated with anatomical locations for the specific electrode recordings. The same features were extracted from the intraoperative patients in order to verify electrode positions in the operating room environment. Results: Two features – a positive and a negative deflection – were identified in the average ERP from the post-operative participants. The peak amplitudes of both features were significantly correlated with the electrode depth position (p = 0.025 for positive deflection and p = 0.039 for negative deflection). The same result was reproduced intra-operatively in the two most recent patients, where more ventral electrode contacts revealed stronger peak amplitudes in comparison to the dorsal electrode contacts. Conclusion: This process was used to physiologically confirm accurate lead placement in the operating room setting. The modified Go/NoGo task elicited robust neural responses in the Cm-Pf region however the signal was not present in the Vim nucleus region of thalamus along the DBS electrode trajectory. We conclude that the differences in ERP responses may be a potentially novel LFP based functional approach for future targeting of the Cm-Pf complex for TS DBS.http://www.sciencedirect.com/science/article/pii/S2213158221000887Centromedian nucleusDeep brain stimulationTourette syndromeStereotactic targetingLocal field potentialEvent-related potential
spellingShingle Jackson N. Cagle
Robert S. Eisinger
Marshall T. Holland
Kelly D. Foote
Michael S. Okun
Aysegul Gunduz
A novel local field potential-based functional approach for targeting the centromedian-parafascicular complex for deep brain stimulation
NeuroImage: Clinical
Centromedian nucleus
Deep brain stimulation
Tourette syndrome
Stereotactic targeting
Local field potential
Event-related potential
title A novel local field potential-based functional approach for targeting the centromedian-parafascicular complex for deep brain stimulation
title_full A novel local field potential-based functional approach for targeting the centromedian-parafascicular complex for deep brain stimulation
title_fullStr A novel local field potential-based functional approach for targeting the centromedian-parafascicular complex for deep brain stimulation
title_full_unstemmed A novel local field potential-based functional approach for targeting the centromedian-parafascicular complex for deep brain stimulation
title_short A novel local field potential-based functional approach for targeting the centromedian-parafascicular complex for deep brain stimulation
title_sort novel local field potential based functional approach for targeting the centromedian parafascicular complex for deep brain stimulation
topic Centromedian nucleus
Deep brain stimulation
Tourette syndrome
Stereotactic targeting
Local field potential
Event-related potential
url http://www.sciencedirect.com/science/article/pii/S2213158221000887
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