Abstract
Original language | English |
---|---|
Pages (from-to) | 961-972 |
Number of pages | 12 |
Journal | Biological Psychiatry: Cognitive Neuroscience and Neuroimaging |
Volume | 6 |
Issue number | 10 |
DOIs | |
Publication status | Published - 1 Oct 2021 |
Keywords
- DOUBLE-BLIND
- FUNCTIONAL-ANATOMY
- GILLES
- HIGH-FREQUENCY STIMULATION
- HUMAN SUBTHALAMIC NUCLEUS
- INTERNUS
- OBSESSIVE-COMPULSIVE DISORDER
- REPETITIVE BEHAVIORS
- TIC SUPPRESSION
- TRANSCRANIAL MAGNETIC STIMULATION
Access to Document
Cite this
- APA
- Author
- BIBTEX
- Harvard
- Standard
- RIS
- Vancouver
}
In: Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, Vol. 6, No. 10, 01.10.2021, p. 961-972.
Research output: Contribution to journal › Article › Academic › peer-review
TY - JOUR
T1 - Basal Ganglia Pathways Associated With Therapeutic Pallidal Deep Brain Stimulation for Tourette Syndrome
AU - Johnson, K.A.
AU - Duff, G.
AU - Foltynie, T.
AU - Hariz, M.
AU - Zrinzo, L.
AU - Joyce, E.M.
AU - Akram, H.
AU - Servello, D.
AU - Galbiati, T.F.
AU - Bona, A.
AU - Porta, M.
AU - Meng, F.G.
AU - Leentjens, A.F.G.
AU - Gunduz, A.
AU - Hu, W.
AU - Foote, K.D.
AU - Okun, M.S.
AU - Butson, C.R.
N1 - Funding Information: KAJ, GD, MH, EMJ, HA, DS, TFG, AB, MP, F-GM, AG, and WH report no biomedical financial interests or potential conflicts of interest. TF has received honoraria for speaking at meetings sponsored by Bill, Profile Pharma, and Boston Scientific; and received grant support from the National Institute of Health Research, Cure Parkinson’s Trust, Michael J. Fox Foundation, Innovate UK, John Black Charitable Foundation, Van Andel Research Institute, and Defeat MSA. LZ acts as a consultant for Medtronic, Boston Scientific, and Elekta. AFGL has received a research grant from the Michael J. Fox Foundation and royalties from Springer media. KDF has received occasional consulting fees from Medtronic and Boston Scientific for deep brain stimulation (DBS)–related work. His research is funded by the National Institutes of Health and multiple foundation sources. Implantable devices for KDF's DBS-related research have been provided by Medtronic and NeuroPace. KDF has participated as a site implanting surgeon in multicenter DBS-related research studies sponsored by Abbott/St. Jude, Boston Scientific, and Functional Neuromodulation. The University of Florida receives partial funding for KDF's functional neurosurgery fellowship from Medtronic. KDF holds 3 DBS-related patents for which he has received no royalties. KDF is an associate editor for the Journal of Parkinson’s Disease. MSO has served as a consultant for the National Parkinson Foundation and has received research grants from National Institutes of Health, National Parkinson Foundation, the Michael J. Fox Foundation, the Parkinson Alliance, Smallwood Foundation, the Bachmann-Strauss Foundation, the Tourette Syndrome Association, and the University of Florida Foundation. MSO has previously received honoraria, but in the past >60 months has received no support from industry. MSO has received royalties for publications with Demos, Manson, Amazon, Smashwords, Books4Patients, and Cambridge (movement disorders books). MSO is an associate editor for New England Journal of Medicine Journal Watch Neurology. MSO has participated in continuing medical education and educational activities on movement disorders (in the last 36 months) sponsored by PeerView, Prime, QuantiaMD, WebMD, Medicus, MedNet, Henry Stewart, and Vanderbilt University. The institution and not MSO receives grants from Medtronic, AbbVie, Allergan, and Advanced Neuromodulation Systems/St. Jude, and the principal investigator has no financial interest in these grants. MSO has participated as a site principal investigator and/or co-investigator for several NIH-, foundation-, and industry-sponsored trials over the years but has not received honoraria. CRB has served as a consultant for NeuroPace, Advanced Bionics, Boston Scientific, Intelect Medical, St. Jude Medical, and Functional Neuromodulation; and he holds intellectual property related to DBS. Funding Information: This work was supported by National Science Foundation Graduate Research Fellowship Program Grant No. 1747505 (to KAJ), National Institutes of Health (NIH) P41 Center for Integrative Biomedical Computing Grant No. GM103545 (to KAJ and CRB), NIH National Institute of Nursing Research Grant No. NR014852 (GD, CRB, and MSO), the National Institute for Health Research University College London Hospitals Biomedical Research Centre (to LZ, EMJ, and TF), an International TS Registry Grant from the Tourette Association of America (principal investigator: MSO), and NIH Grant No. R01NS096008 (to MSO). Funding Information: This work was supported by National Science Foundation Graduate Research Fellowship Program Grant No. 1747505 (to KAJ), National Institutes of Health (NIH) P41 Center for Integrative Biomedical Computing Grant No. GM103545 (to KAJ and CRB), NIH National Institute of Nursing Research Grant No. NR014852 (GD, CRB, and MSO), the National Institute for Health Research University College London Hospitals Biomedical Research Centre (to LZ, EMJ, and TF), an International TS Registry Grant from the Tourette Association of America (principal investigator: MSO), and NIH Grant No. R01NS096008 (to MSO). This study was conducted in collaboration with the Tourette Syndrome Deep Brain Stimulation Working Group; for an updated list of contributing members, please visit the International Tourette Deep Brain Stimulation Database and Registry website (https://tourettedeepbrainstimulationregistry.ese.ufhealth.org/). KAJ, GD, MH, EMJ, HA, DS, TFG, AB, MP, F-GM, AG, and WH report no biomedical financial interests or potential conflicts of interest. TF has received honoraria for speaking at meetings sponsored by Bill, Profile Pharma, and Boston Scientific; and received grant support from the National Institute of Health Research, Cure Parkinson's Trust, Michael J. Fox Foundation, Innovate UK, John Black Charitable Foundation, Van Andel Research Institute, and Defeat MSA. LZ acts as a consultant for Medtronic, Boston Scientific, and Elekta. AFGL has received a research grant from the Michael J. Fox Foundation and royalties from Springer media. KDF has received occasional consulting fees from Medtronic and Boston Scientific for deep brain stimulation (DBS)–related work. His research is funded by the National Institutes of Health and multiple foundation sources. Implantable devices for KDF's DBS-related research have been provided by Medtronic and NeuroPace. KDF has participated as a site implanting surgeon in multicenter DBS-related research studies sponsored by Abbott/St. Jude, Boston Scientific, and Functional Neuromodulation. The University of Florida receives partial funding for KDF's functional neurosurgery fellowship from Medtronic. KDF holds 3 DBS-related patents for which he has received no royalties. KDF is an associate editor for the Journal of Parkinson's Disease. MSO has served as a consultant for the National Parkinson Foundation and has received research grants from National Institutes of Health, National Parkinson Foundation, the Michael J. Fox Foundation, the Parkinson Alliance, Smallwood Foundation, the Bachmann-Strauss Foundation, the Tourette Syndrome Association, and the University of Florida Foundation. MSO has previously received honoraria, but in the past >60 months has received no support from industry. MSO has received royalties for publications with Demos, Manson, Amazon, Smashwords, Books4Patients, and Cambridge (movement disorders books). MSO is an associate editor for New England Journal of Medicine Journal Watch Neurology. MSO has participated in continuing medical education and educational activities on movement disorders (in the last 36 months) sponsored by PeerView, Prime, QuantiaMD, WebMD, Medicus, MedNet, Henry Stewart, and Vanderbilt University. The institution and not MSO receives grants from Medtronic, AbbVie, Allergan, and Advanced Neuromodulation Systems/St. Jude, and the principal investigator has no financial interest in these grants. MSO has participated as a site principal investigator and/or co-investigator for several NIH-, foundation-, and industry-sponsored trials over the years but has not received honoraria. CRB has served as a consultant for NeuroPace, Advanced Bionics, Boston Scientific, Intelect Medical, St. Jude Medical, and Functional Neuromodulation; and he holds intellectual property related to DBS. Publisher Copyright: © 2020 Society of Biological Psychiatry
PY - 2021/10/1
Y1 - 2021/10/1
N2 - BACKGROUND: Deep brain stimulation (DBS) targeting the globus pallidus internus (GPi) can improve tics and comorbid obsessive-compulsive behavior (OCB) in patients with treatment-refractory Tourette syndrome (TS). However, some patients' symptoms remain unresponsive, the stimulation applied across patients is variable, and the mechanisms underlying improvement are unclear. Identifying the fiber pathways surrounding the GPi that are associated with improvement could provide mechanistic insight and refine targeting strategies to improve outcomes. METHODS: Retrospective data were collected for 35 patients who underwent bilateral GPi DBS for TS. Computational models of fiber tract activation were constructed using patient-specific lead locations and stimulation settings to evaluate the effects of DBS on basal ganglia pathways and the internal capsule. We first evaluated the relationship between activation of individual pathways and symptom improvement. Next, linear mixed-effects models with combinations of pathways and clinical variables were compared in order to identify the best-fit predictive models of tic and OCB improvement. RESULTS: The best-fit model of tic improvement included baseline severity and the associative pallido-subthalamic pathway. The best-fit model of OCB improvement included baseline severity and the sensorimotor pallidosubthalamic pathway, with substantial evidence also supporting the involvement of the prefrontal, motor, and premotor internal capsule pathways. The best-fit models of tic and OCB improvement predicted outcomes across the cohort and in cross-validation. CONCLUSIONS: Differences in fiber pathway activation likely contribute to variable outcomes of DBS for TS. Computational models of pathway activation could be used to develop novel approaches for preoperative targeting and selecting stimulation parameters to improve patient outcomes.
AB - BACKGROUND: Deep brain stimulation (DBS) targeting the globus pallidus internus (GPi) can improve tics and comorbid obsessive-compulsive behavior (OCB) in patients with treatment-refractory Tourette syndrome (TS). However, some patients' symptoms remain unresponsive, the stimulation applied across patients is variable, and the mechanisms underlying improvement are unclear. Identifying the fiber pathways surrounding the GPi that are associated with improvement could provide mechanistic insight and refine targeting strategies to improve outcomes. METHODS: Retrospective data were collected for 35 patients who underwent bilateral GPi DBS for TS. Computational models of fiber tract activation were constructed using patient-specific lead locations and stimulation settings to evaluate the effects of DBS on basal ganglia pathways and the internal capsule. We first evaluated the relationship between activation of individual pathways and symptom improvement. Next, linear mixed-effects models with combinations of pathways and clinical variables were compared in order to identify the best-fit predictive models of tic and OCB improvement. RESULTS: The best-fit model of tic improvement included baseline severity and the associative pallido-subthalamic pathway. The best-fit model of OCB improvement included baseline severity and the sensorimotor pallidosubthalamic pathway, with substantial evidence also supporting the involvement of the prefrontal, motor, and premotor internal capsule pathways. The best-fit models of tic and OCB improvement predicted outcomes across the cohort and in cross-validation. CONCLUSIONS: Differences in fiber pathway activation likely contribute to variable outcomes of DBS for TS. Computational models of pathway activation could be used to develop novel approaches for preoperative targeting and selecting stimulation parameters to improve patient outcomes.
KW - DOUBLE-BLIND
KW - FUNCTIONAL-ANATOMY
KW - GILLES
KW - HIGH-FREQUENCY STIMULATION
KW - HUMAN SUBTHALAMIC NUCLEUS
KW - INTERNUS
KW - OBSESSIVE-COMPULSIVE DISORDER
KW - REPETITIVE BEHAVIORS
KW - TIC SUPPRESSION
KW - TRANSCRANIAL MAGNETIC STIMULATION
U2 - 10.1016/j.bpsc.2020.11.005
DO - 10.1016/j.bpsc.2020.11.005
M3 - Article
C2 - 33536144
SN - 2451-9022
VL - 6
SP - 961
EP - 972
JO - Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
JF - Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
IS - 10
ER -