Responsive deep brain stimulation for the treatment of Tourette syndrome.
Closed loop
DBS
Neuromodulation
Programming
Selection
Tic
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
18 Mar 2024
18 Mar 2024
Historique:
received:
06
12
2023
accepted:
14
03
2024
medline:
19
3
2024
pubmed:
19
3
2024
entrez:
19
3
2024
Statut:
epublish
Résumé
To report the results of 'responsive' deep brain stimulation (DBS) for Tourette syndrome (TS) in a National Institutes of Health funded experimental cohort. The use of 'brain derived physiology' as a method to trigger DBS devices to deliver trains of electrical stimulation is a proposed approach to address the paroxysmal motor and vocal tic symptoms which appear as part of TS. Ten subjects underwent bilateral staged DBS surgery and each was implanted with bilateral centromedian thalamic (CM) region DBS leads and bilateral M1 region cortical strips. A series of identical experiments and data collections were conducted on three groups of consecutively recruited subjects. Group 1 (n = 2) underwent acute responsive DBS using deep and superficial leads. Group 2 (n = 4) underwent chronic responsive DBS using deep and superficial leads. Group 3 (n = 4) underwent responsive DBS using only the deep leads. The primary outcome measure for each of the 8 subjects with chronic responsive DBS was calculated as the pre-operative baseline Yale Global Tic Severity Scale (YGTSS) motor subscore compared to the 6 month embedded responsive DBS setting. A responder for the study was defined as any subject manifesting a ≥ 30 points improvement on the YGTSS motor subscale. The videotaped Modified Rush Tic Rating Scale (MRVTRS) was a secondary outcome. Outcomes were collected at 6 months across three different device states: no stimulation, conventional open-loop stimulation, and embedded responsive stimulation. The experience programming each of the groups and the methods applied for programming were captured. There were 10 medication refractory TS subjects enrolled in the study (5 male and 5 female) and 4/8 (50%) in the chronic responsive eligible cohort met the primary outcome manifesting a reduction of the YGTSS motor scale of ≥ 30% when on responsive DBS settings. Proof of concept for the use of responsive stimulation was observed in all three groups (acute responsive, cortically triggered and deep DBS leads only). The responsive approach was safe and well tolerated. TS power spectral changes associated with tics occurred consistently in the low frequency 2-10 Hz delta-theta-low alpha oscillation range. The study highlighted the variety of programming strategies which were employed to achieve responsive DBS and those used to overcome stimulation induced artifacts. Proof of concept was also established for a single DBS lead triggering bi-hemispheric delivery of therapeutic stimulation. Responsive DBS was applied to treat TS related motor and vocal tics through the application of three different experimental paradigms. The approach was safe and effective in a subset of individuals. The use of different devices in this study was not aimed at making between device comparisons, but rather, the study was adapted to the current state of the art in technology. Overall, four of the chronic responsive eligible subjects met the primary outcome variable for clinical effectiveness. Cortical physiology was used to trigger responsive DBS when therapy was limited by stimulation induced artifacts.
Identifiants
pubmed: 38499664
doi: 10.1038/s41598-024-57071-5
pii: 10.1038/s41598-024-57071-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6467Subventions
Organisme : NIH HHS
ID : NIH R01 NR014852
Pays : United States
Organisme : NIH HHS
ID : R01 NS096008
Pays : United States
Informations de copyright
© 2024. The Author(s).
Références
De Salles, A. et al. Modern neurosurgical techniques for psychiatric disorders. Prog. Brain Res. 270(1), 33–59 (2022).
doi: 10.1016/bs.pbr.2022.01.025
pubmed: 35396030
Messina, G., Vetrano, I. G., Bonomo, G. & Broggi, G. Role of deep brain stimulation in management of psychiatric disorders. Prog. Brain Res. 270(1), 61–96 (2022).
doi: 10.1016/bs.pbr.2022.01.026
pubmed: 35396031
Hitti, F. L. et al. Future directions in psychiatric neurosurgery: Proceedings of the 2022 American Society for Stereotactic and Functional Neurosurgery meeting on surgical neuromodulation for psychiatric disorder. Brain Stimul. 16(3), 867–878 (2023).
doi: 10.1016/j.brs.2023.05.011
pubmed: 37217075
Cif, L. & Hariz, M. Seventy years with the globus pallidus: Pallidal surgery for movement disorders between 1947 and 2017. Mov. Disord. 32(7), 972–982 (2017).
doi: 10.1002/mds.27054
pubmed: 28590521
Johnson, K. A. et al. Tourette syndrome: Clinical features, pathophysiology, and treatment. Lancet Neurol. 22(2), 147–158 (2023).
doi: 10.1016/S1474-4422(22)00303-9
pubmed: 36354027
Almeida, L. et al. Chasing tics in the human brain: Development of open, scheduled and closed loop responsive approaches to deep brain stimulation for tourette syndrome. J. Clin. Neurol. 11(2), 122–131 (2015).
doi: 10.3988/jcn.2015.11.2.122
pubmed: 25851890
pmcid: 4387477
Mitchell, K. T. & Starr, P. A. Smart neuromodulation in movement disorders. Handb. Clin. Neurol. 168, 153–161 (2020).
doi: 10.1016/B978-0-444-63934-9.00012-3
pubmed: 32164850
Priori, A. et al. Adaptive deep brain stimulation (aDBS). Int. Rev. Neurobiol. 159, 111–127 (2021).
doi: 10.1016/bs.irn.2021.06.006
pubmed: 34446243
Cagle, J. N. et al. Lead repositioning guided by both physiology and atlas based targeting in Tourette deep brain stimulation. Tremor Other Hyperkinet. Mov. (N. Y.) 10, 18 (2020).
doi: 10.5334/tohm.140
pubmed: 32775032
Cagle, J. N. et al. A novel local field potential-based functional approach for targeting the centromedian-parafascicular complex for deep brain stimulation. Neuroimage Clin. 30, 102644 (2021).
doi: 10.1016/j.nicl.2021.102644
pubmed: 33845353
pmcid: 8064020
Cagle, J. N. et al. Embedded human closed-loop deep brain stimulation for Tourette syndrome: A nonrandomized controlled trial. JAMA Neurol. 79(10), 1064–1068 (2022).
doi: 10.1001/jamaneurol.2022.2741
pubmed: 36094652
pmcid: 9468946
Gunduz, A. & Okun, M. S. A review and update on Tourette syndrome: Where is the field headed?. Curr. Neurol. Neurosci. Rep. 16(4), 37 (2016).
doi: 10.1007/s11910-016-0633-x
pubmed: 26936259
Molina, R. et al. Report of a patient undergoing chronic responsive deep brain stimulation for Tourette syndrome: Proof of concept. J. Neurosurg. 129(2), 308–314 (2018).
doi: 10.3171/2017.6.JNS17626
pubmed: 28960154
Shute, J. B. et al. Thalamocortical network activity enables chronic tic detection in humans with Tourette syndrome. Neuroimage Clin. 12, 165–172 (2016).
doi: 10.1016/j.nicl.2016.06.015
pubmed: 27419067
pmcid: 4936504
Afshar, P. et al. A translational platform for prototyping closed-loop neuromodulation systems. Front. Neural Circ. 6, 117 (2012).
Stanslaski, S. et al. A chronically implantable neural coprocessor for investigating the treatment of neurological disorders. IEEE Trans. Biomed. Circ. Syst. 12(6), 1230–1245 (2018).
doi: 10.1109/TBCAS.2018.2880148
Gunduz, A., Cagle, J. N. Okun, M. S. & Foote, K. D. Simultaneous bilateral stimulation using neurostimulator World Patent. Publication number: 20230166112 (2021).
Rossi, P. J. et al. Scheduled, intermittent stimulation of the thalamus reduces tics in Tourette syndrome. Parkinson. Relat. Disord. 29, 35–41 (2016).
doi: 10.1016/j.parkreldis.2016.05.033
Cagle, J. N. et al. Differentiating tic electrophysiology from voluntary movement in the human thalamocortical circuit. J. Neurol. Neurosurg. Psychiatry 91(5), 533–539 (2020).
doi: 10.1136/jnnp-2019-321973
pubmed: 32139653