Image-based analysis and long-term clinical outcomes of deep brain stimulation for Tourette syndrome: a multisite study

Kara A Johnson, P Thomas Fletcher, Domenico Servello, Alberto Bona, Mauro Porta, Jill L Ostrem, Eric Bardinet, Marie-Laure Welter, Andres M Lozano, Juan Carlos Baldermann, Jens Kuhn, Daniel Huys, Thomas Foltynie, Marwan Hariz, Eileen M Joyce, Ludvic Zrinzo, Zinovia Kefalopoulou, Jian-Guo Zhang, Fan-Gang Meng, ChenCheng Zhang, Zhipei Ling, Xin Xu, Xinguang Yu, Anouk Yjm Smeets, Linda Ackermans, Veerle Visser-Vandewalle, Alon Y Mogilner, Michael H Pourfar, Leonardo Almeida, Aysegul Gunduz, Wei Hu, Kelly D Foote, Michael S Okun, Christopher R Butson, Kara A Johnson, P Thomas Fletcher, Domenico Servello, Alberto Bona, Mauro Porta, Jill L Ostrem, Eric Bardinet, Marie-Laure Welter, Andres M Lozano, Juan Carlos Baldermann, Jens Kuhn, Daniel Huys, Thomas Foltynie, Marwan Hariz, Eileen M Joyce, Ludvic Zrinzo, Zinovia Kefalopoulou, Jian-Guo Zhang, Fan-Gang Meng, ChenCheng Zhang, Zhipei Ling, Xin Xu, Xinguang Yu, Anouk Yjm Smeets, Linda Ackermans, Veerle Visser-Vandewalle, Alon Y Mogilner, Michael H Pourfar, Leonardo Almeida, Aysegul Gunduz, Wei Hu, Kelly D Foote, Michael S Okun, Christopher R Butson

Abstract

Background: Deep brain stimulation (DBS) can be an effective therapy for tics and comorbidities in select cases of severe, treatment-refractory Tourette syndrome (TS). Clinical responses remain variable across patients, which may be attributed to differences in the location of the neuroanatomical regions being stimulated. We evaluated active contact locations and regions of stimulation across a large cohort of patients with TS in an effort to guide future targeting.

Methods: We collected retrospective clinical data and imaging from 13 international sites on 123 patients. We assessed the effects of DBS over time in 110 patients who were implanted in the centromedial (CM) thalamus (n=51), globus pallidus internus (GPi) (n=47), nucleus accumbens/anterior limb of the internal capsule (n=4) or a combination of targets (n=8). Contact locations (n=70 patients) and volumes of tissue activated (n=63 patients) were coregistered to create probabilistic stimulation atlases.

Results: Tics and obsessive-compulsive behaviour (OCB) significantly improved over time (p<0.01), and there were no significant differences across brain targets (p>0.05). The median time was 13 months to reach a 40% improvement in tics, and there were no significant differences across targets (p=0.84), presence of OCB (p=0.09) or age at implantation (p=0.08). Active contacts were generally clustered near the target nuclei, with some variability that may reflect differences in targeting protocols, lead models and contact configurations. There were regions within and surrounding GPi and CM thalamus that improved tics for some patients but were ineffective for others. Regions within, superior or medial to GPi were associated with a greater improvement in OCB than regions inferior to GPi.

Conclusion: The results collectively indicate that DBS may improve tics and OCB, the effects may develop over several months, and stimulation locations relative to structural anatomy alone may not predict response. This study was the first to visualise and evaluate the regions of stimulation across a large cohort of patients with TS to generate new hypotheses about potential targets for improving tics and comorbidities.

Keywords: globus pallidus; neuromodulation; obsessive-compulsive behavior; thalamus; tics.

Conflict of interest statement

Competing interests: JLO has received research grant support from the Michael J Fox Foundation, Boston Scientific, Cala Health, NIH, DARPA, PCORI and Biogen, and she has also received training grant support from Boston Scientific and Medtronic, and has served as a consultant for Acadia Pharmaceuticals and Medtronic. AL serves as a consultant for Boston Scientific and holds intellectual property in the field of DBS. JK has received financial support for investigator-initiated trials from Medtronic and grants from the German Research Foundation (KU2665/1-2) and the Marga and Walter Boll Foundation. CZ has received honoraria and travel expenses from the deep brain stimulation industry (Medtronic, PINS, SceneRay). MSO serves as a consultant for the National Parkinson Foundation, and has received research grants from NIH, NPF, the Michael J Fox Foundation, the Parkinson Alliance, Smallwood Foundation, the Bachmann-Strauss Foundation, the Tourette Syndrome Association, and the UF Foundation. MSO DBS research is supported by R01 NR014852 and R01NS096008. MSO has previously received honoraria, but in the past >60 months has received no support from the 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 CME and educational activities on movement disorders (in the last 36 months) sponsored by PeerView, Prime, QuantiaMD, WebMD, Medicus, MedNet, Henry Stewart and by Vanderbilt University. The institution and not MSO receives grants from Medtronic, AbbVie, Allergan and ANS/St Jude, and the PI has no financial interest in these grants. MSO has participated as a site PI and/or co-I 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.

© Author(s) (or their employer(s)) 2019. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ.

Figures

Figure 1
Figure 1
Tic severity and obsessive–compulsive behaviour over time. (A) YGTSS total scores over time grouped by DBS target. (B–D) YGTSS subscores (motor, phonic and impairment) over time grouped by DBS target. (E) Y-BOCS total scores over time grouped by DBS target. YGTSS subscores and Y-BOCS scores were collected for only a subset of the targets. The number of patients in each group is annotated above each boxplot and is coloured according to the legend. ALIC, anterior limb of the internal capsule; amGPi, anteromedial globus pallidus internus; DBS, deep brain stimulation; CM, centromedial; NA, nucleus accumbens; pvGPi, posteroventral globus pallidus internus; Y-BOCS, Yale-Brown Obsessive Compulsive Scale; YGTSS, Yale Global Tic Severity Scale.
Figure 2
Figure 2
Median time to response across the TS DBS cohort and subgroups. (A) Cumulative probability of response for all patients in the cohort (N=110). (B) Cumulative probability of response for patients implanted in the GPi and CM thalamus. (C) Cumulative probability of response in patients with TS and OCB and patients with TS only. (D) Cumulative probability of response in patients grouped by age at DBS implantation. The shaded regions are 95% CIs. The numbers of patients and the median times to response (in months) are listed in the legends. CM, centromedial; DBS, deep brain stimulation; GPi, globus pallidus internus; OCB, obsessive–compulsive behaviour; TS, Tourette syndrome; YGTSS, Yale Global Tic Severity Scale.
Figure 3
Figure 3
Variability of bilateral active DBS contact locations in the cohort atlas space. (A) Three-dimensional superior view of the locations of the active contacts in the cohort atlas space for n=70 patients relative to nuclei segmentations. Each sphere represents an active DBS contact and is coloured by intended DBS target region as listed in the legend in (B). (B) Sagittal (x), coronal (y) and axial (z) coordinates in mean (SD) mm relative to the mid-commissural point of the cohort atlas. DBS, deep brain stimulation.
Figure 4
Figure 4
PSAs of clinical outcomes in GPi DBS patients. (A) PSA of the proportion of the total number of patients stimulated at each voxel. The region with the greatest number of overlapping VTA across GPi DBS patients was located within the amGPi and the regions inferior of the amGPi. (B) PSA of the mean per cent improvement in YGTSS total score. (C) Regions stimulated in nonresponders, responders and the regions where they overlapped. There was substantial overlap of effective regions and regions that were associated with little to no therapeutic benefit. (D) PSA of the mean per cent improvement in the Y-BOCS total score showed that the VTA of patients who did not reach a 25% improvement extended below the GPi. The VTA of patients who reached a >25% improvement were located within the pallidum and/or medial or superior to the pallidum and did not extend below the GPi. Segmentation outlines of nuclei are overlaid for reference (GPi, yellow; GPe, white). For axial and sagittal views, see online supplementary figures 1-4. amGPi, anteromedial globus pallidus internus; DBS, deep brain stimulation; GPe, globus pallidus externus; GPi, globus pallidus internus; PSA, probabilistic stimulation atlas.
Figure 5
Figure 5
PSAs of clinical outcomes in CM thalamus DBS patients. (A) PSA of the proportion of the total number of patients stimulated at each voxel. The region with the greatest number of overlapping VTA across the CM thalamus DBS patients was located at the intersection of the CMn-Pf complex-Voi. (B) PSA of the mean per cent improvement in YGTSS total score. (C) Regions stimulated in nonresponders, responders and the regions where they overlapped. There were regions associated with improvement and overlapping regions associated with little to no therapeutic benefit. (D) PSA of the mean per cent improvement in the Y-BOCS total score. Segmentation outlines of the nuclei are overlaid for reference (thalamus, white; CM nucleus, light blue; PF complex, dark green; Voi, yellow-green). For axial and sagittal views, see online supplementary figures 6-9. CM, centromedial; CMn-Pf, centromedian nucleus-parafascicular; DBS, deep brain stimulation; PSAs, probabilistic stimulation atlases; Voi, ventro-oralis internus.

References

    1. Robertson MM. Tourette syndrome, associated conditions and the complexities of treatment. Brain 2000;123:425–62. 10.1093/brain/123.3.425
    1. Freeman RD, Fast DK, Burd L, et al. . An international perspective on Tourette syndrome: selected findings from 3500 individuals in 22 countries. Dev Med Child Neurol 2000;42:436–47. 10.1017/S0012162200000839
    1. Leckman JF. Tourette's syndrome. Lancet 2002;360:1577–86. 10.1016/S0140-6736(02)11526-1
    1. Hirschtritt ME, Lee PC, Pauls DL, et al. . Lifetime prevalence, age of risk, and genetic relationships of comorbid psychiatric disorders in Tourette syndrome. JAMA Psychiatry 2015;72:325–33. 10.1001/jamapsychiatry.2014.2650
    1. Groth C, Mol Debes N, Rask CU, et al. . Course of Tourette syndrome and comorbidities in a large prospective clinical study. J Am Acad Child Adolesc Psychiatry 2017;56:304–12. 10.1016/j.jaac.2017.01.010
    1. Albin RL, Mink JW. Recent advances in Tourette syndrome research. Trends Neurosci 2006;29:175–82. 10.1016/j.tins.2006.01.001
    1. Mink JW. Basal ganglia dysfunction in Tourette’s syndrome: a new hypothesis. Pediatr Neurol 2001;25:190–8. 10.1016/S0887-8994(01)00262-4
    1. Buse J, Schoenefeld K, Münchau A, et al. . Neuromodulation in Tourette syndrome: dopamine and beyond. Neurosci Biobehav Rev 2013;37:1069–84. 10.1016/j.neubiorev.2012.10.004
    1. Felling RJ, Singer HS. Neurobiology of Tourette syndrome: current status and need for further investigation. J Neurosci 2011;31:12387–95. 10.1523/JNEUROSCI.0150-11.2011
    1. Draper A, Stephenson MC, Jackson GM, et al. . Increased GABA contributes to enhanced control over motor excitability in Tourette syndrome. Curr Biol 2014;24:2343–7. 10.1016/j.cub.2014.08.038
    1. Quezada J, Coffman KA. Current approaches and new developments in the pharmacological management of Tourette syndrome. CNS Drugs 2018;32:33–45. 10.1007/s40263-017-0486-0
    1. Dutta N, Cavanna AE. The effectiveness of habit reversal therapy in the treatment of Tourette syndrome and other chronic tic disorders: a systematic review. Funct Neurol 2014;28:7–12.
    1. Verdellen C, van de Griendt J, Hartmann A, et al. . European clinical guidelines for Tourette syndrome and other tic disorders. Part III: behavioural and psychosocial interventions. Eur Child Adolesc Psychiatry 2011;20:197–207. 10.1007/s00787-011-0167-3
    1. Roessner V, Plessen KJ, Rothenberger A, et al. . European clinical guidelines for Tourette syndrome and other tic disorders. Part II: pharmacological treatment. Eur Child Adolesc Psychiatry 2011;20:173–96. 10.1007/s00787-011-0163-7
    1. Kious BM, Jimenez-Shahed J, Shprecher DR. Treatment-refractory Tourette syndrome. Prog Neuropsychopharmacol Biol Psychiatry 2016;70:227–36. 10.1016/j.pnpbp.2016.02.003
    1. Pappert EJ, Goetz CG, Louis ED, et al. . Objective assessments of longitudinal outcome in Gilles de la Tourette's syndrome. Neurology 2003;61:936–40. 10.1212/01.WNL.0000086370.10186.7C
    1. Vandewalle V, van der Linden C, Groenewegen HJ, et al. . Stereotactic treatment of Gilles de la Tourette syndrome by high frequency stimulation of thalamus. Lancet 1999;353 10.1016/S0140-6736(98)05964-9
    1. Martinez-Ramirez D, Jiminez-Shahed J, Leckman JF, et al. . Efficacy and safety of deep brain stimulation in Tourette syndrome the International Tourette syndrome deep brain stimulation public database and registry. JAMA Neurol 2018;32607:1–7.
    1. Visser-Vandewalle V, Temel Y, Boon P, et al. . Chronic bilateral thalamic stimulation: a new therapeutic approach in intractable Tourette syndrome. J Neurosurg 2003;99:1094–100. 10.3171/jns.2003.99.6.1094
    1. Houeto JL, et al. Tourette's syndrome and deep brain stimulation. J Neurol Neurosurg Psychiatry 2005;76:992–5. 10.1136/jnnp.2004.043273
    1. Zhang J-G, Ge Y, Stead M, et al. . Long-term outcome of globus pallidus internus deep brain stimulation in patients with Tourette syndrome. Mayo Clin Proc 2014;89:1506–14. 10.1016/j.mayocp.2014.05.019
    1. Kefalopoulou Z, Zrinzo L, Jahanshahi M, et al. . Bilateral globus pallidus stimulation for severe Tourette's syndrome: a double-blind, randomised crossover trial. Lancet Neurol 2015;14:595–605. 10.1016/S1474-4422(15)00008-3
    1. Smeets AYJM, Duits AA, Plantinga BR, et al. . Deep brain stimulation of the internal globus pallidus in refractory Tourette syndrome. Clin Neurol Neurosurg 2016;142:54–9. 10.1016/j.clineuro.2016.01.020
    1. Smeets A, Duits AA, Leentjens AFG, et al. . Thalamic deep brain stimulation for refractory Tourette syndrome: Clinical evidence for increasing disbalance of therapeutic effects and side effects at long-term follow-up. Neuromodulation Technol Neural Interface 2016;2017:197–202.
    1. Okun MS, Foote KD, SS W, et al. . A trial of scheduled deep brain stimulation for Tourette syndrome. JAMA Neurol 2017.
    1. Shahed J, Poysky J, Kenney C, et al. . GPI deep brain stimulation for Tourette syndrome improves tics and psychiatric comorbidities. Neurology 2007;68:159–60. 10.1212/01.wnl.0000250354.81556.90
    1. Neuner I, Podoll K, Lenartz D, et al. . Deep brain stimulation in the nucleus accumbens for intractable Tourette's syndrome: follow-up report of 36 months. Biol Psychiatry 2009;65:e5–6. 10.1016/j.biopsych.2008.09.030
    1. Sachdev PS, Cannon E, Coyne TJ, et al. . Bilateral deep brain stimulation of the nucleus accumbens for comorbid obsessive compulsive disorder and Tourette’s syndrome. BMJ Case Rep 2012:10–12.
    1. Piedimonte F, Andreani JCM, Piedimonte L, et al. . Behavioral and motor improvement after deep brain stimulation of the globus pallidus Externus in a case of Tourette's syndrome. Neuromodulation 2013;16:55–8. 10.1111/j.1525-1403.2012.00526.x
    1. Cury RG, Lopez WOC, dos Santos Ghilardi MG, et al. . Parallel improvement in anxiety and tics after DBS for medically intractable Tourette syndrome: a long-term follow-up. Clin Neurol Neurosurg 2016;144:33–5. 10.1016/j.clineuro.2016.02.030
    1. Ackermans L, Temel Y, Cath D, et al. . Deep brain stimulation in Tourette's syndrome: two targets? Mov Disord. 2006;21:709–13. 10.1002/mds.20816
    1. Kano Y, Matsuda N, Nonaka M, et al. . Sensory phenomena and obsessive-compulsive symptoms in Tourette syndrome following deep brain stimulation: two case reports. J Clin Neurosci 2018:5–7.
    1. Huys D, Bartsch C, Koester P, et al. . Motor improvement and emotional stabilization in patients with Tourette syndrome after deep brain stimulation of the ventral anterior and ventrolateral motor part of the thalamus. Biol Psychiatry 2016;79:392–401. 10.1016/j.biopsych.2014.05.014
    1. Ackermans L, Duits A, van der Linden C, et al. . Double-blind clinical trial of thalamic stimulation in patients with Tourette syndrome. Brain 2011;134:832–44. 10.1093/brain/awq380
    1. Maciunas RJ, Maddux BN, Riley DE, et al. . Prospective randomized double-blind trial of bilateral thalamic deep brain stimulation in adults with Tourette syndrome. JNS 2007;107:1004–14. 10.3171/JNS-07/11/1004
    1. Servello D, Porta M, Sassi M, et al. . Deep brain stimulation in 18 patients with severe Gilles de la Tourette syndrome refractory to treatment: the surgery and stimulation. J Neurol Neurosurg Psychiatry 2008;79:136–42. 10.1136/jnnp.2006.104067
    1. Servello D, Zekaj E, Saleh C, et al. . Deep brain stimulation in Gilles de la Tourette syndrome: what does the future hold? A cohort of 48 patients. Neurosurgery 2016;78:91–100. 10.1227/NEU.0000000000001004
    1. Welter M-L, Mallet L, Houeto J-L, et al. . Internal pallidal and thalamic stimulation in patients with Tourette syndrome. Arch Neurol 2008;65:952–7. 10.1001/archneur.65.7.952
    1. Welter M-L, Houeto J-L, Thobois S, et al. . Anterior pallidal deep brain stimulation for Tourette's syndrome: a randomised, double-blind, controlled trial. Lancet Neurol 2017;16:610–9. 10.1016/S1474-4422(17)30160-6
    1. Martínez-Fernández R, Zrinzo L, Aviles-Olmos I, et al. . Deep brain stimulation for Gilles de la Tourette syndrome: a case series targeting subregions of the globus pallidus internus. Mov. Disord. 2011;26:1922–30. 10.1002/mds.23734
    1. Bajwa RJ, de Lotbinière AJ, King RA, et al. . Deep brain stimulation in Tourette's syndrome. Mov Disord 2007;22:1346–50. 10.1002/mds.21398
    1. Shields DC, Cheng ML, Flaherty AW, et al. . Microelectrode-guided deep brain stimulation for Tourette syndrome: Within-subject comparison of different stimulation sites. Stereotact Funct Neurosurg 2008;86:87–91. 10.1159/000112429
    1. Azimi A, Parvaresh M, Shahidi G, et al. . Anteromedial GPI deep brain stimulation in Tourette syndrome: the first case series from Iran. Clin Neurol Neurosurg 2018;172:116–9. 10.1016/j.clineuro.2018.06.045
    1. Cannon E, Silburn P, Coyne T, et al. . Deep brain stimulation of anteromedial globus pallidus interna for severe Tourette's syndrome. AJP 2012;169:860–6. 10.1176/appi.ajp.2012.11101583
    1. Sachdev PS, Mohan A, Cannon E, et al. . Deep brain stimulation of the antero-medial globus pallidus interna for Tourette syndrome. PLoS ONE 2014;9:e104926 10.1371/journal.pone.0104926
    1. Dehning S, Mehrkens J-H, Müller N, et al. . Therapy-refractory Tourette syndrome: beneficial outcome with globus pallidus internus deep brain stimulation. Mov Disord 2008;23:1300–2. 10.1002/mds.21930
    1. Flaherty AW, Williams ZM, Amirnovin R, et al. . Deep brain stimulation of the anterior internal capsule for the treatment of Tourette syndrome: technical case report. Neurosurgery 2005;57.
    1. Kuhn J, Lenartz D, Mai JK, et al. . Deep brain stimulation of the nucleus accumbens and the internal capsule in therapeutically refractory Tourette-syndrome. J Neurol 2007;254:963–5. 10.1007/s00415-006-0404-8
    1. Greenberg BD, Gabriels LA, Malone DA, et al. . Deep brain stimulation of the ventral internal capsule/ventral striatum for obsessive-compulsive disorder: Worldwide experience. Mol Psychiatry 2010;15:64–79. 10.1038/mp.2008.55
    1. Martinez-Torres I, Hariz MI, Zrinzo L, et al. . Improvement of tics after subthalamic nucleus deep brain stimulation. Neurology 2009;72:1787–9. 10.1212/WNL.0b013e3181a60a0c
    1. Baldermann JC, Schüller T, Huys D, et al. . Deep brain stimulation for Tourette-Syndrome: a systematic review and meta-analysis. Brain Stimul 2016;9:296–304. 10.1016/j.brs.2015.11.005
    1. Butson CR, Cooper SE, Henderson JM, et al. . Patient-specific analysis of the volume of tissue activated during deep brain stimulation. NeuroImage 2007;34:661–70. 10.1016/j.neuroimage.2006.09.034
    1. Butson CR, McIntyre CC. Current steering to control the volume of tissue activated during deep brain stimulation. Brain Stimul 2008;1:7–15. 10.1016/j.brs.2007.08.004
    1. Butson CR, McIntyre CC. Tissue and electrode capacitance reduce neural activation volumes during deep brain stimulation. Clin Neurophysiol 2005;116:2490–500. 10.1016/j.clinph.2005.06.023
    1. Butson CR, Cooper SE, Henderson JM, et al. . Probabilistic analysis of activation volumes generated during deep brain stimulation. Neuroimage 2011;54:2096–104. 10.1016/j.neuroimage.2010.10.059
    1. Cooper SE, Driesslein KG, Noecker AM, et al. . Anatomical targets associated with abrupt versus gradual washout of subthalamic deep brain stimulation effects on bradykinesia. PLoS ONE 2014;9:e99663 10.1371/journal.pone.0099663
    1. Dembek TA, Barbe MT, Åström M, et al. . Probabilistic mapping of deep brain stimulation effects in essential tremor. NeuroImage Clin 2017;13:164–73. 10.1016/j.nicl.2016.11.019
    1. Eisenstein SA, Koller JM, Black KD, et al. . Functional anatomy of subthalamic nucleus stimulation in Parkinson disease. Ann Neurol 2014;76:279–95. 10.1002/ana.24204
    1. Krishna V, King NKK, Sammartino F, et al. . Anterior nucleus deep brain stimulation for refractory epilepsy: insights into patterns of seizure control and efficacious target. Neurosurgery 2016;78:802–11.
    1. Horn A, Neumann WJ, Degen K, et al. . Toward an electrophysiological ‘sweet spot’ for deep brain stimulation in the subthalamic nucleus. Hum Brain Mapp 2017;3390:3377–90.
    1. Deeb W, Rossi PJ, Porta M, et al. . The International deep brain stimulation registry and database for Gilles de la Tourette syndrome: how does it work? Front. Neurosci. 2016;10 10.3389/fnins.2016.00170
    1. Schrock LE, Mink JW, Woods DW, et al. . Tourette syndrome deep brain stimulation: a review and updated recommendations. Mov Disord. 2015;30:448–71. 10.1002/mds.26094
    1. Leckman JF, Riddle MA, Hardin MT, et al. . The Yale Global Tic Severity Scale: initial testing of a Clinician-Rated scale of tic severity. J Am Acad Child Adolesc Psychiatry 1989;28:566–73. 10.1097/00004583-198907000-00015
    1. Goodman WK, et al. The Yale-Brown obsessive compulsive scale. Arch Gen Psychiatry 1989;46:1006–11. 10.1001/archpsyc.1989.01810110048007
    1. Johnson H, Harris G, Williams K. BRAINSFit: mutual information rigid registrations of whole-brain 3D images, using the INSIGHT toolkit. Insight J 2007:1–10.
    1. Fedorov A, Beichel R, Kalpathy-Cramer J, et al. . 3D slicer as an image computing platform for the quantitative imaging network. Magn Reson Imaging 2012;30:1323–41. 10.1016/j.mri.2012.05.001
    1. McIntyre CC, Richardson AG, Grill WM. Modeling the excitability of mammalian nerve fibers: influence of afterpotentials on the recovery cycle. J Neurophysiol 2002;87:995–1006. 10.1152/jn.00353.2001
    1. Carnevale T, Hines M. The NEURON Book. Cambridge University Press, 2006.
    1. Hromatka M, Liu W, Anderson J, et al. . Accounting for Heterogeneity Across Multiple Imaging Sites Using Multi-Task Learning. MICCAI Work Bayesian Graph Model Biomed Imaging, 2015. Available:
    1. Hromatka M, Zhang M, Fleishman G, et al. . A hierarchical Bayesian model for multi-site Diffeomorphic image atlases. Med Image Comput Comput Assist Interv 2015;9350.
    1. Avants B, Epstein C, Grossman M, et al. . Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal 2008;12:26–41. 10.1016/j.media.2007.06.004
    1. Fonov VS, Evans AC, McKinstry RC, et al. . Unbiased nonlinear average age-appropriate brain templates from birth to adulthood. NeuroImage 2009;47 10.1016/S1053-8119(09)70884-5
    1. Fonov V, Evans AC, Botteron K, et al. . Unbiased average age-appropriate atlases for pediatric studies. NeuroImage 2011;54:313–27. 10.1016/j.neuroimage.2010.07.033
    1. Horn A, Kühn AA. Lead-DBS: a toolbox for deep brain stimulation electrode localizations and visualizations. NeuroImage 2015;107:127–35. 10.1016/j.neuroimage.2014.12.002
    1. Makris N, Goldstein JM, Kennedy D, et al. . Decreased volume of left and total anterior insular lobule in schizophrenia. Schizophr Res 2006;83:155–71. 10.1016/j.schres.2005.11.020
    1. Frazier JA, Chiu S, Breeze JL, et al. . Structural brain magnetic resonance imaging of limbic and thalamic volumes in pediatric bipolar disorder. AJP 2005;162:1256–65. 10.1176/appi.ajp.162.7.1256
    1. Desikan RS, Ségonne F, Fischl B, et al. . An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 2006;31:968–80. 10.1016/j.neuroimage.2006.01.021
    1. Goldstein JM, Seidman LJ, Makris N, et al. . Hypothalamic abnormalities in schizophrenia: sex effects and genetic vulnerability. Biol Psychiatry 2007;61:935–45. 10.1016/j.biopsych.2006.06.027
    1. Ewert S, Plettig P, Li N, et al. . Toward defining deep brain stimulation targets in MNI space: a subcortical atlas based on multimodal MRI, histology and structural connectivity. NeuroImage 2018;170:271–82. 10.1016/j.neuroimage.2017.05.015
    1. Chakravarty MM, Bertrand G, Hodge CP, et al. . The creation of a brain atlas for image guided neurosurgery using serial histological data. NeuroImage 2006;30:359–76. 10.1016/j.neuroimage.2005.09.041
    1. Storch EA, De Nadai AS, Lewin AB, et al. . Defining treatment response in pediatric tic disorders: a signal detection analysis of the Yale Global Tic Severity Scale. J Child Adolesc Psychopharmacol 2011;21:621–7. 10.1089/cap.2010.0149
    1. Jeon S, Walkup JT, Woods DW, et al. . Detecting a clinically meaningful change in tic severity in Tourette syndrome: a comparison of three methods. Contemp Clin Trials 2013;36:414–20. 10.1016/j.cct.2013.08.012
    1. Diederich NJ, Kalteis K, Stamenkovic M, et al. . Efficient internal pallidal stimulation in Gilles de la Tourette syndrome: a case report. Mov Disord 2005;20:1496–9. 10.1002/mds.20551
    1. Lozano AM, Mayberg HS, Giacobbe P, et al. . Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression. Biol Psychiatry 2008;64:461–7. 10.1016/j.biopsych.2008.05.034
    1. Bewernick BH, Kayser S, Gippert SM, et al. . Deep brain stimulation to the medial forebrain bundle for depression- long-term outcomes and a novel data analysis strategy. Brain Stimul 2017;10:664–71. 10.1016/j.brs.2017.01.581
    1. Mayberg HS, Lozano AM, Voon V, et al. . Deep brain stimulation for treatment-resistant depression. Neuron 2005;45:651–60. 10.1016/j.neuron.2005.02.014
    1. Bourne SK, Eckhardt CA, Sheth SA, et al. . Mechanisms of deep brain stimulation for obsessive compulsive disorder: effects upon cells and circuits. Front Integr Neurosci 2012;6:1–14. 10.3389/fnint.2012.00029
    1. Krause M, Fogel W, Kloss M, et al. . Pallidal stimulation for dystonia. Neurosurgery 2004;55:1361–70. 10.1227/01.NEU.0000143331.86101.5E
    1. Ruge D, Tisch S, Hariz MI, et al. . Deep brain stimulation effects in dystonia: time course of electrophysiological changes in early treatment. Mov. Disord. 2011;26:1913–21. 10.1002/mds.23731
    1. McCairn KW, Iriki A, Isoda M. Deep brain stimulation reduces Tic-Related neural activity via temporal locking with stimulus pulses. J Neurosci 2013;33:6581–93. 10.1523/JNEUROSCI.4874-12.2013
    1. Bour LJ, Ackermans L, Foncke EMJ, et al. . Tic related local field potentials in the thalamus and the effect of deep brain stimulation in Tourette syndrome: report of three cases. Clin Neurophysiol 2015;126:1578–88. 10.1016/j.clinph.2014.10.217
    1. Maling N, Hashemiyoon R, Foote KD, et al. . Correction: Increased Thalamic Gamma Band Activity Correlates with Symptom Relief following Deep Brain Stimulation in Humans with Tourette’s Syndrome. PLoS ONE 2012;7:1–8. 10.1371/annotation/446ec4cb-63da-42d2-afc6-7e8459b2abbe
    1. Alam M, Schwabe K, Lütjens G, et al. . Comparative characterization of single cell activity in the globus pallidus internus of patients with dystonia or Tourette syndrome. J Neural Transm 2015;122:687–99. 10.1007/s00702-014-1277-0
    1. Priori A, Giannicola G, Rosa M, et al. . Deep brain electrophysiological recordings provide clues to the pathophysiology of Tourette syndrome. Neurosci Biobehav Rev 2013;37:1063–8. 10.1016/j.neubiorev.2013.01.011
    1. Weaver FM, Follett KA, Stern M, et al. . Randomized trial of deep brain stimulation for Parkinson disease: thirty-six-month outcomes. Neurology 2012;79:55–65. 10.1212/WNL.0b013e31825dcdc1
    1. Mink JW. The basal ganglia and involuntary movements. Arch Neurol 2003;60:1365–8. 10.1001/archneur.60.10.1365
    1. Akbarian-Tefaghi L, Zrinzo L, Foltynie T. The use of deep brain stimulation in Tourette syndrome. Brain Sci 2016;6:35–19. 10.3390/brainsci6030035
    1. Hashemiyoon R, Kuhn J, Visser-Vandewalle V. Putting the pieces together in Gilles de la Tourette syndrome: exploring the link between clinical observations and the biological basis of dysfunction. Brain Topogr 2016;30:1–27.
    1. Neumann W-J, Huebl J, Brücke C, et al. . Pallidal and thalamic neural oscillatory patterns in Tourette's syndrome. Ann Neurol 2018;84:505–14. 10.1002/ana.25311
    1. Stern E, Silbersweig DA, Chee K-Y, et al. . A functional neuroanatomy of tics in Tourette syndrome. Arch Gen Psychiatry 2000;57:741–8. 10.1001/archpsyc.57.8.741
    1. Nakao T, Okada K, Kanba S. Neurobiological model of obsessive-compulsive disorder: evidence from recent neuropsychological and neuroimaging findings. Psychiatry Clin Neurosci 2014;68:587–605. 10.1111/pcn.12195
    1. Miyagi Y, Shima F, Sasaki T. Brain shift: an error factor during implantation of deep brain stimulation electrodes. JNS 2007;107:989–97. 10.3171/JNS-07/11/0989
    1. Halpern CH, Danish SF, Baltuch GH, et al. . Brain shift during deep brain stimulation surgery for Parkinson’s disease. Stereotact Funct Neurosurg 2008;86:37–43. 10.1159/000108587
    1. Sillay KA, Kumbier LM, Ross C, et al. . Perioperative brain shift and deep brain stimulating electrode deformation analysis: implications for rigid and non-rigid devices. Ann Biomed Eng 2013;41:293–304. 10.1007/s10439-012-0650-0
    1. Kelly PJ, Gillingham FJ. The long-term results of stereotaxic surgery and L-dopa therapy in patients with Parkinson's disease. J Neurosurg 1980;53:332–7. 10.3171/jns.1980.53.3.0332
    1. Nestor KA, Jones JD, Butson CR, et al. . Coordinate-Based lead location does not predict Parkinson's disease deep brain stimulation outcome. PLoS ONE 2014;9:e93524 10.1371/journal.pone.0093524
    1. Akbarian-Tefaghi L, Akram H, Johansson J, et al. . Refining the deep brain stimulation target within the limbic globus pallidus internus for Tourette syndrome. Stereotact Funct Neurosurg 2017;95:251–8. 10.1159/000478273
    1. Marques JP, Kober T, Krueger G, et al. . MP2RAGE, a self bias-field corrected sequence for improved segmentation and T1-mapping at high field. NeuroImage 2010;49:1271–81. 10.1016/j.neuroimage.2009.10.002
    1. Athawale TM, Johnson KA, Butson CR, et al. . A statistical framework for quantification and visualisation of positional uncertainty in deep brain stimulation electrodes. Comput Methods Biomech Biomed Eng Imaging Vis 2018;00:1–12. 10.1080/21681163.2018.1523750
    1. Saleh C, Dooms G, Berthold C, et al. . Post-operative imaging in deep brain stimulation: a controversial issue. Neuroradiol J 2016;29:244–9. 10.1177/1971400916639960
    1. Hemm S, Coste J, Gabrillargues J, et al. . Contact position analysis of deep brain stimulation electrodes on post-operative CT images. Acta Neurochirurgica 2009;151:823–9. 10.1007/s00701-009-0393-3
    1. Goetz CG, Pappert EJ, Louis ED, et al. . Advantages of a modified scoring method for the rush video-based tic rating scale. Mov Disord 1999;14:502–6. 10.1002/1531-8257(199905)14:3&lt;502::AID-MDS1020&gt;;2-G
    1. Goetz CG, Tanner CM, Wilson RS, et al. . A rating scale for Gilles de la Tourette's syndrome: description, reliability, and validity data. Neurology 1987;37:1542–4. 10.1212/WNL.37.9.1542
    1. Pedroarena-Leal N, Ruge D. Toward a Symptom-Guided neurostimulation for Gilles de la Tourette syndrome. Front Psychiatry 2017;8 10.3389/fpsyt.2017.00029
    1. Worbe Y, Gerardin E, Hartmann A, et al. . Distinct structural changes underpin clinical phenotypes in patients with Gilles de la Tourette syndrome. Brain 2010;133:3649–60. 10.1093/brain/awq293
    1. Almeida L, Martinez-Ramirez D, Rossi PJ, 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 2015;11:122–31. 10.3988/jcn.2015.11.2.122
    1. Molina R, Okun MS, Shute JB, et al. . Report of a patient undergoing chronic responsive deep brain stimulation for Tourette syndrome: proof of concept. J Neurosurg 2017:1–7.
    1. Shute JB, Okun MS, Opri E, et al. . Thalamocortical network activity enables chronic tic detection in humans with Tourette syndrome. NeuroImage Clinical 2016;12:165–72. 10.1016/j.nicl.2016.06.015
    1. Marceglia S, Rosa M, Servello D, et al. . Adaptive deep brain stimulation (aDBS) for Tourette syndrome. Brain Sci 2018;8.
    1. Schüpbach WMM, Chabardes S, Matthies C, et al. . Directional leads for deep brain stimulation: opportunities and challenges. Mov Disord 2017;32:1371–5. 10.1002/mds.27096

Source: PubMed

Sponsor e collaboratori

Condizioni mediche

Interventi farmacologici

3
Sottoscrivi