A unified connectomic target for deep brain stimulation in obsessive-compulsive disorder.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
03 07 2020
Historique:
received: 13 04 2019
accepted: 21 05 2020
entrez: 5 7 2020
pubmed: 6 7 2020
medline: 29 8 2020
Statut: epublish

Résumé

Multiple surgical targets for treating obsessive-compulsive disorder with deep brain stimulation (DBS) have been proposed. However, different targets may modulate the same neural network responsible for clinical improvement. We analyzed data from four cohorts of patients (N = 50) that underwent DBS to the anterior limb of the internal capsule (ALIC), the nucleus accumbens or the subthalamic nucleus (STN). The same fiber bundle was associated with optimal clinical response in cohorts targeting either structure. This bundle connected frontal regions to the STN. When informing the tract target based on the first cohort, clinical improvements in the second could be significantly predicted, and vice versa. To further confirm results, clinical improvements in eight patients from a third center and six patients from a fourth center were significantly predicted based on their stimulation overlap with this tract. Our results show that connectivity-derived models may inform clinical improvements across DBS targets, surgeons and centers. The identified tract target is openly available in atlas form.

Identifiants

pubmed: 32620886
doi: 10.1038/s41467-020-16734-3
pii: 10.1038/s41467-020-16734-3
pmc: PMC7335093
doi:

Types de publication

Clinical Trial Journal Article Multicenter Study Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3364

Subventions

Organisme : Medical Research Council
ID : MR/J012009/1
Pays : United Kingdom
Organisme : NIMH NIH HHS
ID : U54 MH091657
Pays : United States

Références

Ruscio, A. M., Stein, D. J., Chiu, W. T. & Kessler, R. C. The epidemiology of obsessive-compulsive disorder in the National Comorbidity Survey Replication. Mol. Psychiatry 15, 53–63 (2010).
pubmed: 18725912 doi: 10.1038/mp.2008.94
Anderson, D. & Ahmed, A. Treatment of patients with intractable obsessive—compulsive disorder with anterior capsular stimulation: case report. J. Neurosurg. 98, 1104–1108 (2003).
pubmed: 12744372 doi: 10.3171/jns.2003.98.5.1104
Mallet, L. et al. Compulsions, Parkinson’s disease, and stimulation. Lancet 360, 1302–1304 (2002).
pubmed: 12414208 doi: 10.1016/S0140-6736(02)11339-0
Chabardès, S. et al. Deep brain stimulation for obsessive-compulsive disorder: subthalamic nucleus target. World Neurosurg. 80, S31.e1–S31.e8 (2013).
doi: 10.1016/j.wneu.2012.03.010
Sturm, V. et al. The nucleus accumbens: a target for deep brain stimulation in obsessive–compulsive- and anxiety-disorders. J. Chem. Neuroanat. 26, 293–299 (2003).
pubmed: 14729131 doi: 10.1016/j.jchemneu.2003.09.003
Greenberg, B. D. et al. Three-year outcomes in deep brain stimulation for highly resistant obsessive–compulsive disorder. Neuropsychopharmacology 31, 2384–2393 (2006).
pubmed: 16855529 doi: 10.1038/sj.npp.1301165
Jiménez-Ponce, F. et al. Preliminary study in patients with obsessive-compulsive disorder treated with electrical stimulation in the inferior thalamic peduncle. Oper. Neurosurg. 65, ons203–ons209 (2009).
doi: 10.1227/01.NEU.0000345938.39199.90
Luyten, L., Hendrickx, S., Raymaekers, S., Gabriëls, L. & Nuttin, B. Electrical stimulation in the bed nucleus of the stria terminalis alleviates severe obsessive-compulsive disorder. Mol. Psychiatry 21, 1272–1280 (2016).
pubmed: 26303665 doi: 10.1038/mp.2015.124
Nair, G., Evans, A., Bear, R. E., Velakoulis, D. & Bittar, R. G. The anteromedial GPi as a new target for deep brain stimulation in obsessive compulsive disorder. J. Clin. Neurosci. 21, 815–821 (2014).
pubmed: 24524950 doi: 10.1016/j.jocn.2013.10.003
Coenen, V. A. et al. The medial forebrain bundle as a target for deep brain stimulation for obsessive-compulsive disorder. CNS Spectr. 22, 282–289 (2017).
pubmed: 27268576 doi: 10.1017/S1092852916000286
Maarouf, M. et al. Deep brain stimulation of medial dorsal and ventral anterior nucleus of the thalamus in OCD: a retrospective case series. PLoS ONE 11, e0160750 (2016).
pubmed: 27504631 pmcid: 4978440 doi: 10.1371/journal.pone.0160750
Borders, C., Hsu, F., Sweidan, A. J., Matei, E. S. & Bota, R. G. Deep brain stimulation for obsessive compulsive disorder: A review of results by anatomical target. Ment. Illn. 10, 7900 (2018).
Tyagi, H. et al. A randomized trial directly comparing ventral capsule and anteromedial subthalamic nucleus stimulation in obsessive-compulsive disorder: clinical and imaging evidence for dissociable effects. Biol. Psychiatry https://doi.org/10.1016/j.biopsych.2019.01.017 (2019).
Choi, K. S., Riva-Posse, P., Gross, R. E. & Mayberg, H. S. Mapping the “Depression Switch” during intraoperative testing of subcallosal cingulate deep brain stimulation. JAMA Neurol. 72, 1252–1260 (2015).
pubmed: 26408865 pmcid: 4834289 doi: 10.1001/jamaneurol.2015.2564
Riva-Posse, P. et al. A connectomic approach for subcallosal cingulate deep brain stimulation surgery: prospective targeting in treatment-resistant depression. Mol. Psychiatry 23, 843–849 (2018).
pubmed: 28397839 doi: 10.1038/mp.2017.59
Henderson, J. M. M. D. “Connectomic surgery”: diffusion tensor imaging (DTI) tractography as a targeting modality for surgical modulation of neural networks. Front. Integr. Neurosci. 6, 15 (2012).
Petersen, M. V. et al. Holographic reconstruction of axonal pathways in the human brain. Neuron 104, 1056–1064.e3 (2019).
pubmed: 31708306 doi: 10.1016/j.neuron.2019.09.030 pmcid: 6948195
Feldman, R. P. & Goodrich, J. T. Psychosurgery: a historical overview. Neurosurgery 48, 647–659 (2001).
pubmed: 11270556 doi: 10.1097/00006123-200103000-00041
Coenen, V. A., Allert, N. & Mädler, B. A role of diffusion tensor imaging fiber tracking in deep brain stimulation surgery: DBS of the dentato-rubro-thalamic tract (drt) for the treatment of therapy-refractory tremor. Acta Neurochir. 153, 1579–1585 (2011).
pubmed: 21553318 doi: 10.1007/s00701-011-1036-z
Schlaepfer, T. E., Bewernick, B. H., Kayser, S., Hurlemann, R. & Coenen, V. A. Deep Brain Stimulation of the Human Reward System for Major Depression—Rationale, Outcomes and Outlook. Neuropsychopharmacology 39, 1303–1314 (2014).
Heilbronner, S. R., Safadi, Z. & Haber, S. N. in Neuromodulation in Psychiatry (eds. Hamani, C., Lozano, A., Holtzheimer, P. & Mayberg, H.) 27–48 (John Wiley & Sons, Ltd, 2016).
Horn, A. et al. Connectivity predicts deep brain stimulation outcome in Parkinson disease. Ann. Neurol. 82, 67–78 (2017).
pubmed: 28586141 pmcid: 5880678 doi: 10.1002/ana.24974
Irmen, F. et al. Left Prefrontal Connectivity Links Subthalamic Stimulation with Depressive Symptoms. Ann. Neurol. 87, 962–975 (2020).
Baldermann, J. C. et al. Connectivity profile predictive of effective deep brain stimulation in obsessive compulsive disorder. Biol. Psychiatry https://doi.org/10.1016/j.biopsych.2018.12.019 (2019).
Akram, H. et al. Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease. NeuroImage 158, 332–345 (2017).
pubmed: 28711737 doi: 10.1016/j.neuroimage.2017.07.012
Vanegas-Arroyave, N. et al. Tractography patterns of subthalamic nucleus deep brain stimulation. Brain 139, 1200–1210 (2016).
pubmed: 26921616 pmcid: 5006230 doi: 10.1093/brain/aww020
Vissani, M. et al. Spatio-temporal structure of single neuron subthalamic activity identifies DBS target for anesthetized Tourette syndrome patients. J. Neural Eng. 16, 066011 (2019).
pubmed: 31370042 doi: 10.1088/1741-2552/ab37b4
Alkemade, A., Groot, J. M. & Forstmann, B. U. Do we need a human post mortem whole-brain anatomical ground truth in in vivo magnetic resonance imaging? Front. Neuroanat. 12, 110 (2018).
Polosan, M. et al. Affective modulation of the associative-limbic subthalamic nucleus: deep brain stimulation in obsessive–compulsive disorder. Transl. Psychiatry 9, 73 (2019).
pubmed: 30718450 pmcid: 6361948 doi: 10.1038/s41398-019-0404-y
Barcia, J. A. et al. Personalized striatal targets for deep brain stimulation in obsessive-compulsive disorder. Brain Stimul. https://doi.org/10.1016/j.brs.2018.12.226 (2018).
Maier-Hein, K. H. et al. The challenge of mapping the human connectome based on diffusion tractography. Nat. Commun. 8, 1349 (2017).
pubmed: 29116093 pmcid: 5677006 doi: 10.1038/s41467-017-01285-x
Horn, A. et al. Probabilistic conversion of neurosurgical DBS electrode coordinates into MNI space. NeuroImage 150, 395–404 (2017).
pubmed: 28163141 doi: 10.1016/j.neuroimage.2017.02.004
Haynes, W. I. A. & Haber, S. N. The organization of prefrontal-subthalamic inputs in primates provides an anatomical substrate for both functional specificity and integration: implications for basal ganglia models and deep brain stimulation. J. Neurosci. 33, 4804–4814 (2013).
pubmed: 23486951 pmcid: 3755746 doi: 10.1523/JNEUROSCI.4674-12.2013
Nieuwenhuys, R., Voogd, J. & van Huijzen, C. The Human Central Nervous System (Springer, Berlin, 2008).
McIntyre, C. C. & Hahn, P. J. Network perspectives on the mechanisms of deep brain stimulation. Neurobiol. Dis. 38, 329–337 (2010).
pubmed: 19804831 doi: 10.1016/j.nbd.2009.09.022
Nambu, A., Tokuno, H. & Takada, M. Functional significance of the cortico–subthalamo–pallidal ‘hyperdirect’ pathway. Neurosci. Res. 43, 111–117 (2002).
pubmed: 12067746 doi: 10.1016/S0168-0102(02)00027-5
Coenen, V. A. et al. Surgical decision making for deep brain stimulation should not be based on aggregated normative data mining. Brain Stimul. 12, 1345–1348 (2019).
Nougaret, S., Meffre, J., Duclos, Y., Breysse, E. & Pelloux, Y. First evidence of a hyperdirect prefrontal pathway in the primate: precise organization for new insights on subthalamic nucleus functions. Front. Comput. Neurosci. 7, 135 (2013).
Chudasama, Y., Baunez, C. & Robbins, T. W. Functional disconnection of the medial prefrontal cortex and subthalamic nucleus in attentional performance: evidence for corticosubthalamic interaction. J. Neurosci. 23, 5477–5485 (2003).
pubmed: 12843247 pmcid: 6741240 doi: 10.1523/JNEUROSCI.23-13-05477.2003
McGovern, R. A. & Sheth, S. A. Role of the dorsal anterior cingulate cortex in obsessive-compulsive disorder: converging evidence from cognitive neuroscience and psychiatric neurosurgery. J. Neurosurg. 126, 132–147 (2017).
pubmed: 27035167 doi: 10.3171/2016.1.JNS15601
Dougherty, D. D. et al. Prospective long-term follow-up of 44 patients who received cingulotomy for treatment-refractory obsessive-compulsive disorder. Am. J. Psychiatry 159, 269–275 (2002).
pubmed: 11823270 doi: 10.1176/appi.ajp.159.2.269
Schilling, K. G. et al. Challenges in diffusion MRI tractography—lessons learned from international benchmark competitions. Magn. Reson. Imaging 57, 194–209 (2019).
pubmed: 30503948 doi: 10.1016/j.mri.2018.11.014
Parent, A. & Hazrati, L.-N. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidium in basal ganglia circuitry. Brain Res. Rev. 20, 128–154 (1995).
pubmed: 7711765 doi: 10.1016/0165-0173(94)00008-D
Coenen, V. A. et al. Tractographic description of major subcortical projection pathways passing the anterior limb of the internal capsule. Corticopetal organization of networks relevant for psychiatric disorders. NeuroImage Clin. 25, 102165 (2020).
pubmed: 31954987 pmcid: 6965747 doi: 10.1016/j.nicl.2020.102165
Liebrand, L. C. et al. Individual white matter bundle trajectories are associated with deep brain stimulation response in obsessive-compulsive disorder. Brain Stimul. 12, 353–360 (2019).
pubmed: 30522916 doi: 10.1016/j.brs.2018.11.014
Safadi, Z. et al. Functional segmentation of the anterior limb of the internal capsule: linking white matter abnormalities to specific connections. J. Neurosci. 38, 2106–2117 (2018).
pubmed: 29358360 pmcid: 5824744 doi: 10.1523/JNEUROSCI.2335-17.2017
Mataix-Cols, D. et al. Distinct neural correlates of washing, checking, and hoarding symptom dimensions in obsessive-compulsive disorder. Arch. Gen. Psychiatry 61, 564–576 (2004).
pubmed: 15184236 doi: 10.1001/archpsyc.61.6.564
Al-Fatly, B. et al. Connectivity profile of thalamic deep brain stimulation to effectively treat essential tremor. Brain https://doi.org/10.1093/brain/awz236 (2019).
Mayberg, H. S. et al. Deep brain stimulation for treatment-resistant depression. Neuron 45, 651–660 (2005).
pubmed: 15748841 doi: 10.1016/j.neuron.2005.02.014
Schlaepfer, T. E., Bewernick, B. H., Kayser, S., Mädler, B. & Coenen, V. A. Rapid effects of deep brain stimulation for treatment-resistant major depression. Biol. Psychiatry 73, 1204–1212 (2013).
pubmed: 23562618 doi: 10.1016/j.biopsych.2013.01.034
Odekerken, V. J. J. et al. GPi vs STN deep brain stimulation for Parkinson disease: three-year follow-up. Neurology 86, 755–761 (2016).
pubmed: 26819458 doi: 10.1212/WNL.0000000000002401
Van Essen, D. C. et al. The WU-Minn human connectome project: an overview. NeuroImage 80, 62–79 (2013).
pubmed: 23684880 doi: 10.1016/j.neuroimage.2013.05.041
Darby, R. R., Horn, A., Cushman, F. & Fox, M. D. Lesion network localization of criminal behavior. Proc. Natl Acad. Sci. USA 115, 601–606 (2018).
pubmed: 29255017 doi: 10.1073/pnas.1706587115
Joutsa, J. et al. Identifying therapeutic targets from spontaneous beneficial brain lesions. Ann. Neurol. 84, 153–157 (2018).
pubmed: 30014594 doi: 10.1002/ana.25285
Weigand, A. et al. Prospective validation that subgenual connectivity predicts antidepressant efficacy of transcranial magnetic stimulation sites. Biol. Psychiatry 84, 28–37 (2018).
pubmed: 29274805 doi: 10.1016/j.biopsych.2017.10.028
Petersen, M. V. et al. Probabilistic versus deterministic tractography for delineation of the cortico-subthalamic hyperdirect pathway in patients with Parkinson disease selected for deep brain stimulation. J. Neurosurg. 126, 1657–1668 (2017).
pubmed: 27392264 doi: 10.3171/2016.4.JNS1624
Jakab, A. et al. Feasibility of diffusion tractography for the reconstruction of intra-thalamic and cerebello-thalamic targets for functional neurosurgery: a multi-vendor pilot study in four subjects. Front. Neuroanat. 10, 76 (2016).
Horn, A. et al. Lead-DBS v2: towards a comprehensive pipeline for deep brain stimulation imaging. NeuroImage 184, 293–316 (2019).
pubmed: 30179717 doi: 10.1016/j.neuroimage.2018.08.068
Husch, A., V. Petersen, M., Gemmar, P., Goncalves, J. & Hertel, F. PaCER—a fully automated method for electrode trajectory and contact reconstruction in deep brain stimulation. NeuroImage Clin. 17, 80–89 (2017).
pubmed: 29062684 pmcid: 5645007 doi: 10.1016/j.nicl.2017.10.004
Ewert, S. et al. Optimization and comparative evaluation of nonlinear deformation algorithms for atlas-based segmentation of DBS target nuclei. NeuroImage 184, 586–598 (2019).
pubmed: 30267856 doi: 10.1016/j.neuroimage.2018.09.061
Schönecker, T., Kupsch, A., Kühn, A. A., Schneider, G.-H. & Hoffmann, K.-T. Automated optimization of subcortical cerebral mr imaging-atlas coregistration for improved postoperative electrode localization in deep brain stimulation. Am. J. Neuroradiol. 30, 1914–1921 (2009).
pubmed: 19713324 doi: 10.3174/ajnr.A1741 pmcid: 7051288
Avants, B. B., Tustison, N. & Song, G. Advanced normalization tools (ANTS). Insight J. 2, 1–35 (2009).
Pauli, W. M., Nili, A. N. & Tyszka, J. M. A high-resolution probabilistic in vivo atlas of human subcortical brain nuclei. Sci. Data 5, 180063 (2018).
pubmed: 29664465 pmcid: 5903366 doi: 10.1038/sdata.2018.63
Ewert, S. et al. Toward defining deep brain stimulation targets in MNI space: A subcortical atlas based on multimodal MRI, histology and structural connectivity. NeuroImage 170, 271–282 (2018).
pubmed: 28536045 doi: 10.1016/j.neuroimage.2017.05.015
Good, P. I. Permutation, Parametric, and Bootstrap Tests of Hypotheses (Springer-Verlag, 2005).
Mallet, L. et al. Subthalamic nucleus stimulation in severe obsessive–compulsive disorder. N. Engl. J. Med. 359, 2121–2134 (2008).
pubmed: 19005196 doi: 10.1056/NEJMoa0708514
Tsai, H.-C., Chen, S.-Y., Tsai, S.-T., Hung, H.-Y. & Chang, C.-H. Hypomania Following bilateral ventral capsule stimulation in a patient with refractory obsessive-compulsive disorder. Biol. Psychiatry 68, e7–e8 (2010).
pubmed: 20553748 doi: 10.1016/j.biopsych.2010.04.001
Nuttin, B. J. et al. Long-term electrical capsular stimulation in patients with obsessive-compulsive disorder. Neurosurgery 52, 1263–1274 (2003).
pubmed: 12762871 doi: 10.1227/01.NEU.0000064565.49299.9A
Lee, D. J. et al. Inferior thalamic peduncle deep brain stimulation for treatment-refractory obsessive-compulsive disorder: a phase 1 pilot trial. Brain Stimul. 12, 344–352 (2019).
pubmed: 30514614 doi: 10.1016/j.brs.2018.11.012
Nuttin, B. et al. Targeting bed nucleus of the stria terminalis for severe obsessive-compulsive disorder: more unexpected lead placement in obsessive-compulsive disorder than in surgery for movement disorders. World Neurosurg. 80, S30.e11–S30.e16 (2013).
doi: 10.1016/j.wneu.2012.12.029

Auteurs

Ningfei Li (N)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Movement Disorders and Neuromodulation Unit, Department for Neurology, Charitéplatz 1, 10117 Berlin, Germany. ningfei.li@charite.de.

Juan Carlos Baldermann (JC)

Department of Psychiatry and Psychotherapy, Department of Neurology, University of Cologne, Medical Faculty, Cologne, Germany.

Astrid Kibleur (A)

Univ. Grenoble Alpes, 38000, Grenoble, France.
OpenMind Innovation, 75008, Paris, France.

Svenja Treu (S)

Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politecnica de Madrid, Madrid, Spain.

Harith Akram (H)

Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, London, UK.
National Hospital for Neurology and Neurosurgery, UCL Queen Square Institute of Neurology, London, UK.

Gavin J B Elias (GJB)

University Health Network, Toronto, ON, Canada.

Alexandre Boutet (A)

University Health Network, Toronto, ON, Canada.
Joint Department of Medical Imaging, University of Toronto, Toronto, ON, Canada.

Andres M Lozano (AM)

University Health Network, Toronto, ON, Canada.

Bassam Al-Fatly (B)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Movement Disorders and Neuromodulation Unit, Department for Neurology, Charitéplatz 1, 10117 Berlin, Germany.

Bryan Strange (B)

Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politecnica de Madrid, Madrid, Spain.

Juan A Barcia (JA)

Hospital Clínico San Carlos, Neurosurgery Department, Universidad Complutense de Madrid, Madrid, Spain.

Ludvic Zrinzo (L)

Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, London, UK.
National Hospital for Neurology and Neurosurgery, UCL Queen Square Institute of Neurology, London, UK.

Eileen Joyce (E)

Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, London, UK.
National Hospital for Neurology and Neurosurgery, UCL Queen Square Institute of Neurology, London, UK.

Stephan Chabardes (S)

Univ. Grenoble Alpes, 38000, Grenoble, France.

Veerle Visser-Vandewalle (V)

Department of Stereotactic and Functional Neurosurgery, University of Cologne, Cologne, Germany.

Mircea Polosan (M)

Univ. Grenoble Alpes, 38000, Grenoble, France.
Inserm, U1216, Grenoble Institut des Neurosciences, 38000, Grenoble, France.
Psychiatry Department, CHU Grenoble Alpes, 38000, Grenoble, France.

Jens Kuhn (J)

Department of Psychiatry and Psychotherapy, Department of Neurology, University of Cologne, Medical Faculty, Cologne, Germany.
Department of Psychiatry, Psychotherapy and Psychosomatics, EVKLN, Johanniter Hospital Oberhausen, Oberhausen, Germany.

Andrea A Kühn (AA)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Movement Disorders and Neuromodulation Unit, Department for Neurology, Charitéplatz 1, 10117 Berlin, Germany.

Andreas Horn (A)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Movement Disorders and Neuromodulation Unit, Department for Neurology, Charitéplatz 1, 10117 Berlin, Germany.

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