Local neuroanatomical and tract-based proxies of optimal subcallosal cingulate deep brain stimulation
Background: Deep brain stimulation of the subcallosal cingulate area (SCC-DBS) is a promising neuromodulatory therapy for treatment-resistant depression (TRD). Biomarkers of optimal target engagement are needed to guide surgical targeting and stimulation parameter selection and to reduce variance in...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2023-09-01
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| Series: | Brain Stimulation |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1935861X23018909 |
| _version_ | 1797644787858276352 |
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| author | Gavin J.B. Elias Jürgen Germann Alexandre Boutet Michelle E. Beyn Peter Giacobbe Ha Neul Song Ki Sueng Choi Helen S. Mayberg Sidney H. Kennedy Andres M. Lozano |
| author_facet | Gavin J.B. Elias Jürgen Germann Alexandre Boutet Michelle E. Beyn Peter Giacobbe Ha Neul Song Ki Sueng Choi Helen S. Mayberg Sidney H. Kennedy Andres M. Lozano |
| author_sort | Gavin J.B. Elias |
| collection | DOAJ |
| description | Background: Deep brain stimulation of the subcallosal cingulate area (SCC-DBS) is a promising neuromodulatory therapy for treatment-resistant depression (TRD). Biomarkers of optimal target engagement are needed to guide surgical targeting and stimulation parameter selection and to reduce variance in clinical outcome. Objective/Hypothesis: We aimed to characterize the relationship between stimulation location, white matter tract engagement, and clinical outcome in a large (n = 60) TRD cohort treated with SCC-DBS. A smaller cohort (n = 22) of SCC-DBS patients with differing primary indications (bipolar disorder/anorexia nervosa) was utilized as an out-of-sample validation cohort. Methods: Volumes of tissue activated (VTAs) were constructed in standard space using high-resolution structural MRI and individual stimulation parameters. VTA-based probabilistic stimulation maps (PSMs) were generated to elucidate voxelwise spatial patterns of efficacious stimulation. A whole-brain tractogram derived from Human Connectome Project diffusion-weighted MRI data was seeded with VTA pairs, and white matter streamlines whose overlap with VTAs related to outcome (‘discriminative’ streamlines; Puncorrected < 0.05) were identified using t-tests. Linear modelling was used to interrogate the potential clinical relevance of VTA overlap with specific structures. Results: PSMs varied by hemisphere: high-value left-sided voxels were located more anterosuperiorly and squarely in the lateral white matter, while the equivalent right-sided voxels fell more posteroinferiorly and involved a greater proportion of grey matter. Positive discriminative streamlines localized to the bilateral (but primarily left) cingulum bundle, forceps minor/rostrum of corpus callosum, and bilateral uncinate fasciculus. Conversely, negative discriminative streamlines mostly belonged to the right cingulum bundle and bilateral uncinate fasciculus. The best performing linear model, which utilized information about VTA volume overlap with each of the positive discriminative streamline bundles as well as the negative discriminative elements of the right cingulum bundle, explained significant variance in clinical improvement in the primary TRD cohort (R = 0.46, P < 0.001) and survived repeated 10-fold cross-validation (R = 0.50, P = 0.040). This model was also able to predict outcome in the out-of-sample validation cohort (R = 0.43, P = 0.047). Conclusion(s): These findings reinforce prior indications of the importance of white matter engagement to SCC-DBS treatment success while providing new insights that could inform surgical targeting and stimulation parameter selection decisions. |
| first_indexed | 2024-03-11T14:36:11Z |
| format | Article |
| id | doaj.art-df549690733a4725af31a5ab93aba936 |
| institution | Directory Open Access Journal |
| issn | 1935-861X |
| language | English |
| last_indexed | 2024-03-11T14:36:11Z |
| publishDate | 2023-09-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Brain Stimulation |
| spelling | doaj.art-df549690733a4725af31a5ab93aba9362023-10-31T04:09:00ZengElsevierBrain Stimulation1935-861X2023-09-0116512591272Local neuroanatomical and tract-based proxies of optimal subcallosal cingulate deep brain stimulationGavin J.B. Elias0Jürgen Germann1Alexandre Boutet2Michelle E. Beyn3Peter Giacobbe4Ha Neul Song5Ki Sueng Choi6Helen S. Mayberg7Sidney H. Kennedy8Andres M. Lozano9Division of Neurosurgery, Department of Surgery, University Health Network and University of Toronto, Toronto, M5T 2S8, Canada; Krembil Research Institute, University of Toronto, Toronto, M5T 0S8, CanadaDivision of Neurosurgery, Department of Surgery, University Health Network and University of Toronto, Toronto, M5T 2S8, Canada; Krembil Research Institute, University of Toronto, Toronto, M5T 0S8, CanadaDivision of Neurosurgery, Department of Surgery, University Health Network and University of Toronto, Toronto, M5T 2S8, Canada; Krembil Research Institute, University of Toronto, Toronto, M5T 0S8, Canada; Joint Department of Medical Imaging, University of Toronto, Toronto, M5T 1W7, CanadaDivision of Neurosurgery, Department of Surgery, University Health Network and University of Toronto, Toronto, M5T 2S8, CanadaDepartment of Psychiatry, Sunnybrook Health Sciences Centre and University of Toronto, Toronto, M4N 3M5, CanadaNash Family Center for Advanced Circuit Therapeutics, Mount Sinai West, Icahn School of Medicine at Mount Sinai, New York, NY, 10019, USANash Family Center for Advanced Circuit Therapeutics, Mount Sinai West, Icahn School of Medicine at Mount Sinai, New York, NY, 10019, USA; Department of Radiology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USANash Family Center for Advanced Circuit Therapeutics, Mount Sinai West, Icahn School of Medicine at Mount Sinai, New York, NY, 10019, USA; Departments of Neurology and Neurosurgery, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USAKrembil Research Institute, University of Toronto, Toronto, M5T 0S8, Canada; ASR Suicide and Depression Studies Unit, St. Michael's Hospital, University of Toronto, M5B 1M8, Canada; Department of Psychiatry, University Health Network and University of Toronto, Toronto, M5T 2S8, CanadaDivision of Neurosurgery, Department of Surgery, University Health Network and University of Toronto, Toronto, M5T 2S8, Canada; Krembil Research Institute, University of Toronto, Toronto, M5T 0S8, Canada; Corresponding author. 399 Bathurst St., WW 4-431, Toronto Western Hospital, Toronto, ON, M5T 2S8, Canada.Background: Deep brain stimulation of the subcallosal cingulate area (SCC-DBS) is a promising neuromodulatory therapy for treatment-resistant depression (TRD). Biomarkers of optimal target engagement are needed to guide surgical targeting and stimulation parameter selection and to reduce variance in clinical outcome. Objective/Hypothesis: We aimed to characterize the relationship between stimulation location, white matter tract engagement, and clinical outcome in a large (n = 60) TRD cohort treated with SCC-DBS. A smaller cohort (n = 22) of SCC-DBS patients with differing primary indications (bipolar disorder/anorexia nervosa) was utilized as an out-of-sample validation cohort. Methods: Volumes of tissue activated (VTAs) were constructed in standard space using high-resolution structural MRI and individual stimulation parameters. VTA-based probabilistic stimulation maps (PSMs) were generated to elucidate voxelwise spatial patterns of efficacious stimulation. A whole-brain tractogram derived from Human Connectome Project diffusion-weighted MRI data was seeded with VTA pairs, and white matter streamlines whose overlap with VTAs related to outcome (‘discriminative’ streamlines; Puncorrected < 0.05) were identified using t-tests. Linear modelling was used to interrogate the potential clinical relevance of VTA overlap with specific structures. Results: PSMs varied by hemisphere: high-value left-sided voxels were located more anterosuperiorly and squarely in the lateral white matter, while the equivalent right-sided voxels fell more posteroinferiorly and involved a greater proportion of grey matter. Positive discriminative streamlines localized to the bilateral (but primarily left) cingulum bundle, forceps minor/rostrum of corpus callosum, and bilateral uncinate fasciculus. Conversely, negative discriminative streamlines mostly belonged to the right cingulum bundle and bilateral uncinate fasciculus. The best performing linear model, which utilized information about VTA volume overlap with each of the positive discriminative streamline bundles as well as the negative discriminative elements of the right cingulum bundle, explained significant variance in clinical improvement in the primary TRD cohort (R = 0.46, P < 0.001) and survived repeated 10-fold cross-validation (R = 0.50, P = 0.040). This model was also able to predict outcome in the out-of-sample validation cohort (R = 0.43, P = 0.047). Conclusion(s): These findings reinforce prior indications of the importance of white matter engagement to SCC-DBS treatment success while providing new insights that could inform surgical targeting and stimulation parameter selection decisions.http://www.sciencedirect.com/science/article/pii/S1935861X23018909 |
| spellingShingle | Gavin J.B. Elias Jürgen Germann Alexandre Boutet Michelle E. Beyn Peter Giacobbe Ha Neul Song Ki Sueng Choi Helen S. Mayberg Sidney H. Kennedy Andres M. Lozano Local neuroanatomical and tract-based proxies of optimal subcallosal cingulate deep brain stimulation Brain Stimulation |
| title | Local neuroanatomical and tract-based proxies of optimal subcallosal cingulate deep brain stimulation |
| title_full | Local neuroanatomical and tract-based proxies of optimal subcallosal cingulate deep brain stimulation |
| title_fullStr | Local neuroanatomical and tract-based proxies of optimal subcallosal cingulate deep brain stimulation |
| title_full_unstemmed | Local neuroanatomical and tract-based proxies of optimal subcallosal cingulate deep brain stimulation |
| title_short | Local neuroanatomical and tract-based proxies of optimal subcallosal cingulate deep brain stimulation |
| title_sort | local neuroanatomical and tract based proxies of optimal subcallosal cingulate deep brain stimulation |
| url | http://www.sciencedirect.com/science/article/pii/S1935861X23018909 |
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