A connectomic analysis of deep brain stimulation for treatment-resistant depression

Zhoule Zhu; Elizabeth Hubbard; Xinxia Guo; Daniel A.N. Barbosa; Abdul Malik Popal; Chengwei Cai; Hongjie Jiang; Zhe Zheng; Jingquan Lin; Wei Gao; Jianmin Zhang; Katrina Bartas; Desiree Macchia; Pieter Derdeyn; Casey H. Halpern; Helen S. Mayberg; Kevin T. Beier; Junming Zhu; Hemmings Wu

doi:10.1016/j.brs.2021.08.010

A connectomic analysis of deep brain stimulation for treatment-resistant depression

Zhoule Zhu, Elizabeth Hubbard, Xinxia Guo, Daniel A.N. Barbosa, Abdul Malik Popal, Chengwei Cai, Hongjie Jiang, Zhe Zheng, Jingquan Lin, Wei Gao, Jianmin Zhang, Katrina Bartas, Desiree Macchia, Pieter Derdeyn, Casey H. Halpern, Helen S. Mayberg, Kevin T. Beier, Junming Zhu, Hemmings Wu

Research output: Contribution to journal › Article › peer-review

26 Scopus citations

Abstract

Objective: Deep brain stimulation (DBS) has been used as a treatment of last resort for treatment-resistant depression (TRD) for more than a decade. Many DBS targets have been proposed and tested clinically, but the underlying circuit mechanisms remain unclear. Uncovering white matter tracts (WMT) activated by DBS targets may provide crucial information about the circuit substrates mediating DBS efficacy in ameliorating TRD. Methods: We performed probabilistic tractography using diffusion magnetic resonance imaging datas from 100 healthy volunteers in Human Connectome Project datasets to analyze the structural connectivity patterns of stimulation targeting currently-used DBS target for TRD. We generated mean and binary fiber distribution maps and calculated the numbers of WMT streamlines in the dataset. Results: Probabilistic tracking results revealed that activation of distinct DBS targets demonstrated modulation of overlapping but considerably distinct pathways. DBS targets were categorized into 4 groups: Cortical, Striatal, Thalamic, and Medial Forebrain Bundle according to their main modulated WMT and brain areas. Our data also revealed that Brodmann area 10 and amygdala are hub structures that are associated with all DBS targets. Conclusions: Our results together suggest that the distinct mechanism of DBS targets implies individualized target selection and formulation in the future of DBS treatment for TRD. The modulation of Brodmann area 10 and amygdala may be critical for the efficacy of DBS-mediated treatment of TRD.

Original language	English
Pages (from-to)	1226-1233
Number of pages	8
Journal	Brain Stimulation
Volume	14
Issue number	5
DOIs	https://doi.org/10.1016/j.brs.2021.08.010
State	Published - Sep 2021

Keywords

Amygdala
Brodmann area 10
Deep brain stimulation
Tractography
Treatment-resistant depression

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10.1016/j.brs.2021.08.010

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Zhu, Z., Hubbard, E., Guo, X., Barbosa, D. A. N., Popal, A. M., Cai, C., Jiang, H., Zheng, Z., Lin, J., Gao, W., Zhang, J., Bartas, K., Macchia, D., Derdeyn, P., Halpern, C. H., Mayberg, H. S., Beier, K. T., Zhu, J., & Wu, H. (2021). A connectomic analysis of deep brain stimulation for treatment-resistant depression. Brain Stimulation, 14(5), 1226-1233. https://doi.org/10.1016/j.brs.2021.08.010

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title = "A connectomic analysis of deep brain stimulation for treatment-resistant depression",

abstract = "Objective: Deep brain stimulation (DBS) has been used as a treatment of last resort for treatment-resistant depression (TRD) for more than a decade. Many DBS targets have been proposed and tested clinically, but the underlying circuit mechanisms remain unclear. Uncovering white matter tracts (WMT) activated by DBS targets may provide crucial information about the circuit substrates mediating DBS efficacy in ameliorating TRD. Methods: We performed probabilistic tractography using diffusion magnetic resonance imaging datas from 100 healthy volunteers in Human Connectome Project datasets to analyze the structural connectivity patterns of stimulation targeting currently-used DBS target for TRD. We generated mean and binary fiber distribution maps and calculated the numbers of WMT streamlines in the dataset. Results: Probabilistic tracking results revealed that activation of distinct DBS targets demonstrated modulation of overlapping but considerably distinct pathways. DBS targets were categorized into 4 groups: Cortical, Striatal, Thalamic, and Medial Forebrain Bundle according to their main modulated WMT and brain areas. Our data also revealed that Brodmann area 10 and amygdala are hub structures that are associated with all DBS targets. Conclusions: Our results together suggest that the distinct mechanism of DBS targets implies individualized target selection and formulation in the future of DBS treatment for TRD. The modulation of Brodmann area 10 and amygdala may be critical for the efficacy of DBS-mediated treatment of TRD.",

keywords = "Amygdala, Brodmann area 10, Deep brain stimulation, Tractography, Treatment-resistant depression",

author = "Zhoule Zhu and Elizabeth Hubbard and Xinxia Guo and Barbosa, {Daniel A.N.} and Popal, {Abdul Malik} and Chengwei Cai and Hongjie Jiang and Zhe Zheng and Jingquan Lin and Wei Gao and Jianmin Zhang and Katrina Bartas and Desiree Macchia and Pieter Derdeyn and Halpern, {Casey H.} and Mayberg, {Helen S.} and Beier, {Kevin T.} and Junming Zhu and Hemmings Wu",

note = "Publisher Copyright: {\textcopyright} 2021 The Authors",

year = "2021",

month = sep,

doi = "10.1016/j.brs.2021.08.010",

language = "English",

volume = "14",

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Zhu, Z, Hubbard, E, Guo, X, Barbosa, DAN, Popal, AM, Cai, C, Jiang, H, Zheng, Z, Lin, J, Gao, W, Zhang, J, Bartas, K, Macchia, D, Derdeyn, P, Halpern, CH, Mayberg, HS, Beier, KT, Zhu, J & Wu, H 2021, 'A connectomic analysis of deep brain stimulation for treatment-resistant depression', Brain Stimulation, vol. 14, no. 5, pp. 1226-1233. https://doi.org/10.1016/j.brs.2021.08.010

TY - JOUR

T1 - A connectomic analysis of deep brain stimulation for treatment-resistant depression

AU - Zhu, Zhoule

AU - Hubbard, Elizabeth

AU - Guo, Xinxia

AU - Barbosa, Daniel A.N.

AU - Popal, Abdul Malik

AU - Cai, Chengwei

AU - Jiang, Hongjie

AU - Zheng, Zhe

AU - Lin, Jingquan

AU - Gao, Wei

AU - Zhang, Jianmin

AU - Bartas, Katrina

AU - Macchia, Desiree

AU - Derdeyn, Pieter

AU - Halpern, Casey H.

AU - Mayberg, Helen S.

AU - Beier, Kevin T.

AU - Zhu, Junming

AU - Wu, Hemmings

PY - 2021/9

Y1 - 2021/9

N2 - Objective: Deep brain stimulation (DBS) has been used as a treatment of last resort for treatment-resistant depression (TRD) for more than a decade. Many DBS targets have been proposed and tested clinically, but the underlying circuit mechanisms remain unclear. Uncovering white matter tracts (WMT) activated by DBS targets may provide crucial information about the circuit substrates mediating DBS efficacy in ameliorating TRD. Methods: We performed probabilistic tractography using diffusion magnetic resonance imaging datas from 100 healthy volunteers in Human Connectome Project datasets to analyze the structural connectivity patterns of stimulation targeting currently-used DBS target for TRD. We generated mean and binary fiber distribution maps and calculated the numbers of WMT streamlines in the dataset. Results: Probabilistic tracking results revealed that activation of distinct DBS targets demonstrated modulation of overlapping but considerably distinct pathways. DBS targets were categorized into 4 groups: Cortical, Striatal, Thalamic, and Medial Forebrain Bundle according to their main modulated WMT and brain areas. Our data also revealed that Brodmann area 10 and amygdala are hub structures that are associated with all DBS targets. Conclusions: Our results together suggest that the distinct mechanism of DBS targets implies individualized target selection and formulation in the future of DBS treatment for TRD. The modulation of Brodmann area 10 and amygdala may be critical for the efficacy of DBS-mediated treatment of TRD.

AB - Objective: Deep brain stimulation (DBS) has been used as a treatment of last resort for treatment-resistant depression (TRD) for more than a decade. Many DBS targets have been proposed and tested clinically, but the underlying circuit mechanisms remain unclear. Uncovering white matter tracts (WMT) activated by DBS targets may provide crucial information about the circuit substrates mediating DBS efficacy in ameliorating TRD. Methods: We performed probabilistic tractography using diffusion magnetic resonance imaging datas from 100 healthy volunteers in Human Connectome Project datasets to analyze the structural connectivity patterns of stimulation targeting currently-used DBS target for TRD. We generated mean and binary fiber distribution maps and calculated the numbers of WMT streamlines in the dataset. Results: Probabilistic tracking results revealed that activation of distinct DBS targets demonstrated modulation of overlapping but considerably distinct pathways. DBS targets were categorized into 4 groups: Cortical, Striatal, Thalamic, and Medial Forebrain Bundle according to their main modulated WMT and brain areas. Our data also revealed that Brodmann area 10 and amygdala are hub structures that are associated with all DBS targets. Conclusions: Our results together suggest that the distinct mechanism of DBS targets implies individualized target selection and formulation in the future of DBS treatment for TRD. The modulation of Brodmann area 10 and amygdala may be critical for the efficacy of DBS-mediated treatment of TRD.

KW - Amygdala

KW - Brodmann area 10

KW - Deep brain stimulation

KW - Tractography

KW - Treatment-resistant depression

UR - http://www.scopus.com/inward/record.url?scp=85112857286&partnerID=8YFLogxK

U2 - 10.1016/j.brs.2021.08.010

DO - 10.1016/j.brs.2021.08.010

M3 - Article

C2 - 34400379

AN - SCOPUS:85112857286

SN - 1935-861X

VL - 14

SP - 1226

EP - 1233

JO - Brain Stimulation

JF - Brain Stimulation

IS - 5

ER -

A connectomic analysis of deep brain stimulation for treatment-resistant depression

Abstract

Keywords

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