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A Unified Functional Network Target for Deep Brain Stimulation in Obsessive-Compulsive Disorder
Multiple deep brain stimulation (DBS) targets have been proposed for treating intractable obsessive-compulsive disorder (OCD). Here, we investigated whether stimulation effects of different target sites would be mediated by one common or several segregated functional brain networks. First, seeding f...
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| Published in: | Biological psychiatry (1969) 2021-11, Vol.90 (10), p.701-713 |
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| cites | cdi_FETCH-LOGICAL-c470t-2994e4750e644882dcd8213a3ac88caf231f041cfee3bb92ce3c0c67d15bba823 |
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| container_title | Biological psychiatry (1969) |
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| creator | Li, Ningfei Hollunder, Barbara Baldermann, Juan Carlos Kibleur, Astrid Treu, Svenja Akram, Harith Al-Fatly, Bassam Strange, Bryan A. Barcia, Juan A. Zrinzo, Ludvic Joyce, Eileen M. Chabardes, Stephan Visser-Vandewalle, Veerle Polosan, Mircea Kuhn, Jens Kühn, Andrea A. Horn, Andreas |
| description | Multiple deep brain stimulation (DBS) targets have been proposed for treating intractable obsessive-compulsive disorder (OCD). Here, we investigated whether stimulation effects of different target sites would be mediated by one common or several segregated functional brain networks.
First, seeding from active electrodes of 4 OCD patient cohorts (N = 50) receiving DBS to anterior limb of the internal capsule or subthalamic nucleus zones, optimal functional connectivity profiles for maximal Yale-Brown Obsessive Compulsive Scale improvements were calculated and cross-validated in leave-one-cohort-out and leave-one-patient-out designs. Second, we derived optimal target-specific connectivity patterns to determine brain regions mutually predictive of clinical outcome for both targets and others predictive for either target alone. Functional connectivity was defined using resting-state functional magnetic resonance imaging data acquired in 1000 healthy participants.
While optimal functional connectivity profiles showed both commonalities and differences between target sites, robust cross-predictions of clinical improvements across OCD cohorts and targets suggested a shared network. Connectivity to the anterior cingulate cortex, insula, and precuneus, among other regions, was predictive regardless of stimulation target. Regions with maximal connectivity to these commonly predictive areas included the insula, superior frontal gyrus, anterior cingulate cortex, and anterior thalamus, as well as the original stereotactic targets.
Pinpointing the network modulated by DBS for OCD from different target sites identified a set of brain regions to which DBS electrodes associated with optimal outcomes were functionally connected—regardless of target choice. On these grounds, we establish potential brain areas that could prospectively inform additional or alternative neuromodulation targets for obsessive-compulsive disorder. |
| doi_str_mv | 10.1016/j.biopsych.2021.04.006 |
| format | article |
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First, seeding from active electrodes of 4 OCD patient cohorts (N = 50) receiving DBS to anterior limb of the internal capsule or subthalamic nucleus zones, optimal functional connectivity profiles for maximal Yale-Brown Obsessive Compulsive Scale improvements were calculated and cross-validated in leave-one-cohort-out and leave-one-patient-out designs. Second, we derived optimal target-specific connectivity patterns to determine brain regions mutually predictive of clinical outcome for both targets and others predictive for either target alone. Functional connectivity was defined using resting-state functional magnetic resonance imaging data acquired in 1000 healthy participants.
While optimal functional connectivity profiles showed both commonalities and differences between target sites, robust cross-predictions of clinical improvements across OCD cohorts and targets suggested a shared network. Connectivity to the anterior cingulate cortex, insula, and precuneus, among other regions, was predictive regardless of stimulation target. Regions with maximal connectivity to these commonly predictive areas included the insula, superior frontal gyrus, anterior cingulate cortex, and anterior thalamus, as well as the original stereotactic targets.
Pinpointing the network modulated by DBS for OCD from different target sites identified a set of brain regions to which DBS electrodes associated with optimal outcomes were functionally connected—regardless of target choice. On these grounds, we establish potential brain areas that could prospectively inform additional or alternative neuromodulation targets for obsessive-compulsive disorder.</description><identifier>ISSN: 0006-3223</identifier><identifier>EISSN: 1873-2402</identifier><identifier>DOI: 10.1016/j.biopsych.2021.04.006</identifier><identifier>PMID: 34134839</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>ALIC ; Anterior limb of the internal capsule ; Connectome ; DBS ; Deep Brain Stimulation ; Functional connectivity ; Humans ; Internal Capsule - diagnostic imaging ; Magnetic Resonance Imaging ; Obsessive-compulsive disorder ; Obsessive-Compulsive Disorder - diagnostic imaging ; Obsessive-Compulsive Disorder - therapy ; OCD ; STN ; Subthalamic Nucleus</subject><ispartof>Biological psychiatry (1969), 2021-11, Vol.90 (10), p.701-713</ispartof><rights>2021 Society of Biological Psychiatry</rights><rights>Copyright © 2021 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c470t-2994e4750e644882dcd8213a3ac88caf231f041cfee3bb92ce3c0c67d15bba823</citedby><cites>FETCH-LOGICAL-c470t-2994e4750e644882dcd8213a3ac88caf231f041cfee3bb92ce3c0c67d15bba823</cites><orcidid>0000-0002-0695-6025 ; 0000-0003-0067-6177 ; 0000-0001-6476-4091 ; 0000-0002-4719-5293 ; 0000-0003-3315-3591 ; 0000-0003-0469-2844 ; 0000-0001-5851-9268 ; 0000-0003-0104-6927</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,786,790,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34134839$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Li, Ningfei</creatorcontrib><creatorcontrib>Hollunder, Barbara</creatorcontrib><creatorcontrib>Baldermann, Juan Carlos</creatorcontrib><creatorcontrib>Kibleur, Astrid</creatorcontrib><creatorcontrib>Treu, Svenja</creatorcontrib><creatorcontrib>Akram, Harith</creatorcontrib><creatorcontrib>Al-Fatly, Bassam</creatorcontrib><creatorcontrib>Strange, Bryan A.</creatorcontrib><creatorcontrib>Barcia, Juan A.</creatorcontrib><creatorcontrib>Zrinzo, Ludvic</creatorcontrib><creatorcontrib>Joyce, Eileen M.</creatorcontrib><creatorcontrib>Chabardes, Stephan</creatorcontrib><creatorcontrib>Visser-Vandewalle, Veerle</creatorcontrib><creatorcontrib>Polosan, Mircea</creatorcontrib><creatorcontrib>Kuhn, Jens</creatorcontrib><creatorcontrib>Kühn, Andrea A.</creatorcontrib><creatorcontrib>Horn, Andreas</creatorcontrib><title>A Unified Functional Network Target for Deep Brain Stimulation in Obsessive-Compulsive Disorder</title><title>Biological psychiatry (1969)</title><addtitle>Biol Psychiatry</addtitle><description>Multiple deep brain stimulation (DBS) targets have been proposed for treating intractable obsessive-compulsive disorder (OCD). Here, we investigated whether stimulation effects of different target sites would be mediated by one common or several segregated functional brain networks.
First, seeding from active electrodes of 4 OCD patient cohorts (N = 50) receiving DBS to anterior limb of the internal capsule or subthalamic nucleus zones, optimal functional connectivity profiles for maximal Yale-Brown Obsessive Compulsive Scale improvements were calculated and cross-validated in leave-one-cohort-out and leave-one-patient-out designs. Second, we derived optimal target-specific connectivity patterns to determine brain regions mutually predictive of clinical outcome for both targets and others predictive for either target alone. Functional connectivity was defined using resting-state functional magnetic resonance imaging data acquired in 1000 healthy participants.
While optimal functional connectivity profiles showed both commonalities and differences between target sites, robust cross-predictions of clinical improvements across OCD cohorts and targets suggested a shared network. Connectivity to the anterior cingulate cortex, insula, and precuneus, among other regions, was predictive regardless of stimulation target. Regions with maximal connectivity to these commonly predictive areas included the insula, superior frontal gyrus, anterior cingulate cortex, and anterior thalamus, as well as the original stereotactic targets.
Pinpointing the network modulated by DBS for OCD from different target sites identified a set of brain regions to which DBS electrodes associated with optimal outcomes were functionally connected—regardless of target choice. On these grounds, we establish potential brain areas that could prospectively inform additional or alternative neuromodulation targets for obsessive-compulsive disorder.</description><subject>ALIC</subject><subject>Anterior limb of the internal capsule</subject><subject>Connectome</subject><subject>DBS</subject><subject>Deep Brain Stimulation</subject><subject>Functional connectivity</subject><subject>Humans</subject><subject>Internal Capsule - diagnostic imaging</subject><subject>Magnetic Resonance Imaging</subject><subject>Obsessive-compulsive disorder</subject><subject>Obsessive-Compulsive Disorder - diagnostic imaging</subject><subject>Obsessive-Compulsive Disorder - therapy</subject><subject>OCD</subject><subject>STN</subject><subject>Subthalamic Nucleus</subject><issn>0006-3223</issn><issn>1873-2402</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNqFkMlOwzAQQC0EomX5hcpHLgnemjg3SssmVXCAni3HmYBLEgc7Kerfk6qUK6dZ9GZG8xCaUBJTQpPrdZxb14at-YgZYTQmIiYkOUJjKlMeMUHYMRqToRVxxvgInYWwHsqUMXqKRlxQLiTPxkjN8KqxpYUC3_eN6axrdIWfoft2_hO_af8OHS6dxwuAFt96bRv82tm6r_SOxUP5kgcIwW4gmru67atdihc2OF-Av0Anpa4CXP7Gc7S6v3ubP0bLl4en-WwZGZGSLmJZJkCkUwKJEFKywhSSUa65NlIaXTJOSyKoKQF4nmfMADfEJGlBp3muJePn6Gq_t_Xuq4fQqdoGA1WlG3B9UGwqGJ_KVGYDmuxR410IHkrVeltrv1WUqJ1ctVYHuWonVxGhBpPD4OT3Rp_XUPyNHWwOwM0egOHTjQWvgrHQGCisB9Opwtn_bvwAFd-PWQ</recordid><startdate>20211115</startdate><enddate>20211115</enddate><creator>Li, Ningfei</creator><creator>Hollunder, Barbara</creator><creator>Baldermann, Juan Carlos</creator><creator>Kibleur, Astrid</creator><creator>Treu, Svenja</creator><creator>Akram, Harith</creator><creator>Al-Fatly, Bassam</creator><creator>Strange, Bryan A.</creator><creator>Barcia, Juan A.</creator><creator>Zrinzo, Ludvic</creator><creator>Joyce, Eileen M.</creator><creator>Chabardes, Stephan</creator><creator>Visser-Vandewalle, Veerle</creator><creator>Polosan, Mircea</creator><creator>Kuhn, Jens</creator><creator>Kühn, Andrea A.</creator><creator>Horn, Andreas</creator><general>Elsevier Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-0695-6025</orcidid><orcidid>https://orcid.org/0000-0003-0067-6177</orcidid><orcidid>https://orcid.org/0000-0001-6476-4091</orcidid><orcidid>https://orcid.org/0000-0002-4719-5293</orcidid><orcidid>https://orcid.org/0000-0003-3315-3591</orcidid><orcidid>https://orcid.org/0000-0003-0469-2844</orcidid><orcidid>https://orcid.org/0000-0001-5851-9268</orcidid><orcidid>https://orcid.org/0000-0003-0104-6927</orcidid></search><sort><creationdate>20211115</creationdate><title>A Unified Functional Network Target for Deep Brain Stimulation in Obsessive-Compulsive Disorder</title><author>Li, Ningfei ; Hollunder, Barbara ; Baldermann, Juan Carlos ; Kibleur, Astrid ; Treu, Svenja ; Akram, Harith ; Al-Fatly, Bassam ; Strange, Bryan A. ; Barcia, Juan A. ; Zrinzo, Ludvic ; Joyce, Eileen M. ; Chabardes, Stephan ; Visser-Vandewalle, Veerle ; Polosan, Mircea ; Kuhn, Jens ; Kühn, Andrea A. ; Horn, Andreas</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c470t-2994e4750e644882dcd8213a3ac88caf231f041cfee3bb92ce3c0c67d15bba823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>ALIC</topic><topic>Anterior limb of the internal capsule</topic><topic>Connectome</topic><topic>DBS</topic><topic>Deep Brain Stimulation</topic><topic>Functional connectivity</topic><topic>Humans</topic><topic>Internal Capsule - diagnostic imaging</topic><topic>Magnetic Resonance Imaging</topic><topic>Obsessive-compulsive disorder</topic><topic>Obsessive-Compulsive Disorder - diagnostic imaging</topic><topic>Obsessive-Compulsive Disorder - therapy</topic><topic>OCD</topic><topic>STN</topic><topic>Subthalamic Nucleus</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Ningfei</creatorcontrib><creatorcontrib>Hollunder, Barbara</creatorcontrib><creatorcontrib>Baldermann, Juan Carlos</creatorcontrib><creatorcontrib>Kibleur, Astrid</creatorcontrib><creatorcontrib>Treu, Svenja</creatorcontrib><creatorcontrib>Akram, Harith</creatorcontrib><creatorcontrib>Al-Fatly, Bassam</creatorcontrib><creatorcontrib>Strange, Bryan A.</creatorcontrib><creatorcontrib>Barcia, Juan A.</creatorcontrib><creatorcontrib>Zrinzo, Ludvic</creatorcontrib><creatorcontrib>Joyce, Eileen M.</creatorcontrib><creatorcontrib>Chabardes, Stephan</creatorcontrib><creatorcontrib>Visser-Vandewalle, Veerle</creatorcontrib><creatorcontrib>Polosan, Mircea</creatorcontrib><creatorcontrib>Kuhn, Jens</creatorcontrib><creatorcontrib>Kühn, Andrea A.</creatorcontrib><creatorcontrib>Horn, Andreas</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Biological psychiatry (1969)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Ningfei</au><au>Hollunder, Barbara</au><au>Baldermann, Juan Carlos</au><au>Kibleur, Astrid</au><au>Treu, Svenja</au><au>Akram, Harith</au><au>Al-Fatly, Bassam</au><au>Strange, Bryan A.</au><au>Barcia, Juan A.</au><au>Zrinzo, Ludvic</au><au>Joyce, Eileen M.</au><au>Chabardes, Stephan</au><au>Visser-Vandewalle, Veerle</au><au>Polosan, Mircea</au><au>Kuhn, Jens</au><au>Kühn, Andrea A.</au><au>Horn, Andreas</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Unified Functional Network Target for Deep Brain Stimulation in Obsessive-Compulsive Disorder</atitle><jtitle>Biological psychiatry (1969)</jtitle><addtitle>Biol Psychiatry</addtitle><date>2021-11-15</date><risdate>2021</risdate><volume>90</volume><issue>10</issue><spage>701</spage><epage>713</epage><pages>701-713</pages><issn>0006-3223</issn><eissn>1873-2402</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Multiple deep brain stimulation (DBS) targets have been proposed for treating intractable obsessive-compulsive disorder (OCD). Here, we investigated whether stimulation effects of different target sites would be mediated by one common or several segregated functional brain networks.
First, seeding from active electrodes of 4 OCD patient cohorts (N = 50) receiving DBS to anterior limb of the internal capsule or subthalamic nucleus zones, optimal functional connectivity profiles for maximal Yale-Brown Obsessive Compulsive Scale improvements were calculated and cross-validated in leave-one-cohort-out and leave-one-patient-out designs. Second, we derived optimal target-specific connectivity patterns to determine brain regions mutually predictive of clinical outcome for both targets and others predictive for either target alone. Functional connectivity was defined using resting-state functional magnetic resonance imaging data acquired in 1000 healthy participants.
While optimal functional connectivity profiles showed both commonalities and differences between target sites, robust cross-predictions of clinical improvements across OCD cohorts and targets suggested a shared network. Connectivity to the anterior cingulate cortex, insula, and precuneus, among other regions, was predictive regardless of stimulation target. Regions with maximal connectivity to these commonly predictive areas included the insula, superior frontal gyrus, anterior cingulate cortex, and anterior thalamus, as well as the original stereotactic targets.
Pinpointing the network modulated by DBS for OCD from different target sites identified a set of brain regions to which DBS electrodes associated with optimal outcomes were functionally connected—regardless of target choice. On these grounds, we establish potential brain areas that could prospectively inform additional or alternative neuromodulation targets for obsessive-compulsive disorder.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>34134839</pmid><doi>10.1016/j.biopsych.2021.04.006</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-0695-6025</orcidid><orcidid>https://orcid.org/0000-0003-0067-6177</orcidid><orcidid>https://orcid.org/0000-0001-6476-4091</orcidid><orcidid>https://orcid.org/0000-0002-4719-5293</orcidid><orcidid>https://orcid.org/0000-0003-3315-3591</orcidid><orcidid>https://orcid.org/0000-0003-0469-2844</orcidid><orcidid>https://orcid.org/0000-0001-5851-9268</orcidid><orcidid>https://orcid.org/0000-0003-0104-6927</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Biological psychiatry (1969), 2021-11, Vol.90 (10), p.701-713 |
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| language | eng |
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| subjects | ALIC Anterior limb of the internal capsule Connectome DBS Deep Brain Stimulation Functional connectivity Humans Internal Capsule - diagnostic imaging Magnetic Resonance Imaging Obsessive-compulsive disorder Obsessive-Compulsive Disorder - diagnostic imaging Obsessive-Compulsive Disorder - therapy OCD STN Subthalamic Nucleus |
| title | A Unified Functional Network Target for Deep Brain Stimulation in Obsessive-Compulsive Disorder |
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