Left Prefrontal Connectivity Links Subthalamic Stimulation with Depressive Symptoms
Objective Subthalamic nucleus deep brain stimulation (STN‐DBS) in Parkinson's disease (PD) not only stimulates focal target structures but also affects distributed brain networks. The impact this network modulation has on non‐motor DBS effects is not well‐characterized. By focusing on the affec...
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| Veröffentlicht in: | Annals of neurology 2020-06, Vol.87 (6), p.962-975 |
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| container_title | Annals of neurology |
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| creator | Irmen, Friederike Horn, Andreas Mosley, Philip Perry, Alistair Petry‐Schmelzer, Jan Niklas Dafsari, Haidar S. Barbe, Michael Visser‐Vandewalle, Veerle Schneider, Gerd‐Helge Li, Ningfei Kübler, Dorothee Wenzel, Gregor Kühn, Andrea A. |
| description | Objective
Subthalamic nucleus deep brain stimulation (STN‐DBS) in Parkinson's disease (PD) not only stimulates focal target structures but also affects distributed brain networks. The impact this network modulation has on non‐motor DBS effects is not well‐characterized. By focusing on the affective domain, we systematically investigate the impact of electrode placement and associated structural connectivity on changes in depressive symptoms following STN‐DBS, which have been reported to improve, worsen, or remain unchanged.
Methods
Depressive symptoms before and after STN‐DBS surgery were documented in 116 patients with PD from 3 DBS centers (Berlin, Queensland, and Cologne). Based on individual electrode reconstructions, the volumes of tissue activated (VTAs) were estimated and combined with normative connectome data to identify structural connections passing through VTAs. Berlin and Queensland cohorts formed a training and cross‐validation dataset used to identify structural connectivity explaining change in depressive symptoms. The Cologne data served as the test‐set for which depressive symptom change was predicted.
Results
Structural connectivity was linked to depressive symptom change under STN‐DBS. An optimal connectivity map trained on the Berlin cohort could predict changes in depressive symptoms in Queensland patients and vice versa. Furthermore, the joint training‐set map predicted changes in depressive symptoms in the independent test‐set. Worsening of depressive symptoms was associated with left prefrontal connectivity.
Interpretation
Fibers connecting the electrode with left prefrontal areas were associated with worsening of depressive symptoms. Our results suggest that for the left STN‐DBS lead, placement impacting fibers to left prefrontal areas should be avoided to maximize improvement of depressive symptoms. ANN NEUROL 2020;87:962–975 |
| doi_str_mv | 10.1002/ana.25734 |
| format | Article |
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Subthalamic nucleus deep brain stimulation (STN‐DBS) in Parkinson's disease (PD) not only stimulates focal target structures but also affects distributed brain networks. The impact this network modulation has on non‐motor DBS effects is not well‐characterized. By focusing on the affective domain, we systematically investigate the impact of electrode placement and associated structural connectivity on changes in depressive symptoms following STN‐DBS, which have been reported to improve, worsen, or remain unchanged.
Methods
Depressive symptoms before and after STN‐DBS surgery were documented in 116 patients with PD from 3 DBS centers (Berlin, Queensland, and Cologne). Based on individual electrode reconstructions, the volumes of tissue activated (VTAs) were estimated and combined with normative connectome data to identify structural connections passing through VTAs. Berlin and Queensland cohorts formed a training and cross‐validation dataset used to identify structural connectivity explaining change in depressive symptoms. The Cologne data served as the test‐set for which depressive symptom change was predicted.
Results
Structural connectivity was linked to depressive symptom change under STN‐DBS. An optimal connectivity map trained on the Berlin cohort could predict changes in depressive symptoms in Queensland patients and vice versa. Furthermore, the joint training‐set map predicted changes in depressive symptoms in the independent test‐set. Worsening of depressive symptoms was associated with left prefrontal connectivity.
Interpretation
Fibers connecting the electrode with left prefrontal areas were associated with worsening of depressive symptoms. Our results suggest that for the left STN‐DBS lead, placement impacting fibers to left prefrontal areas should be avoided to maximize improvement of depressive symptoms. ANN NEUROL 2020;87:962–975</description><identifier>ISSN: 0364-5134</identifier><identifier>EISSN: 1531-8249</identifier><identifier>DOI: 10.1002/ana.25734</identifier><identifier>PMID: 32239535</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Brain ; Deep brain stimulation ; Electrical stimuli ; Electrodes ; Fibers ; Mental depression ; Movement disorders ; Neural networks ; Neurodegenerative diseases ; Parkinson's disease ; Placement ; Signs and symptoms ; Solitary tract nucleus ; Stimulation ; Subthalamic nucleus ; Surgery ; Training</subject><ispartof>Annals of neurology, 2020-06, Vol.87 (6), p.962-975</ispartof><rights>2020 The Authors. published by Wiley Periodicals, Inc. on behalf of American Neurological Association.</rights><rights>2020 The Authors. Annals of Neurology published by Wiley Periodicals, Inc. on behalf of American Neurological Association.</rights><rights>2020. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3884-2ca8490bb88350e57d4721e79687b5d723e67752d9994e749f78b7a51bcf1b203</citedby><cites>FETCH-LOGICAL-c3884-2ca8490bb88350e57d4721e79687b5d723e67752d9994e749f78b7a51bcf1b203</cites><orcidid>0000-0002-0794-1538 ; 0000-0002-0695-6025 ; 0000-0001-5574-3790 ; 0000-0003-0749-3840 ; 0000-0003-1721-3419 ; 0000-0003-3315-3591</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fana.25734$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fana.25734$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,777,781,1412,27905,27906,45555,45556</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32239535$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Irmen, Friederike</creatorcontrib><creatorcontrib>Horn, Andreas</creatorcontrib><creatorcontrib>Mosley, Philip</creatorcontrib><creatorcontrib>Perry, Alistair</creatorcontrib><creatorcontrib>Petry‐Schmelzer, Jan Niklas</creatorcontrib><creatorcontrib>Dafsari, Haidar S.</creatorcontrib><creatorcontrib>Barbe, Michael</creatorcontrib><creatorcontrib>Visser‐Vandewalle, Veerle</creatorcontrib><creatorcontrib>Schneider, Gerd‐Helge</creatorcontrib><creatorcontrib>Li, Ningfei</creatorcontrib><creatorcontrib>Kübler, Dorothee</creatorcontrib><creatorcontrib>Wenzel, Gregor</creatorcontrib><creatorcontrib>Kühn, Andrea A.</creatorcontrib><title>Left Prefrontal Connectivity Links Subthalamic Stimulation with Depressive Symptoms</title><title>Annals of neurology</title><addtitle>Ann Neurol</addtitle><description>Objective
Subthalamic nucleus deep brain stimulation (STN‐DBS) in Parkinson's disease (PD) not only stimulates focal target structures but also affects distributed brain networks. The impact this network modulation has on non‐motor DBS effects is not well‐characterized. By focusing on the affective domain, we systematically investigate the impact of electrode placement and associated structural connectivity on changes in depressive symptoms following STN‐DBS, which have been reported to improve, worsen, or remain unchanged.
Methods
Depressive symptoms before and after STN‐DBS surgery were documented in 116 patients with PD from 3 DBS centers (Berlin, Queensland, and Cologne). Based on individual electrode reconstructions, the volumes of tissue activated (VTAs) were estimated and combined with normative connectome data to identify structural connections passing through VTAs. Berlin and Queensland cohorts formed a training and cross‐validation dataset used to identify structural connectivity explaining change in depressive symptoms. The Cologne data served as the test‐set for which depressive symptom change was predicted.
Results
Structural connectivity was linked to depressive symptom change under STN‐DBS. An optimal connectivity map trained on the Berlin cohort could predict changes in depressive symptoms in Queensland patients and vice versa. Furthermore, the joint training‐set map predicted changes in depressive symptoms in the independent test‐set. Worsening of depressive symptoms was associated with left prefrontal connectivity.
Interpretation
Fibers connecting the electrode with left prefrontal areas were associated with worsening of depressive symptoms. Our results suggest that for the left STN‐DBS lead, placement impacting fibers to left prefrontal areas should be avoided to maximize improvement of depressive symptoms. ANN NEUROL 2020;87:962–975</description><subject>Brain</subject><subject>Deep brain stimulation</subject><subject>Electrical stimuli</subject><subject>Electrodes</subject><subject>Fibers</subject><subject>Mental depression</subject><subject>Movement disorders</subject><subject>Neural networks</subject><subject>Neurodegenerative diseases</subject><subject>Parkinson's disease</subject><subject>Placement</subject><subject>Signs and symptoms</subject><subject>Solitary tract nucleus</subject><subject>Stimulation</subject><subject>Subthalamic nucleus</subject><subject>Surgery</subject><subject>Training</subject><issn>0364-5134</issn><issn>1531-8249</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><recordid>eNp10EtLAzEUhuEgiq3VhX9ABtzoYtqT2yRZlnqFokJ1HTLTDE2dS51kWvrvHW11Ibg6m4ePw4vQOYYhBiAjU5kh4YKyA9THnOJYEqYOUR9owmKOKeuhE--XAKASDMeoRwmhilPeR7OpzUP00ti8qatgimhSV5XNglu7sI2mrnr30axNw8IUpnRZNAuubAsTXF1FGxcW0Y1dNdZ7t7bRbFuuQl36U3SUm8Lbs_0doLe729fJQzx9vn-cjKdxRqVkMcmMZArSVErKwXIxZ4JgK1QiRcrnglCbCMHJXCnFrGAqFzIVhuM0y3FKgA7Q1W531dQfrfVBl85ntihMZevWa0IlF6AwJB29_EOXddtU3XeaMOAEMAjeqeudypra-66JXjWuNM1WY9BfpXVXWn-X7uzFfrFNSzv_lT9pOzDagY0r7Pb_JT1-Gu8mPwGGXYZz</recordid><startdate>202006</startdate><enddate>202006</enddate><creator>Irmen, Friederike</creator><creator>Horn, Andreas</creator><creator>Mosley, Philip</creator><creator>Perry, Alistair</creator><creator>Petry‐Schmelzer, Jan Niklas</creator><creator>Dafsari, Haidar S.</creator><creator>Barbe, Michael</creator><creator>Visser‐Vandewalle, Veerle</creator><creator>Schneider, Gerd‐Helge</creator><creator>Li, Ningfei</creator><creator>Kübler, Dorothee</creator><creator>Wenzel, Gregor</creator><creator>Kühn, Andrea A.</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>WIN</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7U7</scope><scope>C1K</scope><scope>K9.</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-0794-1538</orcidid><orcidid>https://orcid.org/0000-0002-0695-6025</orcidid><orcidid>https://orcid.org/0000-0001-5574-3790</orcidid><orcidid>https://orcid.org/0000-0003-0749-3840</orcidid><orcidid>https://orcid.org/0000-0003-1721-3419</orcidid><orcidid>https://orcid.org/0000-0003-3315-3591</orcidid></search><sort><creationdate>202006</creationdate><title>Left Prefrontal Connectivity Links Subthalamic Stimulation with Depressive Symptoms</title><author>Irmen, Friederike ; Horn, Andreas ; Mosley, Philip ; Perry, Alistair ; Petry‐Schmelzer, Jan Niklas ; Dafsari, Haidar S. ; Barbe, Michael ; Visser‐Vandewalle, Veerle ; Schneider, Gerd‐Helge ; Li, Ningfei ; Kübler, Dorothee ; Wenzel, Gregor ; Kühn, Andrea A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3884-2ca8490bb88350e57d4721e79687b5d723e67752d9994e749f78b7a51bcf1b203</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Brain</topic><topic>Deep brain stimulation</topic><topic>Electrical stimuli</topic><topic>Electrodes</topic><topic>Fibers</topic><topic>Mental depression</topic><topic>Movement disorders</topic><topic>Neural networks</topic><topic>Neurodegenerative diseases</topic><topic>Parkinson's disease</topic><topic>Placement</topic><topic>Signs and symptoms</topic><topic>Solitary tract nucleus</topic><topic>Stimulation</topic><topic>Subthalamic nucleus</topic><topic>Surgery</topic><topic>Training</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Irmen, Friederike</creatorcontrib><creatorcontrib>Horn, Andreas</creatorcontrib><creatorcontrib>Mosley, Philip</creatorcontrib><creatorcontrib>Perry, Alistair</creatorcontrib><creatorcontrib>Petry‐Schmelzer, Jan Niklas</creatorcontrib><creatorcontrib>Dafsari, Haidar S.</creatorcontrib><creatorcontrib>Barbe, Michael</creatorcontrib><creatorcontrib>Visser‐Vandewalle, Veerle</creatorcontrib><creatorcontrib>Schneider, Gerd‐Helge</creatorcontrib><creatorcontrib>Li, Ningfei</creatorcontrib><creatorcontrib>Kübler, Dorothee</creatorcontrib><creatorcontrib>Wenzel, Gregor</creatorcontrib><creatorcontrib>Kühn, Andrea A.</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Free Content</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Annals of neurology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Irmen, Friederike</au><au>Horn, Andreas</au><au>Mosley, Philip</au><au>Perry, Alistair</au><au>Petry‐Schmelzer, Jan Niklas</au><au>Dafsari, Haidar S.</au><au>Barbe, Michael</au><au>Visser‐Vandewalle, Veerle</au><au>Schneider, Gerd‐Helge</au><au>Li, Ningfei</au><au>Kübler, Dorothee</au><au>Wenzel, Gregor</au><au>Kühn, Andrea A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Left Prefrontal Connectivity Links Subthalamic Stimulation with Depressive Symptoms</atitle><jtitle>Annals of neurology</jtitle><addtitle>Ann Neurol</addtitle><date>2020-06</date><risdate>2020</risdate><volume>87</volume><issue>6</issue><spage>962</spage><epage>975</epage><pages>962-975</pages><issn>0364-5134</issn><eissn>1531-8249</eissn><abstract>Objective
Subthalamic nucleus deep brain stimulation (STN‐DBS) in Parkinson's disease (PD) not only stimulates focal target structures but also affects distributed brain networks. The impact this network modulation has on non‐motor DBS effects is not well‐characterized. By focusing on the affective domain, we systematically investigate the impact of electrode placement and associated structural connectivity on changes in depressive symptoms following STN‐DBS, which have been reported to improve, worsen, or remain unchanged.
Methods
Depressive symptoms before and after STN‐DBS surgery were documented in 116 patients with PD from 3 DBS centers (Berlin, Queensland, and Cologne). Based on individual electrode reconstructions, the volumes of tissue activated (VTAs) were estimated and combined with normative connectome data to identify structural connections passing through VTAs. Berlin and Queensland cohorts formed a training and cross‐validation dataset used to identify structural connectivity explaining change in depressive symptoms. The Cologne data served as the test‐set for which depressive symptom change was predicted.
Results
Structural connectivity was linked to depressive symptom change under STN‐DBS. An optimal connectivity map trained on the Berlin cohort could predict changes in depressive symptoms in Queensland patients and vice versa. Furthermore, the joint training‐set map predicted changes in depressive symptoms in the independent test‐set. Worsening of depressive symptoms was associated with left prefrontal connectivity.
Interpretation
Fibers connecting the electrode with left prefrontal areas were associated with worsening of depressive symptoms. Our results suggest that for the left STN‐DBS lead, placement impacting fibers to left prefrontal areas should be avoided to maximize improvement of depressive symptoms. ANN NEUROL 2020;87:962–975</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>32239535</pmid><doi>10.1002/ana.25734</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-0794-1538</orcidid><orcidid>https://orcid.org/0000-0002-0695-6025</orcidid><orcidid>https://orcid.org/0000-0001-5574-3790</orcidid><orcidid>https://orcid.org/0000-0003-0749-3840</orcidid><orcidid>https://orcid.org/0000-0003-1721-3419</orcidid><orcidid>https://orcid.org/0000-0003-3315-3591</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Wiley Online Library Journals Frontfile Complete |
| subjects | Brain Deep brain stimulation Electrical stimuli Electrodes Fibers Mental depression Movement disorders Neural networks Neurodegenerative diseases Parkinson's disease Placement Signs and symptoms Solitary tract nucleus Stimulation Subthalamic nucleus Surgery Training |
| title | Left Prefrontal Connectivity Links Subthalamic Stimulation with Depressive Symptoms |
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