Links between electroconvulsive therapy responsive and cognitive impairment multimodal brain networks in late-life major depressive disorder
Abstract Background Although electroconvulsive therapy (ECT) is an effective treatment for depression, ECT cognitive impairment remains a major concern. The neurobiological underpinnings and mechanisms underlying ECT antidepressant and cognitive impairment effects remain unknown. This investigation...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-12-01
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| Series: | BMC Medicine |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12916-022-02678-6 |
| _version_ | 1827974479090810880 |
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| author | Shile Qi Vince D. Calhoun Daoqiang Zhang Jeremy Miller Zhi-De Deng Katherine L. Narr Yvette Sheline Shawn M. McClintock Rongtao Jiang Xiao Yang Joel Upston Tom Jones Jing Sui Christopher C. Abbott |
| author_facet | Shile Qi Vince D. Calhoun Daoqiang Zhang Jeremy Miller Zhi-De Deng Katherine L. Narr Yvette Sheline Shawn M. McClintock Rongtao Jiang Xiao Yang Joel Upston Tom Jones Jing Sui Christopher C. Abbott |
| author_sort | Shile Qi |
| collection | DOAJ |
| description | Abstract Background Although electroconvulsive therapy (ECT) is an effective treatment for depression, ECT cognitive impairment remains a major concern. The neurobiological underpinnings and mechanisms underlying ECT antidepressant and cognitive impairment effects remain unknown. This investigation aims to identify ECT antidepressant-response and cognitive-impairment multimodal brain networks and assesses whether they are associated with the ECT-induced electric field (E-field) with an optimal pulse amplitude estimation. Methods A single site clinical trial focused on amplitude (600, 700, and 800 mA) included longitudinal multimodal imaging and clinical and cognitive assessments completed before and immediately after the ECT series (n = 54) for late-life depression. Another two independent validation cohorts (n = 84, n = 260) were included. Symptom and cognition were used as references to supervise fMRI and sMRI fusion to identify ECT antidepressant-response and cognitive-impairment multimodal brain networks. Correlations between ECT-induced E-field within these two networks and clinical and cognitive outcomes were calculated. An optimal pulse amplitude was estimated based on E-field within antidepressant-response and cognitive-impairment networks. Results Decreased function in the superior orbitofrontal cortex and caudate accompanied with increased volume in medial temporal cortex showed covarying functional and structural alterations in both antidepressant-response and cognitive-impairment networks. Volume increases in the hippocampal complex and thalamus were antidepressant-response specific, and functional decreases in the amygdala and hippocampal complex were cognitive-impairment specific, which were validated in two independent datasets. The E-field within these two networks showed an inverse relationship with HDRS reduction and cognitive impairment. The optimal E-filed range as [92.7–113.9] V/m was estimated to maximize antidepressant outcomes without compromising cognitive safety. Conclusions The large degree of overlap between antidepressant-response and cognitive-impairment networks challenges parameter development focused on precise E-field dosing with new electrode placements. The determination of the optimal individualized ECT amplitude within the antidepressant and cognitive networks may improve the treatment benefit–risk ratio. Trial registration ClinicalTrials.gov Identifier: NCT02999269. |
| first_indexed | 2024-04-09T19:55:02Z |
| format | Article |
| id | doaj.art-35e29fc7300846a9a32e5ab19dcad5c9 |
| institution | Directory Open Access Journal |
| issn | 1741-7015 |
| language | English |
| last_indexed | 2024-04-09T19:55:02Z |
| publishDate | 2022-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Medicine |
| spelling | doaj.art-35e29fc7300846a9a32e5ab19dcad5c92023-04-03T05:30:07ZengBMCBMC Medicine1741-70152022-12-0120111310.1186/s12916-022-02678-6Links between electroconvulsive therapy responsive and cognitive impairment multimodal brain networks in late-life major depressive disorderShile Qi0Vince D. Calhoun1Daoqiang Zhang2Jeremy Miller3Zhi-De Deng4Katherine L. Narr5Yvette Sheline6Shawn M. McClintock7Rongtao Jiang8Xiao Yang9Joel Upston10Tom Jones11Jing Sui12Christopher C. Abbott13College of Computer Science and Technology, Nanjing University of Aeronautics and AstronauticsTri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS) Georgia State University, Georgia Institute of Technology, Emory UniversityCollege of Computer Science and Technology, Nanjing University of Aeronautics and AstronauticsDepartment of Psychiatry, University of New MexicoNoninvasive Neuromodulation Unit, Experimental Therapeutics & Pathophysiology Branch, National Institute of Mental HealthDepartments of Neurology, Psychiatry and Biobehavioral Sciences, University of CaliforniaDepartment of Psychiatry, University of PennsylvaniaDivision of Psychology, Department of Psychiatry, UT Southwestern Medical CenterState Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal UniversityHuaxi Brain Research Center, West China Hospital of Sichuan UniversityDepartment of Psychiatry, University of New MexicoDepartment of Psychiatry, University of New MexicoState Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal UniversityDepartment of Psychiatry, University of New MexicoAbstract Background Although electroconvulsive therapy (ECT) is an effective treatment for depression, ECT cognitive impairment remains a major concern. The neurobiological underpinnings and mechanisms underlying ECT antidepressant and cognitive impairment effects remain unknown. This investigation aims to identify ECT antidepressant-response and cognitive-impairment multimodal brain networks and assesses whether they are associated with the ECT-induced electric field (E-field) with an optimal pulse amplitude estimation. Methods A single site clinical trial focused on amplitude (600, 700, and 800 mA) included longitudinal multimodal imaging and clinical and cognitive assessments completed before and immediately after the ECT series (n = 54) for late-life depression. Another two independent validation cohorts (n = 84, n = 260) were included. Symptom and cognition were used as references to supervise fMRI and sMRI fusion to identify ECT antidepressant-response and cognitive-impairment multimodal brain networks. Correlations between ECT-induced E-field within these two networks and clinical and cognitive outcomes were calculated. An optimal pulse amplitude was estimated based on E-field within antidepressant-response and cognitive-impairment networks. Results Decreased function in the superior orbitofrontal cortex and caudate accompanied with increased volume in medial temporal cortex showed covarying functional and structural alterations in both antidepressant-response and cognitive-impairment networks. Volume increases in the hippocampal complex and thalamus were antidepressant-response specific, and functional decreases in the amygdala and hippocampal complex were cognitive-impairment specific, which were validated in two independent datasets. The E-field within these two networks showed an inverse relationship with HDRS reduction and cognitive impairment. The optimal E-filed range as [92.7–113.9] V/m was estimated to maximize antidepressant outcomes without compromising cognitive safety. Conclusions The large degree of overlap between antidepressant-response and cognitive-impairment networks challenges parameter development focused on precise E-field dosing with new electrode placements. The determination of the optimal individualized ECT amplitude within the antidepressant and cognitive networks may improve the treatment benefit–risk ratio. Trial registration ClinicalTrials.gov Identifier: NCT02999269.https://doi.org/10.1186/s12916-022-02678-6Electroconvulsive therapyAntidepressantCognitive impairmentElectric fieldMultimodal fusion |
| spellingShingle | Shile Qi Vince D. Calhoun Daoqiang Zhang Jeremy Miller Zhi-De Deng Katherine L. Narr Yvette Sheline Shawn M. McClintock Rongtao Jiang Xiao Yang Joel Upston Tom Jones Jing Sui Christopher C. Abbott Links between electroconvulsive therapy responsive and cognitive impairment multimodal brain networks in late-life major depressive disorder BMC Medicine Electroconvulsive therapy Antidepressant Cognitive impairment Electric field Multimodal fusion |
| title | Links between electroconvulsive therapy responsive and cognitive impairment multimodal brain networks in late-life major depressive disorder |
| title_full | Links between electroconvulsive therapy responsive and cognitive impairment multimodal brain networks in late-life major depressive disorder |
| title_fullStr | Links between electroconvulsive therapy responsive and cognitive impairment multimodal brain networks in late-life major depressive disorder |
| title_full_unstemmed | Links between electroconvulsive therapy responsive and cognitive impairment multimodal brain networks in late-life major depressive disorder |
| title_short | Links between electroconvulsive therapy responsive and cognitive impairment multimodal brain networks in late-life major depressive disorder |
| title_sort | links between electroconvulsive therapy responsive and cognitive impairment multimodal brain networks in late life major depressive disorder |
| topic | Electroconvulsive therapy Antidepressant Cognitive impairment Electric field Multimodal fusion |
| url | https://doi.org/10.1186/s12916-022-02678-6 |
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