Cargando…

Mechanisms underlying capsulotomy for refractory obsessive-compulsive disorder: neural correlates of negative affect processing overlap with deep brain stimulation targets

Ablative procedures such as anterior capsulotomy are potentially effective in refractory obsessive-compulsive disorder (OCD). Converging evidence suggests the ventral internal capsule white matter tracts traversing the rostral cingulate and ventrolateral prefrontal cortex and thalamus is the optimal...

Descripción completa

Detalles Bibliográficos
Autores principales: Cui, Hailun, Zhang, Yingying, Zhao, Yijie, Zhao, Ying, Ding, Qiong, Chen, Ruiqin, Manssuer, Luis, Zhang, Chencheng, Liu, Wenjuan, Li, Dianyou, Sun, Bomin, Voon, Valerie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10615758/
https://www.ncbi.nlm.nih.gov/pubmed/36878966
http://dx.doi.org/10.1038/s41380-023-01989-1
_version_ 1785129273808388096
author Cui, Hailun
Zhang, Yingying
Zhao, Yijie
Zhao, Ying
Ding, Qiong
Chen, Ruiqin
Manssuer, Luis
Zhang, Chencheng
Liu, Wenjuan
Li, Dianyou
Sun, Bomin
Voon, Valerie
author_facet Cui, Hailun
Zhang, Yingying
Zhao, Yijie
Zhao, Ying
Ding, Qiong
Chen, Ruiqin
Manssuer, Luis
Zhang, Chencheng
Liu, Wenjuan
Li, Dianyou
Sun, Bomin
Voon, Valerie
author_sort Cui, Hailun
collection PubMed
description Ablative procedures such as anterior capsulotomy are potentially effective in refractory obsessive-compulsive disorder (OCD). Converging evidence suggests the ventral internal capsule white matter tracts traversing the rostral cingulate and ventrolateral prefrontal cortex and thalamus is the optimal target for clinical efficacy across multiple deep brain stimulation targets for OCD. Here we ask which prefrontal regions and underlying cognitive processes might be implicated in the effects of capsulotomy by using both task fMRI and neuropsychological tests assessing OCD-relevant cognitive mechanisms known to map across prefrontal regions connected to the tracts targeted in capsulotomy. We tested OCD patients at least 6 months post-capsulotomy (n = 27), OCD controls (n = 33) and healthy controls (n = 34). We used a modified aversive monetary incentive delay paradigm with negative imagery and a within session extinction trial. Post-capsulotomy OCD subjects showed improved OCD symptoms, disability and quality of life with no differences in mood or anxiety or cognitive task performance on executive, inhibition, memory and learning tasks. Task fMRI revealed post-capsulotomy decreases in the nucleus accumbens during negative anticipation, and in the left rostral cingulate and left inferior frontal cortex during negative feedback. Post-capsulotomy patients showed attenuated accumbens-rostral cingulate functional connectivity. Rostral cingulate activity mediated capsulotomy improvement on obsessions. These regions overlap with optimal white matter tracts observed across multiple stimulation targets for OCD and might provide insights into further optimizing neuromodulation approaches. Our findings also suggest that aversive processing theoretical mechanisms may link ablative, stimulation and psychological interventions.
format Online
Article
Text
id pubmed-10615758
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-106157582023-11-01 Mechanisms underlying capsulotomy for refractory obsessive-compulsive disorder: neural correlates of negative affect processing overlap with deep brain stimulation targets Cui, Hailun Zhang, Yingying Zhao, Yijie Zhao, Ying Ding, Qiong Chen, Ruiqin Manssuer, Luis Zhang, Chencheng Liu, Wenjuan Li, Dianyou Sun, Bomin Voon, Valerie Mol Psychiatry Article Ablative procedures such as anterior capsulotomy are potentially effective in refractory obsessive-compulsive disorder (OCD). Converging evidence suggests the ventral internal capsule white matter tracts traversing the rostral cingulate and ventrolateral prefrontal cortex and thalamus is the optimal target for clinical efficacy across multiple deep brain stimulation targets for OCD. Here we ask which prefrontal regions and underlying cognitive processes might be implicated in the effects of capsulotomy by using both task fMRI and neuropsychological tests assessing OCD-relevant cognitive mechanisms known to map across prefrontal regions connected to the tracts targeted in capsulotomy. We tested OCD patients at least 6 months post-capsulotomy (n = 27), OCD controls (n = 33) and healthy controls (n = 34). We used a modified aversive monetary incentive delay paradigm with negative imagery and a within session extinction trial. Post-capsulotomy OCD subjects showed improved OCD symptoms, disability and quality of life with no differences in mood or anxiety or cognitive task performance on executive, inhibition, memory and learning tasks. Task fMRI revealed post-capsulotomy decreases in the nucleus accumbens during negative anticipation, and in the left rostral cingulate and left inferior frontal cortex during negative feedback. Post-capsulotomy patients showed attenuated accumbens-rostral cingulate functional connectivity. Rostral cingulate activity mediated capsulotomy improvement on obsessions. These regions overlap with optimal white matter tracts observed across multiple stimulation targets for OCD and might provide insights into further optimizing neuromodulation approaches. Our findings also suggest that aversive processing theoretical mechanisms may link ablative, stimulation and psychological interventions. Nature Publishing Group UK 2023-03-06 2023 /pmc/articles/PMC10615758/ /pubmed/36878966 http://dx.doi.org/10.1038/s41380-023-01989-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Cui, Hailun
Zhang, Yingying
Zhao, Yijie
Zhao, Ying
Ding, Qiong
Chen, Ruiqin
Manssuer, Luis
Zhang, Chencheng
Liu, Wenjuan
Li, Dianyou
Sun, Bomin
Voon, Valerie
Mechanisms underlying capsulotomy for refractory obsessive-compulsive disorder: neural correlates of negative affect processing overlap with deep brain stimulation targets
title Mechanisms underlying capsulotomy for refractory obsessive-compulsive disorder: neural correlates of negative affect processing overlap with deep brain stimulation targets
title_full Mechanisms underlying capsulotomy for refractory obsessive-compulsive disorder: neural correlates of negative affect processing overlap with deep brain stimulation targets
title_fullStr Mechanisms underlying capsulotomy for refractory obsessive-compulsive disorder: neural correlates of negative affect processing overlap with deep brain stimulation targets
title_full_unstemmed Mechanisms underlying capsulotomy for refractory obsessive-compulsive disorder: neural correlates of negative affect processing overlap with deep brain stimulation targets
title_short Mechanisms underlying capsulotomy for refractory obsessive-compulsive disorder: neural correlates of negative affect processing overlap with deep brain stimulation targets
title_sort mechanisms underlying capsulotomy for refractory obsessive-compulsive disorder: neural correlates of negative affect processing overlap with deep brain stimulation targets
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10615758/
https://www.ncbi.nlm.nih.gov/pubmed/36878966
http://dx.doi.org/10.1038/s41380-023-01989-1
work_keys_str_mv AT cuihailun mechanismsunderlyingcapsulotomyforrefractoryobsessivecompulsivedisorderneuralcorrelatesofnegativeaffectprocessingoverlapwithdeepbrainstimulationtargets
AT zhangyingying mechanismsunderlyingcapsulotomyforrefractoryobsessivecompulsivedisorderneuralcorrelatesofnegativeaffectprocessingoverlapwithdeepbrainstimulationtargets
AT zhaoyijie mechanismsunderlyingcapsulotomyforrefractoryobsessivecompulsivedisorderneuralcorrelatesofnegativeaffectprocessingoverlapwithdeepbrainstimulationtargets
AT zhaoying mechanismsunderlyingcapsulotomyforrefractoryobsessivecompulsivedisorderneuralcorrelatesofnegativeaffectprocessingoverlapwithdeepbrainstimulationtargets
AT dingqiong mechanismsunderlyingcapsulotomyforrefractoryobsessivecompulsivedisorderneuralcorrelatesofnegativeaffectprocessingoverlapwithdeepbrainstimulationtargets
AT chenruiqin mechanismsunderlyingcapsulotomyforrefractoryobsessivecompulsivedisorderneuralcorrelatesofnegativeaffectprocessingoverlapwithdeepbrainstimulationtargets
AT manssuerluis mechanismsunderlyingcapsulotomyforrefractoryobsessivecompulsivedisorderneuralcorrelatesofnegativeaffectprocessingoverlapwithdeepbrainstimulationtargets
AT zhangchencheng mechanismsunderlyingcapsulotomyforrefractoryobsessivecompulsivedisorderneuralcorrelatesofnegativeaffectprocessingoverlapwithdeepbrainstimulationtargets
AT liuwenjuan mechanismsunderlyingcapsulotomyforrefractoryobsessivecompulsivedisorderneuralcorrelatesofnegativeaffectprocessingoverlapwithdeepbrainstimulationtargets
AT lidianyou mechanismsunderlyingcapsulotomyforrefractoryobsessivecompulsivedisorderneuralcorrelatesofnegativeaffectprocessingoverlapwithdeepbrainstimulationtargets
AT sunbomin mechanismsunderlyingcapsulotomyforrefractoryobsessivecompulsivedisorderneuralcorrelatesofnegativeaffectprocessingoverlapwithdeepbrainstimulationtargets
AT voonvalerie mechanismsunderlyingcapsulotomyforrefractoryobsessivecompulsivedisorderneuralcorrelatesofnegativeaffectprocessingoverlapwithdeepbrainstimulationtargets