Exploring the connectivity of dorsolateral prefrontal cortex and the modulatory impact of transcranial magnetic stimulation in adolescents with depression: a focus on pain-related cognitive processing

Abstract Background Abnormal cognitive response to pain is consistently associated with deleterious outcomes among adolescents with depression. Highly relevant to both pain and cognition, dorsolateral prefrontal cortex (DLPFC) is important to understanding pain cognition. Our study aimed to characte...

Full description

Saved in:
Bibliographic Details
Main Authors: Dan Qiao, Yiran Li, Xiaoyu Zhang, Yujiao Wen, Xuemin Zhang, Lu Ma, Gaizhi Li, Chunxia Yang, Zhifen Liu
Format: Article
Language:English
Published: BMC 2024-11-01
Series:BMC Psychiatry
Subjects:
Online Access:https://doi.org/10.1186/s12888-024-06321-x
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846147502647017472
author Dan Qiao
Yiran Li
Xiaoyu Zhang
Yujiao Wen
Xuemin Zhang
Lu Ma
Gaizhi Li
Chunxia Yang
Zhifen Liu
author_facet Dan Qiao
Yiran Li
Xiaoyu Zhang
Yujiao Wen
Xuemin Zhang
Lu Ma
Gaizhi Li
Chunxia Yang
Zhifen Liu
author_sort Dan Qiao
collection DOAJ
description Abstract Background Abnormal cognitive response to pain is consistently associated with deleterious outcomes among adolescents with depression. Highly relevant to both pain and cognition, dorsolateral prefrontal cortex (DLPFC) is important to understanding pain cognition. Our study aimed to characterize the circuit of DLPFC and the efficacy of transcranial magnetic stimulation (TMS) over DLPFC on pain cognition in adolescents with depression. Methods Using neuroimaging data, we first compared functional connectivity (FC) of DLPFC between 60 adolescents with depression and 65 controls. The patients were then divided into add-on TMS group (N = 30) and Sertraline group (N = 30). Clinical outcome was determined using Pain Vigilance and Awareness Questionnaire (PVAQ) and Pain Catastrophizing Scale (PCS). Finally, we conducted regression analysis to assess the effect that FC of DLPFC contributes to in predicting clinical outcome. Results FC analysis showed that compared to controls, patients displayed hyperconnection of left DLPFC - left triangular part of inferior frontal gyrus (IFG), which was significantly correlated with higher PCS total-, magnification- and helplessness-scores. Patients also showed hyperconnection of right DLPFC - right supramarginal gyrus (SMG), which was correlated with lower PCS total- and rumination- scores. After intervention, the add-on TMS group displayed significantly decreased score on PVAQ, PCS total and rumination. FC of left DLPFC - bilateral triangular part of IFG, - right SMG, as well as right DLPFC - left putamen, could predict the improvement of pain vigilance and magnification. Conclusion Our results point to a key role of DLPFC acting as a connection linking cognitive control and pain processing in adolescents with depression. Trial registration The study is registered in https://www.chictr.org.cn/ with a registration number ChiCTR2000039503 (date: 10.30.2020).
format Article
id doaj-art-78dfae0bcc774c059a8efff9aae15dc4
institution Kabale University
issn 1471-244X
language English
publishDate 2024-11-01
publisher BMC
record_format Article
series BMC Psychiatry
spelling doaj-art-78dfae0bcc774c059a8efff9aae15dc42024-12-01T12:38:53ZengBMCBMC Psychiatry1471-244X2024-11-0124111310.1186/s12888-024-06321-xExploring the connectivity of dorsolateral prefrontal cortex and the modulatory impact of transcranial magnetic stimulation in adolescents with depression: a focus on pain-related cognitive processingDan Qiao0Yiran Li1Xiaoyu Zhang2Yujiao Wen3Xuemin Zhang4Lu Ma5Gaizhi Li6Chunxia Yang7Zhifen Liu8Department of Psychiatry, First Hospital of Shanxi Medical UniversityDepartment of Psychiatry, First Hospital of Shanxi Medical UniversityDepartment of Psychiatry, First Hospital of Shanxi Medical UniversityDepartment of Psychiatry, First Hospital of Shanxi Medical UniversityDepartment of Psychiatry, First Hospital of Shanxi Medical UniversityDepartment of Psychiatry, First Hospital of Shanxi Medical UniversityDepartment of Psychiatry, First Hospital of Shanxi Medical UniversityDepartment of Psychiatry, First Hospital of Shanxi Medical UniversityDepartment of Psychiatry, First Hospital of Shanxi Medical UniversityAbstract Background Abnormal cognitive response to pain is consistently associated with deleterious outcomes among adolescents with depression. Highly relevant to both pain and cognition, dorsolateral prefrontal cortex (DLPFC) is important to understanding pain cognition. Our study aimed to characterize the circuit of DLPFC and the efficacy of transcranial magnetic stimulation (TMS) over DLPFC on pain cognition in adolescents with depression. Methods Using neuroimaging data, we first compared functional connectivity (FC) of DLPFC between 60 adolescents with depression and 65 controls. The patients were then divided into add-on TMS group (N = 30) and Sertraline group (N = 30). Clinical outcome was determined using Pain Vigilance and Awareness Questionnaire (PVAQ) and Pain Catastrophizing Scale (PCS). Finally, we conducted regression analysis to assess the effect that FC of DLPFC contributes to in predicting clinical outcome. Results FC analysis showed that compared to controls, patients displayed hyperconnection of left DLPFC - left triangular part of inferior frontal gyrus (IFG), which was significantly correlated with higher PCS total-, magnification- and helplessness-scores. Patients also showed hyperconnection of right DLPFC - right supramarginal gyrus (SMG), which was correlated with lower PCS total- and rumination- scores. After intervention, the add-on TMS group displayed significantly decreased score on PVAQ, PCS total and rumination. FC of left DLPFC - bilateral triangular part of IFG, - right SMG, as well as right DLPFC - left putamen, could predict the improvement of pain vigilance and magnification. Conclusion Our results point to a key role of DLPFC acting as a connection linking cognitive control and pain processing in adolescents with depression. Trial registration The study is registered in https://www.chictr.org.cn/ with a registration number ChiCTR2000039503 (date: 10.30.2020).https://doi.org/10.1186/s12888-024-06321-xAdolescent depressionPainCognitionDorsolateral prefrontal cortexTranscranial magnetic stimulation
spellingShingle Dan Qiao
Yiran Li
Xiaoyu Zhang
Yujiao Wen
Xuemin Zhang
Lu Ma
Gaizhi Li
Chunxia Yang
Zhifen Liu
Exploring the connectivity of dorsolateral prefrontal cortex and the modulatory impact of transcranial magnetic stimulation in adolescents with depression: a focus on pain-related cognitive processing
BMC Psychiatry
Adolescent depression
Pain
Cognition
Dorsolateral prefrontal cortex
Transcranial magnetic stimulation
title Exploring the connectivity of dorsolateral prefrontal cortex and the modulatory impact of transcranial magnetic stimulation in adolescents with depression: a focus on pain-related cognitive processing
title_full Exploring the connectivity of dorsolateral prefrontal cortex and the modulatory impact of transcranial magnetic stimulation in adolescents with depression: a focus on pain-related cognitive processing
title_fullStr Exploring the connectivity of dorsolateral prefrontal cortex and the modulatory impact of transcranial magnetic stimulation in adolescents with depression: a focus on pain-related cognitive processing
title_full_unstemmed Exploring the connectivity of dorsolateral prefrontal cortex and the modulatory impact of transcranial magnetic stimulation in adolescents with depression: a focus on pain-related cognitive processing
title_short Exploring the connectivity of dorsolateral prefrontal cortex and the modulatory impact of transcranial magnetic stimulation in adolescents with depression: a focus on pain-related cognitive processing
title_sort exploring the connectivity of dorsolateral prefrontal cortex and the modulatory impact of transcranial magnetic stimulation in adolescents with depression a focus on pain related cognitive processing
topic Adolescent depression
Pain
Cognition
Dorsolateral prefrontal cortex
Transcranial magnetic stimulation
url https://doi.org/10.1186/s12888-024-06321-x
work_keys_str_mv AT danqiao exploringtheconnectivityofdorsolateralprefrontalcortexandthemodulatoryimpactoftranscranialmagneticstimulationinadolescentswithdepressionafocusonpainrelatedcognitiveprocessing
AT yiranli exploringtheconnectivityofdorsolateralprefrontalcortexandthemodulatoryimpactoftranscranialmagneticstimulationinadolescentswithdepressionafocusonpainrelatedcognitiveprocessing
AT xiaoyuzhang exploringtheconnectivityofdorsolateralprefrontalcortexandthemodulatoryimpactoftranscranialmagneticstimulationinadolescentswithdepressionafocusonpainrelatedcognitiveprocessing
AT yujiaowen exploringtheconnectivityofdorsolateralprefrontalcortexandthemodulatoryimpactoftranscranialmagneticstimulationinadolescentswithdepressionafocusonpainrelatedcognitiveprocessing
AT xueminzhang exploringtheconnectivityofdorsolateralprefrontalcortexandthemodulatoryimpactoftranscranialmagneticstimulationinadolescentswithdepressionafocusonpainrelatedcognitiveprocessing
AT luma exploringtheconnectivityofdorsolateralprefrontalcortexandthemodulatoryimpactoftranscranialmagneticstimulationinadolescentswithdepressionafocusonpainrelatedcognitiveprocessing
AT gaizhili exploringtheconnectivityofdorsolateralprefrontalcortexandthemodulatoryimpactoftranscranialmagneticstimulationinadolescentswithdepressionafocusonpainrelatedcognitiveprocessing
AT chunxiayang exploringtheconnectivityofdorsolateralprefrontalcortexandthemodulatoryimpactoftranscranialmagneticstimulationinadolescentswithdepressionafocusonpainrelatedcognitiveprocessing
AT zhifenliu exploringtheconnectivityofdorsolateralprefrontalcortexandthemodulatoryimpactoftranscranialmagneticstimulationinadolescentswithdepressionafocusonpainrelatedcognitiveprocessing