Enhancing ventrolateral prefrontal cortex activation mitigates social pain and modifies subsequent social attitudes: Insights from TMS and fMRI

Social pain, a multifaceted emotional response triggered by interpersonal rejection or criticism, profoundly impacts mental well-being and social interactions. While prior research has implicated the right ventrolateral prefrontal cortex (rVLPFC) in mitigating social pain, the precise neural mechani...

Full description

Bibliographic Details
Main Authors: Sijin Li, Xueying Cao, Yiwei Li, Yuyao Tang, Si Cheng, Dandan Zhang
Format: Article
Language:English
Published: Elsevier 2024-04-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811924001150
_version_ 1797199860714176512
author Sijin Li
Xueying Cao
Yiwei Li
Yuyao Tang
Si Cheng
Dandan Zhang
author_facet Sijin Li
Xueying Cao
Yiwei Li
Yuyao Tang
Si Cheng
Dandan Zhang
author_sort Sijin Li
collection DOAJ
description Social pain, a multifaceted emotional response triggered by interpersonal rejection or criticism, profoundly impacts mental well-being and social interactions. While prior research has implicated the right ventrolateral prefrontal cortex (rVLPFC) in mitigating social pain, the precise neural mechanisms and downstream effects on subsequent social attitudes remain elusive. This study employed transcranial magnetic stimulation (TMS) integrated with fMRI recordings during a social pain task to elucidate these aspects. Eighty participants underwent either active TMS targeting the rVLPFC (n = 41) or control stimulation at the vertex (n = 39). Our results revealed that TMS-induced rVLPFC facilitation significantly reduced self-reported social pain, confirming the causal role of the rVLPFC in social pain relief. Functional connectivity analyses demonstrated enhanced interactions between the rVLPFC and the dorsolateral prefrontal cortex, emphasizing the collaborative engagement of prefrontal regions in emotion regulation. Significantly, we observed that negative social feedback led to negative social attitudes, whereas rVLPFC activation countered this detrimental effect, showcasing the potential of the rVLPFC as a protective buffer against adverse social interactions. Moreover, our study uncovered the impact role of the hippocampus in subsequent social attitudes, a relationship particularly pronounced during excitatory TMS over the rVLPFC. These findings offer promising avenues for improving mental health within the intricate dynamics of social interactions. By advancing our comprehension of the neural mechanisms underlying social pain relief, this research introduces novel intervention strategies for individuals grappling with social distress. Empowering individuals to modulate rVLPFC activation may facilitate reshaping social attitudes and successful reintegration into communal life.
first_indexed 2024-04-24T07:22:28Z
format Article
id doaj.art-cf1c5428acaf431bb6c0391827112eaa
institution Directory Open Access Journal
issn 1095-9572
language English
last_indexed 2024-04-24T07:22:28Z
publishDate 2024-04-01
publisher Elsevier
record_format Article
series NeuroImage
spelling doaj.art-cf1c5428acaf431bb6c0391827112eaa2024-04-21T04:14:19ZengElsevierNeuroImage1095-95722024-04-01292120620Enhancing ventrolateral prefrontal cortex activation mitigates social pain and modifies subsequent social attitudes: Insights from TMS and fMRISijin Li0Xueying Cao1Yiwei Li2Yuyao Tang3Si Cheng4Dandan Zhang5Institute of Brain and Psychological Sciences, Sichuan Normal University, Chengdu 610066, China; School of Psychology, Shenzhen University, Shenzhen 518060, ChinaSchool of Psychology, Shenzhen University, Shenzhen 518060, ChinaInstitute of Brain and Psychological Sciences, Sichuan Normal University, Chengdu 610066, ChinaInstitute of Brain and Psychological Sciences, Sichuan Normal University, Chengdu 610066, ChinaSchool of Psychology, Shenzhen University, Shenzhen 518060, ChinaInstitute of Brain and Psychological Sciences, Sichuan Normal University, Chengdu 610066, China; Shenzhen-Hong Kong Institute of Brain Science, Shenzhen 518055, China; Magnetic Resonance Imaging Center, Shenzhen University, Shenzhen 518060, China; Corresponding author.Social pain, a multifaceted emotional response triggered by interpersonal rejection or criticism, profoundly impacts mental well-being and social interactions. While prior research has implicated the right ventrolateral prefrontal cortex (rVLPFC) in mitigating social pain, the precise neural mechanisms and downstream effects on subsequent social attitudes remain elusive. This study employed transcranial magnetic stimulation (TMS) integrated with fMRI recordings during a social pain task to elucidate these aspects. Eighty participants underwent either active TMS targeting the rVLPFC (n = 41) or control stimulation at the vertex (n = 39). Our results revealed that TMS-induced rVLPFC facilitation significantly reduced self-reported social pain, confirming the causal role of the rVLPFC in social pain relief. Functional connectivity analyses demonstrated enhanced interactions between the rVLPFC and the dorsolateral prefrontal cortex, emphasizing the collaborative engagement of prefrontal regions in emotion regulation. Significantly, we observed that negative social feedback led to negative social attitudes, whereas rVLPFC activation countered this detrimental effect, showcasing the potential of the rVLPFC as a protective buffer against adverse social interactions. Moreover, our study uncovered the impact role of the hippocampus in subsequent social attitudes, a relationship particularly pronounced during excitatory TMS over the rVLPFC. These findings offer promising avenues for improving mental health within the intricate dynamics of social interactions. By advancing our comprehension of the neural mechanisms underlying social pain relief, this research introduces novel intervention strategies for individuals grappling with social distress. Empowering individuals to modulate rVLPFC activation may facilitate reshaping social attitudes and successful reintegration into communal life.http://www.sciencedirect.com/science/article/pii/S1053811924001150Social painSocial feedbackVentrolateral prefrontal cortexHippocampusTranscranial magnetic stimulationSocial attitude
spellingShingle Sijin Li
Xueying Cao
Yiwei Li
Yuyao Tang
Si Cheng
Dandan Zhang
Enhancing ventrolateral prefrontal cortex activation mitigates social pain and modifies subsequent social attitudes: Insights from TMS and fMRI
NeuroImage
Social pain
Social feedback
Ventrolateral prefrontal cortex
Hippocampus
Transcranial magnetic stimulation
Social attitude
title Enhancing ventrolateral prefrontal cortex activation mitigates social pain and modifies subsequent social attitudes: Insights from TMS and fMRI
title_full Enhancing ventrolateral prefrontal cortex activation mitigates social pain and modifies subsequent social attitudes: Insights from TMS and fMRI
title_fullStr Enhancing ventrolateral prefrontal cortex activation mitigates social pain and modifies subsequent social attitudes: Insights from TMS and fMRI
title_full_unstemmed Enhancing ventrolateral prefrontal cortex activation mitigates social pain and modifies subsequent social attitudes: Insights from TMS and fMRI
title_short Enhancing ventrolateral prefrontal cortex activation mitigates social pain and modifies subsequent social attitudes: Insights from TMS and fMRI
title_sort enhancing ventrolateral prefrontal cortex activation mitigates social pain and modifies subsequent social attitudes insights from tms and fmri
topic Social pain
Social feedback
Ventrolateral prefrontal cortex
Hippocampus
Transcranial magnetic stimulation
Social attitude
url http://www.sciencedirect.com/science/article/pii/S1053811924001150
work_keys_str_mv AT sijinli enhancingventrolateralprefrontalcortexactivationmitigatessocialpainandmodifiessubsequentsocialattitudesinsightsfromtmsandfmri
AT xueyingcao enhancingventrolateralprefrontalcortexactivationmitigatessocialpainandmodifiessubsequentsocialattitudesinsightsfromtmsandfmri
AT yiweili enhancingventrolateralprefrontalcortexactivationmitigatessocialpainandmodifiessubsequentsocialattitudesinsightsfromtmsandfmri
AT yuyaotang enhancingventrolateralprefrontalcortexactivationmitigatessocialpainandmodifiessubsequentsocialattitudesinsightsfromtmsandfmri
AT sicheng enhancingventrolateralprefrontalcortexactivationmitigatessocialpainandmodifiessubsequentsocialattitudesinsightsfromtmsandfmri
AT dandanzhang enhancingventrolateralprefrontalcortexactivationmitigatessocialpainandmodifiessubsequentsocialattitudesinsightsfromtmsandfmri