A Lesion-Derived Brain Network for Emotion Regulation

Jing Jiang; Michael A. Ferguson; Jordan Grafman; Alexander L. Cohen; Michael D. Fox

doi:10.1016/j.biopsych.2023.02.007

A Lesion-Derived Brain Network for Emotion Regulation

Jing Jiang^*, Michael A. Ferguson, Jordan Grafman, Alexander L. Cohen, Michael D. Fox

^*Corresponding author for this work

Physical Medicine and Rehabilitation

Research output: Contribution to journal › Article › peer-review

16 Scopus citations

Abstract

Background: Emotion regulation has been linked to specific brain networks based on functional neuroimaging, but networks causally involved in emotion regulation remain unknown. Methods: We studied patients with focal brain damage (N = 167) who completed the managing emotion subscale of the Mayer-Salovey-Caruso Emotional Intelligence Test, a measure of emotion regulation. First, we tested whether patients with lesions to an a priori network derived from functional neuroimaging showed impaired emotion regulation. Next, we leveraged lesion network mapping to derive a de novo brain network for emotion regulation. Finally, we used an independent lesion database (N = 629) to test whether damage to this lesion-derived network would increase the risk of neuropsychiatric conditions associated with emotion regulation impairment. Results: First, patients with lesions intersecting the a priori emotion regulation network derived from functional neuroimaging showed impairments in the managing emotion subscale of the Mayer-Salovey-Caruso Emotional Intelligence Test. Next, our de novo brain network for emotion regulation derived from lesion data was defined by functional connectivity to the left ventrolateral prefrontal cortex. Finally, in the independent database, lesions associated with mania, criminality, and depression intersected this de novo brain network more than lesions associated with other disorders. Conclusions: The findings suggest that emotion regulation maps to a connected brain network centered on the left ventrolateral prefrontal cortex. Lesion damage to part of this network is associated with reported difficulties in managing emotions and is related to increased likelihood of having one of several neuropsychiatric disorders.

Original language	English (US)
Pages (from-to)	640-649
Number of pages	10
Journal	Biological psychiatry
Volume	94
Issue number	8
DOIs	https://doi.org/10.1016/j.biopsych.2023.02.007
State	Published - Oct 15 2023

Funding

This work was supported by the Ellison/Baszucki Foundation (to MDF) and the Brain and Behavior Research Foundation Young Investigator grant (Grant No. 29441 [to JJ]). MDF was also supported by the Nancy Lurie Marks Foundation, the Kaye Family Research Endowment, and the National Institutes of Health (Grant Nos. R01MH113929, R21MH126271, R56AG069086, R01MH115949, and R01AG060987). AC was supported by a Shields Research grant from the Child Neurology Foundation, the Simons Foundation Autism Research Initiative Bridge to Independence Fellowship, and the National Institute of Mental Health (Grant No. K23MH120510). JJ, ALC, and MDF conceptualized and developed methods; JJ, ALC, and MAF performed data analyses; JJ wrote manuscript drafts; and JG provided a patient dataset with behavioral and demographic data. All authors revised the manuscript. A previous version of this paper was published as a preprint on Research Square:https://doi.org/10.21203/rs.3.rs-1363458/v1. Questions about the Vietnam Head Injury Study data analyzed in this study are available from Jordan Grafman while the corresponding author can provide other data upon reasonable request. The code and other data used in this study are available from the corresponding author upon reasonable request. MDF is a consultant for Magnus Medical and Solaris and holds intellectual property on using connectivity imaging to guide brain stimulation treatments. All other authors report no biomedical financial interests or potential conflicts of interest. This work was supported by the Ellison/Baszucki Foundation (to MDF) and the Brain and Behavior Research Foundation Young Investigator grant (Grant No. 29441 [to JJ]). MDF was also supported by the Nancy Lurie Marks Foundation, the Kaye Family Research Endowment, and the National Institutes of Health (Grant Nos. R01MH113929, R21MH126271, R56AG069086, R01MH115949, and R01AG060987). AC was supported by a Shields Research grant from the Child Neurology Foundation, the Simons Foundation Autism Research Initiative Bridge to Independence Fellowship, and the National Institute of Mental Health (Grant No. K23MH120510).

Keywords

Brain lesion
Emotion regulation
Functional connectivity
Lesion network mapping
fMRI

ASJC Scopus subject areas

Biological Psychiatry

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10.1016/j.biopsych.2023.02.007

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title = "A Lesion-Derived Brain Network for Emotion Regulation",

abstract = "Background: Emotion regulation has been linked to specific brain networks based on functional neuroimaging, but networks causally involved in emotion regulation remain unknown. Methods: We studied patients with focal brain damage (N = 167) who completed the managing emotion subscale of the Mayer-Salovey-Caruso Emotional Intelligence Test, a measure of emotion regulation. First, we tested whether patients with lesions to an a priori network derived from functional neuroimaging showed impaired emotion regulation. Next, we leveraged lesion network mapping to derive a de novo brain network for emotion regulation. Finally, we used an independent lesion database (N = 629) to test whether damage to this lesion-derived network would increase the risk of neuropsychiatric conditions associated with emotion regulation impairment. Results: First, patients with lesions intersecting the a priori emotion regulation network derived from functional neuroimaging showed impairments in the managing emotion subscale of the Mayer-Salovey-Caruso Emotional Intelligence Test. Next, our de novo brain network for emotion regulation derived from lesion data was defined by functional connectivity to the left ventrolateral prefrontal cortex. Finally, in the independent database, lesions associated with mania, criminality, and depression intersected this de novo brain network more than lesions associated with other disorders. Conclusions: The findings suggest that emotion regulation maps to a connected brain network centered on the left ventrolateral prefrontal cortex. Lesion damage to part of this network is associated with reported difficulties in managing emotions and is related to increased likelihood of having one of several neuropsychiatric disorders.",

keywords = "Brain lesion, Emotion regulation, Functional connectivity, Lesion network mapping, fMRI",

author = "Jing Jiang and Ferguson, \{Michael A.\} and Jordan Grafman and Cohen, \{Alexander L.\} and Fox, \{Michael D.\}",

note = "Publisher Copyright: {\textcopyright} 2023 Society of Biological Psychiatry",

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N2 - Background: Emotion regulation has been linked to specific brain networks based on functional neuroimaging, but networks causally involved in emotion regulation remain unknown. Methods: We studied patients with focal brain damage (N = 167) who completed the managing emotion subscale of the Mayer-Salovey-Caruso Emotional Intelligence Test, a measure of emotion regulation. First, we tested whether patients with lesions to an a priori network derived from functional neuroimaging showed impaired emotion regulation. Next, we leveraged lesion network mapping to derive a de novo brain network for emotion regulation. Finally, we used an independent lesion database (N = 629) to test whether damage to this lesion-derived network would increase the risk of neuropsychiatric conditions associated with emotion regulation impairment. Results: First, patients with lesions intersecting the a priori emotion regulation network derived from functional neuroimaging showed impairments in the managing emotion subscale of the Mayer-Salovey-Caruso Emotional Intelligence Test. Next, our de novo brain network for emotion regulation derived from lesion data was defined by functional connectivity to the left ventrolateral prefrontal cortex. Finally, in the independent database, lesions associated with mania, criminality, and depression intersected this de novo brain network more than lesions associated with other disorders. Conclusions: The findings suggest that emotion regulation maps to a connected brain network centered on the left ventrolateral prefrontal cortex. Lesion damage to part of this network is associated with reported difficulties in managing emotions and is related to increased likelihood of having one of several neuropsychiatric disorders.

AB - Background: Emotion regulation has been linked to specific brain networks based on functional neuroimaging, but networks causally involved in emotion regulation remain unknown. Methods: We studied patients with focal brain damage (N = 167) who completed the managing emotion subscale of the Mayer-Salovey-Caruso Emotional Intelligence Test, a measure of emotion regulation. First, we tested whether patients with lesions to an a priori network derived from functional neuroimaging showed impaired emotion regulation. Next, we leveraged lesion network mapping to derive a de novo brain network for emotion regulation. Finally, we used an independent lesion database (N = 629) to test whether damage to this lesion-derived network would increase the risk of neuropsychiatric conditions associated with emotion regulation impairment. Results: First, patients with lesions intersecting the a priori emotion regulation network derived from functional neuroimaging showed impairments in the managing emotion subscale of the Mayer-Salovey-Caruso Emotional Intelligence Test. Next, our de novo brain network for emotion regulation derived from lesion data was defined by functional connectivity to the left ventrolateral prefrontal cortex. Finally, in the independent database, lesions associated with mania, criminality, and depression intersected this de novo brain network more than lesions associated with other disorders. Conclusions: The findings suggest that emotion regulation maps to a connected brain network centered on the left ventrolateral prefrontal cortex. Lesion damage to part of this network is associated with reported difficulties in managing emotions and is related to increased likelihood of having one of several neuropsychiatric disorders.

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KW - Emotion regulation

KW - Functional connectivity

KW - Lesion network mapping

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A Lesion-Derived Brain Network for Emotion Regulation

Abstract

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Keywords

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