Tracing the Neural Carryover Effects of Interpersonal Anger on Resting-State fMRI in Men and Their Relation to Traumatic Stress Symptoms in a Subsample of Soldiers.

Gadi Gilam,Eyal Fruchter,Talma Hendler,Efrat Kliper,Adi Maron-Katz,Ron Shamir,Tamar Lin

doi:10.3389/fnbeh.2017.00252

Abstract

Uncontrolled anger may lead to aggression and is common in various clinical conditions, including post traumatic stress disorder. Emotion regulation strategies may vary with some more adaptive and efficient than others in reducing angry feelings. However, such feelings tend to linger after anger provocation, extending the challenge of coping with anger beyond provocation. Task-independent resting-state (rs) fMRI may be a particularly useful paradigm to reveal neural processes of spontaneous recovery from a preceding negative emotional experience. We aimed to trace the carryover effects of anger on endogenous neural dynamics by applying a data-driven examination of changes in functional connectivity (FC) during rs-fMRI between before and after an interpersonal anger induction (N = 44 men). Anger was induced based on unfair monetary offers in a previously validated decision-making task. We calculated a common measure of global FC (gFC) which captures the level of FC between each region and all other regions in the brain, and examined which brain regions manifested changes in this measure following anger. We next examined the changes in all functional connections of each individuated brain region with all other brain regions to reveal which connections underlie the differences found in the gFC analysis of the previous step. We subsequently examined the relation of the identified neural modulations in the aftermath of anger with state- and trait- like measures associated with anger, including brain structure, and in a subsample of designated infantry soldiers (N = 21), with levels of traumatic stress symptoms (TSS) measured 1 year later following combat-training. The analysis pipeline revealed an increase in right amygdala gFC in the aftermath of anger and specifically with the right inferior frontal gyrus (IFG).We found that the increase in FC between the right amygdala and right IFG following anger was positively associated with smaller right IFG volume, higher trait-anger level and among soldiers with more TSS. Moreover, higher levels of right amygdala gFC at baseline predicted less reported anger during the subsequent anger provocation. The results suggest that increased amygdala-IFG connectivity following anger is associated with maladaptive recovery, and relates to long-term development of stress symptomatology in a subsample of soldiers.

Highlights

There are various emotion regulation strategies one may recruit to cope with anger, some more adaptive than others
We demonstrated that ventro-medial PFC (vmPFC) activation and posterior insula-medial thalamus connectivity modulated angry feelings leading to increased acceptance of unfair offers and gaining more money throughout the game, providing a neural model for spontaneous anger regulation
Since anger dysregulation and rumination are characteristic of PTSD patients (Michael et al, 2007; Olatunji et al, 2010), we aimed to examined whether the identified rs-functional connectivity (FC) modulations identified in the entire sample at the beginning of their respective programs could be predictive of traumatic stress symptoms (TSS) levels in soldiers towards the end of combat-training, possibly linking neural processes of recovery from anger to later development of stress symptomatology

Summary

Introduction

There are various emotion regulation strategies one may recruit to cope with anger, some more adaptive than others. A few previous studies adopted such an approach in regards to an induced emotional experience, mostly revealing increased neural coupling between prefrontal, limbic and paralimbic brain regions including the medial PFC, amygdala, cingulate and insular cortices, some of which were associated with sustainment of the emotional experience (e.g., Harrison et al, 2008; van Marle et al, 2010; Veer et al, 2011; Schultz et al, 2012; Vaisvaser et al, 2013; Maron-Katz et al, 2016; Clemens et al, 2017). To examine if the identified rs-FC modulations associated with participants’ anger experience and reaction during provocation, we tested whether the identified modulations, either in gFC or in specific connections, corresponded to participants’ self-reported angry feelings and their total monetary gain accumulated throughout the game. We tested the correspondence of both trait-anger and gray matter volume in the same brain regions in which the rs-FC modulations were identified

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