Is neuroticism really bad for you? Dynamics in personality and limbic reactivity prior to, during and following real-life combat stress

Noa Magal, Talma Hendler, Roee Admon

Research output: Contribution to journalArticlepeer-review

Abstract

The personality trait of neuroticism is considered a risk factor for stress vulnerability, putatively via its association with elevated limbic reactivity. Nevertheless, majority of evidence to date that relates neuroticism, neural reactivity and stress vulnerability stems from cross-sectional studies conducted in a “stress-free” environment. Here, using a unique prospective longitudinal design, we assessed personality, stress-related symptoms and neural reactivity at three time points over the course of four and a half years; accounting for prior to, during, and long-time following a stressful military service that included active combat. Results revealed that despite exposure to multiple potentiality traumatic events, majority of soldiers exhibited none-to-mild levels of posttraumatic and depressive symptoms during and following their military service. In contrast, a quadratic pattern of change in personality emerged overtime, with neuroticism being the only personality trait to increase during stressful military service and subsequently decrease following discharge. Elevated neuroticism during military service was associated with reduced amygdala and hippocampus activation in response to stress-related content, and this association was also reversed following discharge. A similar pattern was found between neuroticism and hippocampus-anterior cingulate cortex (ACC) functional connectivity in response to stress-related content. Taken together these findings suggest that stressful military service at young adulthood may yield a temporary increase in neuroticism mediated by a temporary decrease in limbic reactivity, with both effects being reversed long-time following discharge. Considering that participants exhibited low levels of stress-related symptoms throughout the study period, these dynamic patterns may depict behavioral and neural mechanisms that facilitate stress resilience.

Original languageEnglish
Article number100361
JournalNeurobiology of Stress
Volume15
DOIs
StatePublished - Nov 2021

Bibliographical note

Funding Information:
Compared to the wealth of longitudinal behavioral studies on neuroticism, as reviewed above, neuroimaging literature on neuroticism mostly relied on cross-sectional designs. Majority of studies associated elevated neuroticism with increased reactivity to negatively charged stimuli in limbic brain regions, particularly the hippocampus, amygdala, and anterior cingulate cortex (ACC) (Allen and DeYoung, 2016; Brown et al., 2020; Canli, 2008; Chan et al., 2009; Cunningham et al., 2011; Haas et al., 2007; Hyde et al., 2011; Ormel et al., 2013; Schuyler et al., 2014; Servaas et al., 2013). Though other studies did not find such associations (Bruhl et al., 2011; Cremers et al., 2010; Drabant et al., 2009; Neumann, 2020; Silverman et al., 2019; Thomas et al., 2011). Studies assessing the association between neuroticism scores and functional connectivity patterns also yielded mixed findings, including increased (Cremers et al., 2010) and decreased (Yang et al., 2020) connectivity of the amygdala with the dorsomedial prefrontal (dmPFC), as well as increased amygdala connectivity with the ventromedial prefrontal cortex (vmPFC) (Silverman et al., 2019) and decreased connectivity with the ACC (Cremers et al., 2010; Deng et al., 2019). Additional support for the putative role of the ACC in neuroticism, particularly its dorsal part (dACC), stems from a recent meta-analysis demonstrating a positive relationship between dACC gray matter volume and neuroticism scores among healthy adults (Liu et al., 2021). Taken together, neuroimaging literature highlighted the amygdala, hippocampus, and ACC as neural structures that may relate to neuroticism scores, though multiple inconsistences emerged, potentially implying that the association between neuroticism and limbic reactivity is dynamic and context dependent (Servaas et al., 2013). In support of that, using a within-subject design it was recently demonstrated that neuroticism scores are associated with selectively enhanced amygdala response to fearful faces under stress, but not in stress-free conditions (Everaerd et al., 2015). Longitudinal investigation of the relations between neuroticism and neural reactivity is still missing. Accordingly, it is unclear whether stress-induced dynamics in neuroticism are associated with changes in limbic activation and functional connectivity patterns during stress as well as long-time following its offset.This work was supported by the Brain & Behavior Research Foundation (Formerly NARSAD) Young Investigator Award (Grant ID: 25993) awarded to R.A. The study sponsor had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Funding Information:
This work was supported by the Brain & Behavior Research Foundation (Formerly NARSAD ) Young Investigator Award (Grant ID: 25993) awarded to R.A. The study sponsor had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Publisher Copyright:
© 2021 The Authors

Keywords

  • Amygdala
  • Anterior Cingulate Cortex
  • Hippocampus
  • Longitudinal
  • Neuroticism
  • Personality
  • Resilience
  • Stress
  • fMRI

ASJC Scopus subject areas

  • Biochemistry
  • Physiology
  • Molecular Biology
  • Endocrinology
  • Endocrine and Autonomic Systems
  • Cellular and Molecular Neuroscience

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