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Sex-dependent correlations between the personality dimension of harm avoidance and the resting-state functional connectivity of amygdala subregions.

ABSTRACT: Harm avoidance (HA) is a personality dimension involving the tendency to respond intensely to signals of aversive stimuli. Many previous neuroimaging studies have associated HA scores with the structural and functional organization of the amygdala, but none of these studies have evaluated the correlation between HA score and amygdala resting-state functional connectivity (rsFC). Moreover, the amygdala is not a homogeneous structure, and it has been divided into several structurally and functionally distinct subregions. Investigating the associations between HA score and properties of subregions of the amygdala could greatly improve our understanding of HA. In the present study, using a large sample of 291 healthy young adults, we aimed to uncover correlations between HA scores and the rsFCs of each amygdala subregion and to uncover possible sex-based differences in these correlations. We found that subregions of the amygdala showed different rsFC patterns, which contributed differently to individual HA scores. More specifically, HA scores were correlated with rsFCs between the laterobasal amygdala subregion and temporal and occipital cortices related to emotional information input, between the centromedial subregion and the frontal cortices associated with emotional output control, and between the superficial subregion and the frontal and temporal areas involved in both functions. Moreover, significant gender-based differences were uncovered in these correlations. Our findings provide a more detailed model of association between HA scores and amygdala rsFC, extend our understanding of the connectivity of subregions of the amygdala, and confirm sex-based differences in HA associations.

SUBMITTER: Li Y

PROVIDER: S-EPMC3338761 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Sex-dependent correlations between the personality dimension of harm avoidance and the resting-state functional connectivity of amygdala subregions.

Li Ying Y Qin Wen W Jiang Tianzi T Zhang Yunting Y Yu Chunshui C

PloS one 20120427 4

Harm avoidance (HA) is a personality dimension involving the tendency to respond intensely to signals of aversive stimuli. Many previous neuroimaging studies have associated HA scores with the structural and functional organization of the amygdala, but none of these studies have evaluated the correlation between HA score and amygdala resting-state functional connectivity (rsFC). Moreover, the amygdala is not a homogeneous structure, and it has been divided into several structurally and functiona ...[more]

PMID: 22558274

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Project description:Personality neuroscience aims to find associations between brain measures and personality traits. Findings to date have been severely limited by a number of factors, including small sample size and omission of out-of-sample prediction. We capitalized on the recent availability of a large database, together with the emergence of specific criteria for best practices in neuroimaging studies of individual differences. We analyzed resting-state functional magnetic resonance imaging data from 884 young healthy adults in the Human Connectome Project (HCP) database. We attempted to predict personality traits from the "Big Five", as assessed with the NEO-FFI test, using individual functional connectivity matrices. After regressing out potential confounds (such as age, sex, handedness and fluid intelligence), we used a cross-validated framework, together with test-retest replication (across two sessions of resting-state fMRI for each subject), to quantify how well the neuroimaging data could predict each of the five personality factors. We tested three different (published) denoising strategies for the fMRI data, two inter-subject alignment and brain parcellation schemes, and three different linear models for prediction. As measurement noise is known to moderate statistical relationships, we performed final prediction analyses using average connectivity across both imaging sessions (1 h of data), with the analysis pipeline that yielded the highest predictability overall. Across all results (test/retest; 3 denoising strategies; 2 alignment schemes; 3 models), Openness to experience emerged as the only reliably predicted personality factor. Using the full hour of resting-state data and the best pipeline, we could predict Openness to experience (NEOFAC_O: r=0.24, R2=0.024) almost as well as we could predict the score on a 24-item intelligence test (PMAT24_A_CR: r=0.26, R2=0.044). Other factors (Extraversion, Neuroticism, Agreeableness and Conscientiousness) yielded weaker predictions across results that were not statistically significant under permutation testing. We also derived two superordinate personality factors ("α" and "β") from a principal components analysis of the NEO-FFI factor scores, thereby reducing noise and enhancing the precision of these measures of personality. We could account for 5% of the variance in the β superordinate factor (r=0.27, R2=0.050), which loads highly on Openness to experience. We conclude with a discussion of the potential for predicting personality from neuroimaging data and make specific recommendations for the field.

Project description:During adolescence, considerable social and biological changes occur that interact with functional brain maturation, some of which are sex-specific. The amygdala is one brain area that has displayed sexual dimorphism, specifically in socio-affective (superficial amygdala [SFA]), stress (centromedial amygdala [CMA]), and learning and memory (basolateral amygdala [BLA]) processing. The amygdala has also been implicated in mood and anxiety disorders which display sex-specific features, most prominently observed during adolescence. Using functional magnetic resonance imaging (fMRI), the present study examined the interaction of age and sex on resting state functional connectivity (RSFC) of amygdala sub-regions, BLA and SFA, in a sample of healthy adolescents between the ages 10 and 16 years (n = 122, 71 boys). Whole-brain, voxel-wise partial correlation analyses were conducted to determine RSFC of bilateral BLA and SFA seed regions, created using the Eickhoff-Zilles maximum probability maps based on cytoarchitectonic mapping and FMRIB's Integrated Registration and Segmentation Tool (FIRST). Monte Carlo simulation was implemented to correct for multiple comparisons (threshold of 53 contiguous voxels with a z-value ? 2.25). Results indicated that with increasing age, there was a corresponding decrease in RSFC between both amygdala sub-regions and parieto-occipital cortices, with a concurrent increase in RSFC with medial prefrontal cortex (mPFC). Specifically, boys and girls demonstrated increased coupling of mPFC and left and right SFA with age, respectively; however, neither sex showed increased connectivity between mPFC and BLA, which could indicate relative immaturity of fronto-limbic networks that is similar across sex. A dissociation in connectivity between BLA- and SFA-parieto-occipital RSFC emerged, in which girls had weaker negative RSFC between SFA and parieto-occipital regions and boys had weaker negative RSFC of BLA and parieto-occipital regions with increased age, both standing in contrast to adult patterns of amygdala sub-regional RSFC. The present findings suggest relative immaturity of amygdala sub-regional RSFC with parieto-occipital cortices during adolescence, with unique patterns in both sexes that may support memory and socio-affective processing in boys and girls, respectively. Understanding the underlying normative functional architecture of brain networks associated with the amygdala during adolescence may better inform future research of the neural features associated with increased risk for internalizing psychopathology.

Project description:IMPORTANCE:Major depressive disorder (MDD) frequently emerges during adolescence and can lead to persistent illness, disability, and suicide. The maturational changes that take place in the brain during adolescence underscore the importance of examining neurobiological mechanisms during this time of early illness. However, neural mechanisms of depression in adolescents have been understudied. Research has implicated the amygdala in emotion processing in mood disorders, and adult depression studies have suggested amygdala-frontal connectivity deficits. Resting-state functional magnetic resonance imaging is an advanced tool that can be used to probe neural networks and identify brain-behavior relationships. OBJECTIVE:To examine amygdala resting-state functional connectivity (RSFC) in adolescents with and without MDD using resting-state functional magnetic resonance imaging as well as how amygdala RSFC relates to a broad range of symptom dimensions. DESIGN, SETTING, AND PARTICIPANTS:A cross-sectional resting-state functional magnetic resonance imaging study was conducted within a depression research program at an academic medical center. Participants included 41 adolescents and young adults aged 12 to 19 years with MDD and 29 healthy adolescents (frequency matched on age and sex) with no psychiatric diagnoses. MAIN OUTCOMES AND MEASURES:Using a whole-brain functional connectivity approach, we examined the correlation of spontaneous fluctuation of the blood oxygen level-dependent signal of each voxel in the whole brain with that of the amygdala. RESULTS:Adolescents with MDD showed lower positive RSFC between the amygdala and hippocampus, parahippocampus, and brainstem (z >2.3, corrected P < .05); this connectivity was inversely correlated with general depression (R?=?-.523, P?=?.01), dysphoria (R?=?-.455, P?=?.05), and lassitude (R?=?-.449, P?=?.05) and was positively correlated with well-being (R?=?.470, P?=?.03). Patients also demonstrated greater (positive) amygdala-precuneus RSFC (z >2.3, corrected P < .05) in contrast to negative amygdala-precuneus RSFC in the adolescents serving as controls. CONCLUSIONS AND RELEVANCE:Impaired amygdala-hippocampal/brainstem and amygdala-precuneus RSFC have not previously been highlighted in depression and may be unique to adolescent MDD. These circuits are important for different aspects of memory and self-processing and for modulation of physiologic responses to emotion. The findings suggest potential mechanisms underlying both mood and vegetative symptoms, potentially via impaired processing of memories and visceral signals that spontaneously arise during rest, contributing to the persistent symptoms experienced by adolescents with depression.

Dataset Information

Sex-dependent correlations between the personality dimension of harm avoidance and the resting-state functional connectivity of amygdala subregions.

Publications

Sex-dependent correlations between the personality dimension of harm avoidance and the resting-state functional connectivity of amygdala subregions.

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