Neural correlates of emotional personality: a structural and functional magnetic resonance imaging study

Abstract

Studies addressing brain correlates of emotional personality have remained sparse, despite the involvement of emotional personality in health and well-being. This study investigates structural and functional brain correlates of psychological and physiological measures related to emotional personality. Psychological measures included neuroticism, extraversion, and agreeableness scores, as assessed using a standard personality questionnaire. As a physiological measure we used a cardiac amplitude signature, the so-called E κ value (computed from the electrocardiogram) which has previously been related to tender emotionality. Questionnaire scores and E κ values were related to both functional (eigenvector centrality mapping, ECM) and structural (voxel-based morphometry, VBM) neuroimaging data. Functional magnetic resonance imaging (fMRI) data were obtained from 22 individuals (12 females) while listening to music (joy, fear, or neutral music). ECM results showed that agreeableness scores correlated with centrality values in the dorsolateral prefrontal cortex, the anterior cingulate cortex, and the ventral striatum (nucleus accumbens). Individuals with higher E κ values (indexing higher tender emotionality) showed higher centrality values in the subiculum of the right hippocampal formation. Structural MRI data from an independent sample of 59 individuals (34 females) showed that neuroticism scores correlated with volume of the left amygdaloid complex. In addition, individuals with higher E κ showed larger gray matter volume in the same portion of the subiculum in which individuals with higher E κ showed higher centrality values. Our results highlight a role of the amygdala in neuroticism. Moreover, they indicate that a cardiac signature related to emotionality (E κ) correlates with both function (increased network centrality) and structure (grey matter volume) of the subiculum of the hippocampal formation, suggesting a role of the hippocampal formation for emotional personality. Results are the first to show personality-related differences using eigenvector centrality mapping, and the first to show structural brain differences for a physiological measure associated with personality.

Figure 1. Modulatory influence of psychological factors on reginal cardiac activity.

(a) From each of n = 81 participants (22 in Experiment 1, and 59 in Experiment 2), NEO scores as well as a 12-lead rest electrocardiogram (ECG) were obtained. (b) From each ECG, absolute values of mean R-, RS-, and T-wave amplitudes were measured electronically (separately for the leads aVL, RIII, and all chest leads), and then computed according to the equation shown in (c), resulting in a single E _κ value for each participant (E _κ is taken to reflect tender emotionality). E _κ values were computed using the absolute amplitude values of the T-wave of aVL (T_aVL), the RS-wave of aVL (RS_aVL), the R-wave of III (R_III) and the maximal RS-wave measured at any of the chest leads (RS_Vmax). For better readability, E _κ values were scaled with a factor of α = 10. (d) Functional magnetic resonance (MR) images were obtained from the participants of Experiment 1, and structural MR images were acquired from the participants of Experiment 2. In Experiment 1, Eigenvector Centrality Maps (ECMs) were computed for each participant. ECMs were then correlated with NEO scores of participants (upper left panel of d), and compared between groups of individuals with higher and lower E _κ values (upper right panel of d). Likewise, structural data obtained in Experiment 2 were correlated with NEO scores (lower left panel of d), and compared between groups of individuals with higher and lower E _κ values (lower right panel of d). The bottom panel illustrates standard ECG leads: The six extremity leads (I, II, III, aVL, aVR, aVF) record voltage differences by means of electrodes placed on the limbs (e). The triangle shows the spatial relationships of the extremity leads, which record electrical voltages onto the frontal plane of the body. The six chest leads (V1–V6) record voltage differences by means of electrodes placed on the chest wall (f). The oval indicates spatial relationships of the six chest leads, which record electrical voltages transmitted onto the horizontal plane.

Box 1. Illustration of procedure and data analysis.

Figure 2. Experiment 1: Functional neuroimaging data (Eigenvector Centrality Mapping).

Results were controlled for age and gender, and corrected for multiple comparisons (p<.05). Images are shown in neurological convention. The upper panel (a) shows results of correlations of Eigenvector Centrality Maps (ECMs) with agreeableness scores. For each participant, one ECM was computed for the entire fMRI session. Positive correlations (shown in red-yellow colours) were found in the posterior superior frontal sulcus bilaterally (upper left image), the ventral striatum/nucleus accumbens (arrows in left upper and lower image), and in the anterior cingulate cortex (lower left image). Negative correlations (shown in blue) were observed in the central sulcus (arrowheads in right image). The bottom panel (b) shows the comparison of ECMs between groups of participants with higher and lower E _κ values. Individuals with higher E _κ (taken to reflect higher tender emotionality) showed higher centrality values in the subiculum of the right hippocampal formation (crosshairs in upper images), in the auditory cortex bilaterally, in both anterior and posterior cingulate cortex (lower left image), the anterior fronto-median cortex (lower left image), and the Rolandic operculum (arrowhead in lower right image). The group with lower E _κ showed higher centrality values in the lateral geniculate body bilaterally (blue clusters in upper left image) as well as in the visual cortex (V1, blue cluster in lower left image).

Figure 3. Experiment 2: Structural neuroimaging data (voxel-based morphometry).

Results were controlled for total brain volume, age and gender, images are shown in neurological convention. The upper panel (a) shows results of the correlations of grey matter volume with neuroticism scores (uncorrected data with a threshold of p<.001 and a minimum cluster size of 10 voxels). The crosshair indicates a positive correlation in the left amygdaloid complex (significant in the region of interest analysis, p<.05, FWE-corrected). The left image shows a coronal section, the right image shows a sagittal section. The middle panel (b) shows the comparison of structural data between groups of participants with higher and lower E _κ values (uncorrected data with a threshold of p<.001 and a minimum cluster size of 10 voxels). A difference between groups was found in the subiculum of the right hippocampal formation (significant in the region of interest analysis, p<.05, FWE-corrected). Gray matter volume was larger in the group of participants with higher E _κ values (taken to reflect higher tender emotionality). Note the consistency with the group difference observed in the left subiculum in the functional data (Figure 2b). The left image shows a coronal section, the right image an axial section. The bottom panel (c) shows the same results as (b), projected on the cytoarchitectonic probability map of the hippocampal formation provided by Amunts et al. using the Anatomy Toolbox provided by Eickhoff et al. . The group difference is located with 90% probability in the subiculum.