Oxytocin receptor polymorphism and childhood social experiences shape adult personality, brain structure and neural correlates of mentalizing.

INTRODUCTION: The oxytocin system is involved in human social behavior and social cognition such as attachment, emotion recognition and mentalizing (i.e. the ability to represent mental states of oneself and others). It is shaped by social experiences in early life, especially by parent-infant interactions. The single nucleotid polymorphism rs53576 in the oxytocin receptor (OXTR) gene has been linked to social behavioral phenotypes. METHOD: In 195 adult healthy subjects we investigated the interaction of OXTR rs53576 and childhood attachment security (CAS) on the personality traits "adult attachment style" and "alexithymia" (i.e. emotional self-awareness), on brain structure (voxel-based morphometry) and neural activation (fMRI) during an interactive mentalizing paradigm (prisoner's dilemma game; subgroup: n=163). RESULTS: We found that in GG-homozygotes, but not in A-allele carriers, insecure childhood attachment is - in adulthood - associated with a) higher attachment-related anxiety and alexithymia, b) higher brain gray matter volume of left amygdala and lower volumes in right superior parietal lobule (SPL), left temporal pole (TP), and bilateral frontal regions, and c) higher mentalizing-related neural activity in bilateral TP and precunei, and right middle and superior frontal gyri. Interaction effects of genotype and CAS on brain volume and/or function were associated with individual differences in alexithymia and attachment-related anxiety. Interactive effects were in part sexually dimorphic. CONCLUSION: The interaction of OXTR genotype and CAS modulates adult personality as well as brain structure and function of areas implicated in salience processing and mentalizing. Rs53576 GG-homozygotes are partially more susceptible to childhood attachment experiences than A-allele carriers.

A voxel-based morphometry study on adult attachment style and affective loss.

The successful recovery from affective loss (i.e., bereavement, relationship breakup) has been linked to adult attachment style (AAS), a personality trait. Up to now, the association between AAS, affective loss experiences and brain gray matter volume is unclear. In 192 healthy subjects we investigated the association between MRI brain gray matter volume, applying voxel based morphometry, AAS (Relationship Scales Questionnaire (RSQ), subscales "avoidance" (AV) and "anxiety" (ANX)), and number of affective losses within the last 5 years (AL; List of Threatening Experiences Questionnaire). In a whole-brain analysis (p < 0.05 FWE-corrected) ANX compared to AV was significantly more positively associated with brain gray matter volume in the left insula and in the pars opercularis of left inferior frontal gyrus. In additional region-of-interest (ROI) analyses (p < 0.05 FWE-corrected), based on previously reported findings, no significant associations were observed. ANX and AV differently correlate with local volumes of the left insula and pars opercularis of the left inferior frontal gyrus, which are implicated in emotion processing, empathy and emotion regulation among other functions. Our results support the notion that individual attachment styles, which develop in the interplay of genes and social environment, differ in their correlation with brain structure.

Adult attachment style modulates neural responses in a mentalizing task.

Adult attachment style (AAS) is a personality trait that affects social cognition. Behavioral data suggest that AAS influences mentalizing proficiency, i.e. the ability to predict and explain people's behavior with reference to mental states, but the neural correlates are unknown. We here tested how the AAS dimensions "avoidance" (AV) and "anxiety" (ANX) modulate neural correlates of mentalizing. We measured brain activation using functional magnetic resonance imaging (fMRI) in 164 healthy subjects during an interactive mentalizing paradigm (Prisoner's Dilemma Game). AAS was assessed with the Relationship Scales Questionnaire, including the subscales AV and ANX. Our task elicited a strong activation of the mentalizing network, including bilateral precuneus, (anterior, middle, and posterior) cingulate cortices, temporal poles, inferior frontal gyri (IFG), temporoparietal junctions, superior medial frontal gyri as well as right medial orbital frontal gyrus, superior temporal gyrus, middle frontal gyrus (MFG), and amygdala. We found that AV is positively and ANX negatively correlated with task-associated neural activity in the right amygdala, MFG, midcingulate cortex, and superior parietal lobule, and in bilateral IFG. These data suggest that avoidantly attached adults activate brain areas implicated in emotion regulation and cognitive control to a larger extent than anxiously attached individuals during mentalizing.