Abstract

Face expressions are a rich source of social signals. Here we estimated the proportion of phenotypic variance in the brain response to facial expressions explained by common genetic variance captured by ∼500,000 single nucleotide polymorphisms. Using genomic-relationship-matrix restricted maximum likelihood (GREML), we related this global genetic variance to that in the brain response to facial expressions, as assessed with functional magnetic resonance imaging (fMRI) in a community-based sample of adolescents (n = 1,620). Brain response to facial expressions was measured in 25 regions constituting a face network, as defined previously. In 9 out of these 25 regions, common genetic variance explained a significant proportion of phenotypic variance (40–50%) in their response to ambiguous facial expressions; this was not the case for angry facial expressions. Across the network, the strength of the genotype-phenotype relationship varied as a function of the inter-individual variability in the number of functional connections possessed by a given region (R2 = 0.38, p<0.001). Furthermore, this variability showed an inverted U relationship with both the number of observed connections (R2 = 0.48, p<0.001) and the magnitude of brain response (R2 = 0.32, p<0.001). Thus, a significant proportion of the brain response to facial expressions is predicted by common genetic variance in a subset of regions constituting the face network. These regions show the highest inter-individual variability in the number of connections with other network nodes, suggesting that the genetic model captures variations across the adolescent brains in co-opting these regions into the face network.

Highlights

  • Interactions with peers are of high relevance to our mental health

  • In a subset of brain regions, we explained 40–50% of phenotypic variance by genetic variance. These brain regions appear to differ from the rest of the face network in the degree of inter-individual variations in their functional connectivity

  • We propose that these regions, including the prefrontal and premotor cortex, represent ‘‘Optional’’ part of the network co-opted by its ‘‘Obligatory’’ members, including the posterior part of the superior temporal sulcus, fusiform face area and the lateral occipital cortex, concerned with processing complex visual stimuli

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Summary

Introduction

Interactions with peers are of high relevance to our mental health. Patients with various psychological disorders show impairments in face perception and emotion recognition [1,2,3,4]. Differential neural responses to faces have been reported in various psychological disorders including depression [5], psychopathy and/or aggressive tendencies [6], autism [7], and schizophrenia [8]. Our ability to process faces is modulated by both environment and genes. Zhu and colleagues observed that inter-individual variations in face perception are heritable, with

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