Neural Activity while Imitating Emotional Faces is Related to Both Lower and Higher-Level Social Cognitive Performance

Colin Hawco,Aristotle N Voineskos,Anil K Malhotra,Marco Iacoboni,Anthony R Mcintosh,Natasa Kovacevic,Joseph D Viviano,Robert W Buchanan

doi:10.1038/s41598-017-01316-z

Abstract

Imitation and observation of actions and facial emotional expressions activates the human fronto-parietal mirror network. There is skepticism regarding the role of this low-level network in more complex high-level social behaviour. We sought to test whether neural activation during an observation/imitation task was related to both lower and higher level social cognition. We employed an established observe/imitate task of emotional faces during functional MRI in 28 healthy adults, with final analyses based on 20 individuals following extensive quality control. Partial least squares (PLS) identified patterns of relationships between spatial activation and a battery of objective out-of-scanner assessments that index lower and higher-level social cognitive performance, including the Penn emotion recognition task, reading the mind in the eyes, the awareness of social inference test (TASIT) parts 1, 2, and 3, and the relationships across domains (RAD) test. Strikingly, activity in limbic, right inferior frontal, and inferior parietal areas during imitation of emotional faces correlated with performance on emotion evaluation (TASIT1), social inference - minimal (TASIT2), social inference - enriched (TASIT3), and the RAD tests. These results show a role for this network in both lower-level and higher-level social cognitive processes which are collectively critical for social functioning in everyday life.

Highlights

Most neuroimaging studies examining the lateral fronto-parietal network have made use of hand actions or other forms of simple motor stimuli[9]
latent variables (LVs) 2 shows a large amount of overlap with LV 1, suggesting some of the variance within those regions is explained by aspects of both LVs 1 and 2
The majority of the variance explained by LV 1, but some additional variance within those voxels is explained by the pattern of emotional faces >neutral and fixation in Imitate and increased activity in fixation trials for Observe, as seen in LV 2

Summary

Introduction

Most neuroimaging studies examining the lateral fronto-parietal network have made use of hand actions or other forms of simple motor stimuli[9]. Some have taken the concept of mirroring one step further, by arguing that the lateral fronto-parietal network is important for emotional empathy by permitting humans to feel what others feel, and potentially to assess or interpret emotional cues and social behaviour[10,11,12] Investigating this issue may be best served by paradigms utilizing socially relevant stimuli as opposed to simple motor acts. Recent work has shown structural changes in right fronto-parietal cortex in more socially impaired people with schizophrenia[18, 19], a group of individuals in whom higher-level social cognitive processes such as theory of mind are more prominently affected[20] These findings raise the question of whether neural activation during basic mirroring tasks is related to higher-level social cognitive abilities. We hypothesized that a) consistent with previous studies, imitating emotional faces would activate the mirroring network, more prominently in the imitate than the observe condition, and b) neural activity during imitation of emotional faces (rather than imitating neutral faces or observing faces) would be associated with both lower-level and higher-level social cognitive performance

Objectives

Methods

Results

Conclusion