Action Observation Network activity related to object-directed and socially directed actions in Adolescents

Abstract

The Action Observation Network (AON) encompasses brain areas consistently engaged when we observe others actions. Although the core nodes of the AON are present from childhood, it is not known to what extent they are sensitive to different action features during development. As social cognitive abilities continue to mature during adolescence, the AON response to socially-oriented actions, but not to object-related actions, may differ in adolescents and adults. To test this hypothesis, we scanned with functional magnetic resonance imaging (fMRI) 28 typically-developing teenagers and 25 adults while they passively watched videos of hand actions varying along two dimensions: sociality (i.e. directed towards another person or not) and transitivity (i.e. involving an object or not). We found that observing actions recruited the same fronto-parietal and occipito-temporal regions in adults and adolescents. The modulation of voxelwise activity by the social or transitive nature of the action was similar in both groups of participants. Multivariate pattern analysis, however, revealed that the accuracy in decoding the social dimension from the brain activity patterns, increased with age in lateral occipital and parietal regions, known to be involved in semantic representations of actions, as well as in posterior superior temporal sulcus, a region commonly associated with perception of high level features necessary for social perception. Change in decoding the transitive dimension was observed only in the latter region. These findings indicate that the representation of others actions, and in particular their social dimensions, in the adolescent AON is still not as robust as in adults. Significance statementThe activity of the action observation network in the human brain is modulated according to the purpose of the observed action, in particular the extent to which it involves interaction with an object or another person. How this conceptual representation of actions is implemented during development is largely unknown. Here, using multivoxel pattern analysis of fMRI data, we discovered that, while the action observation network is in place in adolescence, the fine-grain organization of its posterior regions is less robust than in adults to decode the social or transitive dimensions of an action. This finding highlights the late maturation of social processing in the human brain.