Atypical Resting-State EEG Graph Metrics of Network Efficiency Across Development in Autism and Their Association with Social Cognition: Results from the LEAP Study.

Abstract

Autism has been associated with differences in functional brain network organization. However, the exact nature of these differences across development compared to non-autistic individuals and their relationship to autism-related social cognition, remains unclear. This study first aimed to identify EEG resting-state network characteristics in autistic versus non-autistic children, adolescents, and adults. Second, we investigated associations with social cognition measures. Analyzing resting-state EEG data from the EU-AIMS Longitudinal European Autism Project, we compared network metrics (global efficiency, clustering coefficient, and small-worldness) between 344 autistic and non-autistic individuals within and across age groups in four frequency bands (delta, theta, alpha, and beta). If significant, we explored their relationships to measures of empathy (empathy quotient), complex emotion recognition [reading the mind in the eyes task (RMET)], and theory of mind (animated shapes task). Compared to their non-autistic peers, autistic adolescents showed lower alpha global efficiency, while autistic adults showed lower alpha clustering and small-worldness. No network differences were observed among children. In adolescents, higher long-range integration was tentatively associated with higher RMET scores; in those with high autistic traits, higher long-range integration related to fewer parent-reported empathic behaviors. No brain-behavior relationships were observed in adults. Our findings suggest subtle differences in network topology between autistic and non-autistic individuals, with less efficient long-range efficiency during adolescence, and less local and overall network efficiency in adulthood. Furthermore, long-range integration may play a role in complex emotion recognition and empathy difficulties associated with autism in adolescence.