Autism spectrum disorder (ASD) is characterized by differences in social communication and interaction, alongside restricted and repetitive behaviors. The hypothesis that ASD is associated with an altered cortical excitation-inhibition (EI) balance has been the subject of extensive investigations, yet the evidence supporting it remains mixed. A key challenge in testing this hypothesis is that the EI balance also changes substantially during typical maturation, from childhood through adolescence and into early adulthood. We used resting-state magnetoencephalography (MEG) recordings to examine the developmental trajectory of cortical EI alterations, with regional specificity, in a large cross-sectional cohort (N = 172), comprised of 92 typically developing (TD) individuals and 80 individuals diagnosed with ASD, spanning ages 6-32. To that end, functional EI (fEI), derived from critical brain dynamics, was estimated across 500 cortical parcellations in cortical space. Group-averaged fEI maps revealed broadly similar large-scale topographic patterns in the TD and ASD groups when averaged across all ages. When divided by age into childhood (6-12 years, N ASD = 18, N TD = 16), adolescence (13-18 years, N ASD = 27, N TD = 41) and adulthood (19-32 years, N ASD = 28, N TD = 26), we found an overall pattern of increased global fEI in childhood and decreased fEI in adolescence in the ASD group, with no evidence of a difference between groups in fEI in adulthood. Additional parcel-wise regression analyses identified a significant main effect of diagnostic group, independent of age, in the right dorsolateral prefrontal cortex, where TD individuals showed higher fEI than those with ASD across all ages. Furthermore, a significant group-by-age interaction was observed in the left inferior parietal cortex, where we found evidence that fEI increased with age in TD individuals (beta = 0.012, p = 0.006) but no evidence of a similar age-dependent increase in those with ASD (beta = 0.001, p = 0.84), indicating diverging developmental trajectories. Finally, fEI in paracentral and precuneus cortical regions was associated with ASD symptom severity. Together, these findings support a scenario in which EI imbalance, as assessed with fEI, is not globally distributed in ASD, and is not static through development, but is instead expressed through regionally and developmentally specific differences, with implications for understanding the neural substrates of ASD phenotypic heterogeneity.
Osorio, S., Tan, J., Khan, S., Ahlfors, S. P., Mamashli, F., Alho, J., Joseph, R. M., Levine, G., Graham, S., Joshi, G., Nayal, Z., McGuiggan, N. M., Losh, A., Pawlyszyn, S., Mercaldo, N., Hamalainen, M. S., Kenet, T.
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