Hierarchical Heterogeneity across Human Cortex Shapes Large-Scale Neural Dynamics

The large-scale organization of dynamical neural activity across cortex emerges through long-range interactions among local circuits. We hypothesized that large-scale dynamics are also shaped by heterogeneity of intrinsic local properties across cortical areas. One key axis along which microcircuit properties are specialized relates to hierarchical levels of cortical organization. We developed a large-scale dynamical circuit model of human cortex that incorporates heterogeneity of local synaptic strengths, following a hierarchical axis inferred from magnetic resonance imaging (MRI)-derived T1- to T2-weighted (T1w/T2w) mapping and fit the model using multimodal neuroimaging data. We found that incorporating hierarchical heterogeneity substantially improves the model fit to functional MRI (fMRI)-measured resting-state functional connectivity and captures sensory-association organization of multiple fMRI features. The model predicts hierarchically organized higher-frequency spectral power, which we tested with resting-state magnetoencephalography. These findings suggest circuit-level mechanisms linking spatiotemporal levels of analysis and highlight the importance of local properties and their hierarchical specialization on the large-scale organization of human cortical dynamics. Demirtaş et al. report a large-scale circuit model of human cortex incorporating regional heterogeneity in microcircuit properties using T1w/T2w mapping for parametrization across the cortical hierarchy and fitting models to resting-state functional connectivity. This study shows that hierarchical heterogeneity provides an organizing principle for spatiotemporal dynamics of human cortex.