A conserved node degree-based backbone and flexible hub organization of brain connectome underlying naturalistic movie watching

Abstract

How does the brain organize and transmit information during naturalistic conditions? Using large-scale movie-watching fMRI data spanning 14 diverse clips, validated in an independent dataset, we revealed a degree-based dual architecture of the functional connectome under naturalistic stimuli. During movie watching, the brain consistently expresses a conserved network backbone characterized by persistently high node degree in temporal and occipital sensory cortices and parietal association regions, whereas anterior higher-order cognitive regions show relatively lower node degree and substantially greater variability across different clips. We further found that this backbone links brain network organizational patterns to stimulus features of the clips, particularly audiovisual features capturing human presence and social communication. Within this backbone, subregions in superior temporal gyrus (STG), temporo-parieto-occipital junction (TPOJ), precuneus/posterior cingulate cortex, intraparietal sulcus (IPS), dorsal/ventral visual stream (DVS/VVS), and middle temporal visual and motion-sensitive areas (MT+) frequently emerge as connetome hubs, statistically mediating associations between multiple stimulus features and the integration of distinct large-scale functional systems. This study demonstrated a mechanistic framework in which movie watching relies on a conserved network backbone for stable large-scale integration, alongside stimulus-dependent rich-club hubs that flexibly mediate naturalistic information across distributed cortical systems.