Movie features are hierarchically encoded in the dynamics of functional connectivity

The perception of the external environment relies on a cascade of neural computations in the visual cortex, where stimulus features are represented hierarchically. These features can be extracted through Convolutional neural networks (CNN) from naturalistic stimuli. Neuroimaging studies showed that these are processed along the dorsal and ventral visual streams and linked a gradient of increasing complexity to sequential activations and reorganization of cortical interactions. Spectrally, in the alpha and beta bands, Magnetoencephalography revealed that natural viewing induced a reduction in the amplitude of functional connectivity and a maintenance of topography at rest. However, the impact of specific stimulus features on functional connectivity remains unclear. To address this gap, we acquired MEG data on 12 subjects (5 female) during movie watching and used CNN to track the dynamics of movie features. Then, we compared the temporal dynamics of CNN layers with changes in functional connectivity in the alpha and beta bands. Our findings show that feature encoding in functional connectivity relates to a complex temporal, spectral, and topological organization. In both bands, increasing stimulus complexity involved a higher number of connections and longer temporal delays between stimulus and the connectivity dynamics. Moreover, as complexity increased, we observed a shift in the involvement of connector hubs from low-level nodes to high-level ones in the visual network. Finally, a spectral dissociation emerged: the alpha band primarily encoded mid-level features, while the beta band encoded higher-level ones.Significance statement The brain's perception of external stimuli is typically investigated through encoding models of the visual system, focusing on functional activations and sequential recruitment of visual regions. However, much less is known about how stimulus features shape brain communication. To address this gap, we combined Magnetoencephalography with convolutional neural network (CNN) to characterize how movie watching shapes the dynamics and topology of functional brain connectivity. We found that the connectivity dynamics aligned with the temporal evolution of the stimulus in the alpha and beta bands. Increasing stimulus complexity was associated with a greater number of connections, longer temporal delays between stimulus and connectivity dynamics, and a shift in the involvement of connector hubs from low-level to high-level regions.