Predictive coding of natural images by V1 firing rates and rhythmic synchronization

Predictive coding is an important candidate theory of self-supervised learning in the brain. Its central idea is that sensory responses result from comparisons between bottom-up inputs and contextual predictions, a process in which rates and synchronization may play distinct roles. We recorded from awake macaque V1 and developed a technique to quantify stimulus predictability for natural images based on self-supervised, generative neural networks. We find that neuronal firing rates were mainly modulated by the contextual predictability of higher-order image features, which correlated strongly with human perceptual similarity judgments. By contrast, V1 gamma (γ)-synchronization increased monotonically with the contextual predictability of low-level image features and emerged exclusively for larger stimuli. Consequently, γ-synchronization was induced by natural images that are highly compressible and low-dimensional. Natural stimuli with low predictability induced prominent, late-onset beta (β)-synchronization, likely reflecting cortical feedback. Our findings reveal distinct roles of synchronization and firing rates in the predictive coding of natural images.