Activation/suppression balances in rat Superior Colliculus encode the visual continuity illusion

Abstract

When visual stimuli are presented at a sufficiently high temporal frequency, visual perception shifts from the static to dynamic vision mode, thereby facilitating a continuity illusion which is key for correctly identifying continuous and moving objects and placing them in the context of the surrounding environment. However, how this continuity illusion is encoded along the entire visual pathway remains poorly understood, with disparate Flicker Fusion Frequency (FFF) thresholds measured at retinal, cortical, and behavioural levels. Here, we hypothesized that these disparities may suggest that other brain areas may be involved in encoding the shift from static to dynamic vision modes. We employ a comprehensive approach encompassing behavioural measurements, whole brain activation mapping with high fidelity functional MRI (fMRI), and local electrophysiological validation for studying the mechanisms underlying the shift from static to dynamic vision modes in the rat. Our behavioural measurements reported an FFF threshold proxy of 18{+/-}2 Hz. At the network level, functional MRI revealed that the superior colliculus (SC) exhibits marked signal transitions from positive to negative fMRI signal regimes at the behaviourally measured FFF threshold surrogates, with a strong linear correlation between fMRI signal and behaviour, while thalamic and cortical visual areas displayed a significantly poorer correlation with the behaviour. fMRI-driven neurometric curves approximated the behavioural psychometric curve in SC but not in the other visual areas. Electrophysiological recordings in SC suggested that these fMRI signals transitions arise from strong neural activation/suppression at low/high frequency regimes, respectively, and that a transition between these regimes occurs around the measured FFF threshold proxies. Lesions in V1 further reinforced that these transitions originate in SC. Combined, our data suggests a critical role for SC in encoding temporal frequency discriminations, in particular the shifts from the static to the dynamic vision modes.