Peripheral-to-foveal cortico-collicular processing of visual information across eye movements

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Saccadic eye movements cause substantial visual uncertainty due to the rapidity with which they translate images of the environment across the retina. Moreover, because a large portion of the visual system is organized retinotopically, every time a saccade occurs, neurons representing the foveal retinal image region in multiple brain areas experience a different post-saccadic scene portion than the scene portion that they experience before eye movement onset. This, coupled with the fact that post-saccadic sensory input arrives well after eye movement onset (due to long afferent processing delays and strong motion blur caused by saccades), suggests a need for a mechanism to bridge trans-saccadic visual processing. Such bridging needs to happen both in time (across saccade duration) as well as in space (linking a retinotopically peripheral pre-saccadic image of the eye movement target to a foveal post-saccadic version of it). Trans-saccadic peripheral-to-foveal transfer of visual information between different retinotopically organized populations of neurons could be a means to realize exactly such a bridge, and perceptual evidence for this transfer exists. In this project, we will unravel the cortical and subcortical mechanisms associated with trans-saccadic peripheral-to-foveal transfer of visual information. We will demonstrate that there is a predictive remapping of peripheral visual feature information of a stable saccade target to foveal visual representations in both the superior colliculus (SC) and primary visual cortex (V1). We will also causally demonstrate that such remapping can be jumpstarted in the SC motor bursts themselves (which are known to drive eye movements via downstream projections to brainstem and cerebellar motor control nuclei). This jumpstarting happens via embedding a sensory-tuned signal in the SC motor bursts, meaning that saccade commands in the SC simultaneously also represent the visual appearance of peripheral saccade targets. We argue that endowing SC motor bursts with such a sensory tuning signal allows the SC to provide visual areas with a peripheral scene preview for bridging perception; that is, because SC motor bursts are temporally coincident with saccades, the scene preview embedded in them is available exactly when vision (via sensory afference) is most uncertain (intra-saccadically). Finally, because the SC has ascending feedback projections to the cortex, we will investigate whether the SC’s sensory-tuned motor burst activity is critical for trans-saccadic remapping of visual features to the fovea at the cortical level, or whether cortico-cortical interactions (perhaps via area V4) are sufficient. Our experiments will reveal highly novel mechanistic insights on peripheral-to-foveal cortico-collicular processing of visual information across eye movements.