Mammals achieve common neural coverage of visual scenes using distinct sampling behaviors

Abstract

Most vertebrates use head and eye movements to quickly change gaze orientation and sample different portions of the environment with periods of stable fixation. Visual information must be integrated across fixations to construct a complete perspective of the visual environment. In concert with this sampling strategy, neurons adapt to unchanging input to conserve energy and ensure that only novel information from each fixation is processed. We demonstrate how adaptation recovery times and saccade properties interact, and thus shape spatiotemporal tradeoffs observed in the motor and visual systems of mice, cats, marmosets, macaques, and humans. These tradeoffs predict that in order to achieve similar visual coverage over time, animals with smaller receptive field sizes require faster saccade rates. Indeed, we find comparable sampling of the visual environment by neuronal populations across mammals when integrating measurements of saccadic behavior with receptive field sizes and V1 neuronal density. We propose that these mammals share a common statistically driven strategy of maintaining coverage of their visual environment over time calibrated to their respective visual system characteristics.Significance StatementMammals rapidly move their eyes to sample their visual environment over successive fixations, but they use different spatial and temporal strategies for this sampling. We demonstrate that these different strategies achieve similar neuronal receptive field coverage over time. Because mammals have distinct sensory receptive field sizes and neuronal densities for sampling and processing information, they require different eye movement strategies to encode natural scenes.