Abstract
Small fly eyes should not see fine image details. Because flies exhibit saccadic visual behaviors and their compound eyes have relatively few ommatidia (sampling points), their photoreceptors would be expected to generate blurry and coarse retinal images of the world. Here we demonstrate that Drosophila see the world far better than predicted from the classic theories. By using electrophysiological, optical and behavioral assays, we found that R1-R6 photoreceptors' encoding capacity in time is maximized to fast high-contrast bursts, which resemble their light input during saccadic behaviors. Whilst over space, R1-R6s resolve moving objects at saccadic speeds beyond the predicted motion-blur-limit. Our results show how refractory phototransduction and rapid photomechanical photoreceptor contractions jointly sharpen retinal images of moving objects in space-time, enabling hyperacute vision, and explain how such microsaccadic information sampling exceeds the compound eyes' optical limits. These discoveries elucidate how acuity depends upon photoreceptor function and eye movements.
Highlights
The acuity of an eye is limited by its photoreceptor spacing, which provides the grain of the retinal image
Because each photoreceptor’s signal-to-noise ratio and receptive field size adapt dynamically to light changes, acuity depends upon the eye movements that cause them
To make these relationships clear, the results are presented in the following order: 1. We show that photoreceptors capture most visual information from high-contrast bursts, and reveal how this is achieved by refractory photon sampling and connectivity (Figures 1–5)
Summary
The acuity of an eye is limited by its photoreceptor spacing, which provides the grain of the retinal image. To resolve two moving objects is harder, as vision becomes further limited by each photoreceptor’s finite integration time and receptive field size (Srinivasan and Bernard, 1975; Juusola and French, 1997; Land, 1997). Animals - from insects to man - view the world by using saccades, fast movements, which direct their eyes to the surroundings, and fixation intervals between the saccades, during which gaze is held near stationary (Land, 1999). Information would be captured during fixations whilst during saccades animals would be effectively blind. This viewpoint, ignores fast photoreceptor adaptation, which causes perceptual fading during fixation (Ditchburn and Ginsborg, 1952; Riggs and Ratliff, 1952), reducing visual information and possibly rendering perception to mean light only. To maximize information and acuity, it is plausible that evolution has optimized photoreceptor function in respect to visual behaviors and needs
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