Microsaccadic sampling of moving image information provides Drosophila hyperacute vision.
Microsaccadic sampling of moving image information provides Drosophila hyperacute vision.
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DOI:
10.7554/elife.26117
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发表时间:
2017-09-05
期刊:
影响因子:
7.7
通讯作者:
Takalo J
中科院分区:
文献类型:
--
作者:
Juusola M;Dau A;Song Z;Solanki N;Rien D;Jaciuch D;Dongre SA;Blanchard F;de Polavieja GG;Hardie RC;Takalo J
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. Fruit flies have five eyes: two large compound eyes which support vision, plus three smaller single lens eyes which are used for navigation. Each compound eye monitors 180° of space and consists of roughly 750 units, each containing eight light-sensitive cells called photoreceptors. This relatively wide spacing of photoreceptors is thought to limit the sharpness, or acuity, of vision in fruit flies. The area of the human retina (the light-sensitive surface at back of our eyes) that generates our sharpest vision contains photoreceptors that are 500 times more densely packed. Despite their differing designs, human and fruit fly eyes work via the same general principles. If we, or a fruit fly, were to hold our gaze completely steady, the world would gradually fade from view as the eye adapted to the unchanging visual stimulus. To ensure this does not happen, animals continuously make rapid, automatic eye movements called microsaccades. These refresh the image on the retina and prevent it from fading. Yet it is not known why do they not also cause blurred vision. Standard accounts of vision assume that the retina and the brain perform most of the information processing required, with photoreceptors simply detecting how much light enters the eye. However, Juusola, Dau, Song et al. now challenge this idea by showing that photoreceptors are specially adapted to detect the fluctuating patterns of light that enter the eye as a result of microsaccades. Moreover, fruit fly eyes resolve small moving objects far better than would be predicted based on the spacing of their photoreceptors. The discovery that photoreceptors are well adapted to deal with eye movements changes our understanding of insect vision. The findings also disprove the 100-year-old dogma that the spacing of photoreceptors limits the sharpness of vision in compound eyes. Further studies are required to determine whether photoreceptors in the retinas of other animals, including humans, have similar properties.