Microsaccadic sampling of moving image information provides Drosophila hyperacute vision

Elife. 2017 Sep 5;6:e26117. doi: 10.7554/eLife.26117.

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.

Keywords: D. melanogaster; Hyperacuity; computational biology; information theory; neuroscience; photoreceptor transduction; saccadic eye movements; stochasticity; systems biology; systems modeling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Computer Simulation
  • Drosophila melanogaster / physiology*
  • Drosophila melanogaster / ultrastructure
  • Eye Movements / physiology*
  • Fixation, Ocular / physiology
  • Models, Neurological
  • Movement
  • Photic Stimulation*
  • Photons
  • Photoreceptor Cells, Invertebrate / metabolism
  • Photoreceptor Cells, Invertebrate / ultrastructure
  • Retina / physiology
  • Vision, Ocular / physiology*
  • Visual Acuity / physiology*