Literature DB >> 28870284

Microsaccadic sampling of moving image information provides Drosophila hyperacute vision.

Mikko Juusola1,2, An Dau2, Zhuoyi Song2, Narendra Solanki2, Diana Rien1,2, David Jaciuch2, Sidhartha Anil Dongre2, Florence Blanchard2, Gonzalo G de Polavieja3, Roger C Hardie4, Jouni Takalo2.   

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.

Entities:  

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

Mesh:

Year:  2017        PMID: 28870284      PMCID: PMC5584993          DOI: 10.7554/eLife.26117

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  148 in total

1.  Anticipation of moving stimuli by the retina.

Authors:  M J Berry; I H Brivanlou; T A Jordan; M Meister
Journal:  Nature       Date:  1999-03-25       Impact factor: 49.962

2.  Shaker K+ channels contribute early nonlinear amplification to the light response in Drosophila photoreceptors.

Authors:  Mikko Juusola; Jeremy E Niven; Andrew S French
Journal:  J Neurophysiol       Date:  2003-05-21       Impact factor: 2.714

3.  Miniature eye movements enhance fine spatial detail.

Authors:  Michele Rucci; Ramon Iovin; Martina Poletti; Fabrizio Santini
Journal:  Nature       Date:  2007-06-14       Impact factor: 49.962

4.  Microscopic eye movements compensate for nonhomogeneous vision within the fovea.

Authors:  Martina Poletti; Chiara Listorti; Michele Rucci
Journal:  Curr Biol       Date:  2013-08-15       Impact factor: 10.834

5.  Direct connections between the R7/8 and R1-6 photoreceptor subsystems in the dipteran visual system.

Authors:  S R Shaw; A Fröhlich; I A Meinertzhagen
Journal:  Cell Tissue Res       Date:  1989-08       Impact factor: 5.249

6.  Subcellular Imaging of Voltage and Calcium Signals Reveals Neural Processing In Vivo.

Authors:  Helen H Yang; François St-Pierre; Xulu Sun; Xiaozhe Ding; Michael Z Lin; Thomas R Clandinin
Journal:  Cell       Date:  2016-06-02       Impact factor: 41.582

7.  The Drosophila SK channel (dSK) contributes to photoreceptor performance by mediating sensitivity control at the first visual network.

Authors:  Ahmad N Abou Tayoun; Xiaofeng Li; Brian Chu; Roger C Hardie; Mikko Juusola; Patrick J Dolph
Journal:  J Neurosci       Date:  2011-09-28       Impact factor: 6.167

8.  Separation of receptor and lamina potentials in the electroretinogram of normal and mutant Drosophila.

Authors:  M Heisenberg
Journal:  J Exp Biol       Date:  1971-08       Impact factor: 3.312

9.  Functional connectivity in the retina at the resolution of photoreceptors.

Authors:  Greg D Field; Jeffrey L Gauthier; Alexander Sher; Martin Greschner; Timothy A Machado; Lauren H Jepson; Jonathon Shlens; Deborah E Gunning; Keith Mathieson; Wladyslaw Dabrowski; Liam Paninski; Alan M Litke; E J Chichilnisky
Journal:  Nature       Date:  2010-10-07       Impact factor: 49.962

10.  Ih channels control feedback regulation from amacrine cells to photoreceptors.

Authors:  Wen Hu; Tingting Wang; Xiao Wang; Junhai Han
Journal:  PLoS Biol       Date:  2015-04-01       Impact factor: 8.029

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  12 in total

1.  Fly eyes are not still: a motion illusion in Drosophila flight supports parallel visual processing.

Authors:  Wael Salem; Benjamin Cellini; Mark A Frye; Jean-Michel Mongeau
Journal:  J Exp Biol       Date:  2020-05-28       Impact factor: 3.312

2.  Ca2+-Activated K+ Channels Reduce Network Excitability, Improving Adaptability and Energetics for Transmitting and Perceiving Sensory Information.

Authors:  Xiaofeng Li; Ahmad Abou Tayoun; Zhuoyi Song; An Dau; Diana Rien; David Jaciuch; Sidhartha Dongre; Florence Blanchard; Anton Nikolaev; Lei Zheng; Murali K Bollepalli; Brian Chu; Roger C Hardie; Patrick J Dolph; Mikko Juusola
Journal:  J Neurosci       Date:  2019-07-26       Impact factor: 6.167

3.  Rapid Release of Ca2+ from Endoplasmic Reticulum Mediated by Na+/Ca2+ Exchange.

Authors:  Che-Hsiung Liu; Zijing Chen; Megan K Oliva; Junjie Luo; Simon Collier; Craig Montell; Roger C Hardie
Journal:  J Neurosci       Date:  2020-03-10       Impact factor: 6.167

Review 4.  A biomimetic fly photoreceptor model elucidates how stochastic adaptive quantal sampling provides a large dynamic range.

Authors:  Zhuoyi Song; Mikko Juusola
Journal:  J Physiol       Date:  2017-05-17       Impact factor: 5.182

Review 5.  How a fly photoreceptor samples light information in time.

Authors:  Mikko Juusola; Zhuoyi Song
Journal:  J Physiol       Date:  2017-04-17       Impact factor: 5.182

6.  Modeling elucidates how refractory period can provide profound nonlinear gain control to graded potential neurons.

Authors:  Zhuoyi Song; Yu Zhou; Mikko Juusola
Journal:  Physiol Rep       Date:  2017-06

7.  Contrast sensitivity reveals an oculomotor strategy for temporally encoding space.

Authors:  Antonino Casile; Jonathan D Victor; Michele Rucci
Journal:  Elife       Date:  2019-01-08       Impact factor: 8.140

8.  A low-cost hyperspectral scanner for natural imaging and the study of animal colour vision above and under water.

Authors:  N E Nevala; T Baden
Journal:  Sci Rep       Date:  2019-07-25       Impact factor: 4.379

9.  Visual approach computation in feeding hoverflies.

Authors:  Malin Thyselius; Paloma T Gonzalez-Bellido; Trevor J Wardill; Karin Nordström
Journal:  J Exp Biol       Date:  2018-05-22       Impact factor: 3.312

10.  Can Drosophila melanogaster tell who's who?

Authors:  Jonathan Schneider; Nihal Murali; Graham W Taylor; Joel D Levine
Journal:  PLoS One       Date:  2018-10-24       Impact factor: 3.240

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