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Binocular mirror–symmetric microsaccadic sampling enables Drosophila hyperacute 3D vision

Kemppainen, Joni ; Scales, Ben ; Haghighi, Keivan Razban ; Takalo, Jouni ; Mansour, Neveen ; McManus, James ; Leko, Gabor ; Saari, Paulus ; Hurcomb, James and Antohi, Andra , et al. (2022) In Proceedings of the National Academy of Sciences of the United States of America 119(12).
Abstract

Neural mechanisms behind stereopsis, which requires simultaneous disparity inputs from two eyes, have remained mysterious. Here we show how ultrafast mirror-symmetric photomechanical contractions in the frontal forward-facing left and right eye photoreceptors give Drosophila superresolution three-dimensional (3D) vision. By interlinking multiscale in vivo assays with multiscale simulations, we reveal how these photoreceptor microsaccades—by verging, diverging, and narrowing the eyes’ overlapping receptive fields—channel depth information, as phasic binocular image motion disparity signals in time. We further show how peripherally, outside stereopsis, microsaccadic sampling tracks a flying fly’s optic flow field to better resolve the... (More)

Neural mechanisms behind stereopsis, which requires simultaneous disparity inputs from two eyes, have remained mysterious. Here we show how ultrafast mirror-symmetric photomechanical contractions in the frontal forward-facing left and right eye photoreceptors give Drosophila superresolution three-dimensional (3D) vision. By interlinking multiscale in vivo assays with multiscale simulations, we reveal how these photoreceptor microsaccades—by verging, diverging, and narrowing the eyes’ overlapping receptive fields—channel depth information, as phasic binocular image motion disparity signals in time. We further show how peripherally, outside stereopsis, microsaccadic sampling tracks a flying fly’s optic flow field to better resolve the world in motion. These results change our understanding of how insect compound eyes work and suggest a general dynamic stereo-information sampling strategy for animals, robots, and sensors.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Active sampling, Adaptive optics, Compound eyes, Stereovision
in
Proceedings of the National Academy of Sciences of the United States of America
volume
119
issue
12
article number
e2109717119
publisher
National Academy of Sciences
external identifiers
  • scopus:85126701227
  • pmid:35298337
ISSN
0027-8424
DOI
10.1073/pnas.2109717119
language
English
LU publication?
yes
id
ecfa146e-4690-46c1-bc44-966861821e77
date added to LUP
2022-06-09 10:17:37
date last changed
2024-06-13 16:07:09
@article{ecfa146e-4690-46c1-bc44-966861821e77,
  abstract     = {{<p>Neural mechanisms behind stereopsis, which requires simultaneous disparity inputs from two eyes, have remained mysterious. Here we show how ultrafast mirror-symmetric photomechanical contractions in the frontal forward-facing left and right eye photoreceptors give Drosophila superresolution three-dimensional (3D) vision. By interlinking multiscale in vivo assays with multiscale simulations, we reveal how these photoreceptor microsaccades—by verging, diverging, and narrowing the eyes’ overlapping receptive fields—channel depth information, as phasic binocular image motion disparity signals in time. We further show how peripherally, outside stereopsis, microsaccadic sampling tracks a flying fly’s optic flow field to better resolve the world in motion. These results change our understanding of how insect compound eyes work and suggest a general dynamic stereo-information sampling strategy for animals, robots, and sensors.</p>}},
  author       = {{Kemppainen, Joni and Scales, Ben and Haghighi, Keivan Razban and Takalo, Jouni and Mansour, Neveen and McManus, James and Leko, Gabor and Saari, Paulus and Hurcomb, James and Antohi, Andra and Suuronen, Jussi Petteri and Blanchard, Florence and Hardie, Roger C. and Song, Zhuoyi and Hampton, Mark and Eckermann, Marina and Westermeier, Fabian and Frohn, Jasper and Hoekstra, Hugo and Lee, Chi Hon and Huttula, Marko and Mokso, Rajmund and Juusola, Mikko}},
  issn         = {{0027-8424}},
  keywords     = {{Active sampling; Adaptive optics; Compound eyes; Stereovision}},
  language     = {{eng}},
  month        = {{03}},
  number       = {{12}},
  publisher    = {{National Academy of Sciences}},
  series       = {{Proceedings of the National Academy of Sciences of the United States of America}},
  title        = {{Binocular mirror–symmetric microsaccadic sampling enables Drosophila hyperacute 3D vision}},
  url          = {{http://dx.doi.org/10.1073/pnas.2109717119}},
  doi          = {{10.1073/pnas.2109717119}},
  volume       = {{119}},
  year         = {{2022}},
}