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Kemppainen, J., Scales, B., Razban Haghighi, K., Takalo, J., Mansour, N., McManus, J., Leko, G., Saari, P., Hurcomb, J., Antohi, A., Suuronen, J.-P., Blanchard, F., Hardie, R. C., Song, Z., Hampton, M., Eckermann, M., Westermeier, F., Frohn, J., Hoekstra, H., … Juusola, M. (2022). Binocular mirror–symmetric microsaccadic sampling enables Drosophila hyperacute 3D vision. Proceedings of the National Academy of Sciences, 119(12), e2109717119. https://doi.org/10.1073/pnas.2109717119

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

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Author: Kemppainen, Joni1; Scales, Ben1; Haghighi, Keivan Razban1;
Organizations: 1Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, United Kingdom
2Department of Image Processing and Computer Graphics, University of Szeged, H-6701 Szeged, Hungary
3Nano and Molecular Systems, University of Oulu, Oulu FIN-90041, Finland
4European Synchrotron Radiation Facility, 38043 Grenoble, France
5Xploraytion GmbH, D-10625, Berlin, Germany
6Department of Physiology Development and Neuroscience, Cambridge University, Cambridge CB2 3EG, United Kingdom
7Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai 200433, China
8Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Ministry of Education, Fudan University, Shanghai 200433, China
9Ministry of Education Frontiers Center for Brain Science, Fudan University, Shanghai 200433, China
10University of Sheffield Advanced Manufacturing Research Centre, Sheffield S9 1ZA, United Kingdom
11Institut für Röntgenphysik, Georg August Universität Göttingen, 37077 Göttingen, Germany
12Deutsches Elektronen-Synchrotron, 22607 Hamburg, Germany
13Faculty of Electrical Engineering, Mathematics, and Computer Science, University of Twente, UT7522 NB Enschede, The Netherlands
14Institute of Cellular and Organismic Biology, Academia Sinica, Taipei 11529, Taiwan
15MAX IV Laboratory, Lund University, SE-221 00 Lund, Sweden
16National Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China
Format: article
Version: published version
Access: open
Online Access: PDF Full Text (PDF, 3.6 MB)
Persistent link: http://urn.fi/urn:nbn:fi-fe2022122072863
Language: English
Published: National Academy of Sciences of the United States of America, 2022
Publish Date: 2022-12-20
Description:

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 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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Series: Proceedings of the National Academy of Sciences of the United States of America
ISSN: 0027-8424
ISSN-E: 1091-6490
ISSN-L: 0027-8424
Volume: 119
Issue: 12
Article number: e2109717119
DOI: 10.1073/pnas.2109717119
OADOI: https://oadoi.org/10.1073/pnas.2109717119
Type of Publication: A1 Journal article – refereed
Field of Science: 114 Physical sciences
Subjects:
active sampling
adaptive optics
compound eyes
stereovision
Article
Funding: This work was supported by Jane and Aatos Erkko Foundation fellowships (J.T. and M.J.), The Leverhulme Trust (RPG-2012-567 to M.J.), the Biotechnology and Biological Sciences Research Council (BBSRC) (BB/F012071/1, BB/D001900/1, and BB/H013849/1 to M.J.), the Engineering and Physical Sciences Research Council (EP/P006094/1 to M.J.), the White Rose BBSRC Doctoral Training Program (BB/M011151/1 to B.S. and M.J.), the Open Research Fund of the State Key Laboratory of Cognitive Neuroscience and Learning (M.J.), a High-End Foreign Expert Grant by the Chinese Government (GDT20151100004 to M.J.), DESY (I-20190808 EC, I-20180674 EC, and I-20170823 to R.M. and M.J.), and the ESRF (LS-2780 to R.M. and M.J. and IH-LS-3170 to J.-P.S.) beam-time grants.
Dataset Reference: X-ray imaging data have been deposited in GitHub (https://github.com/JuusolaLab/Hyperacute_Stereopsis_paper). All other study data are included in the article and/or supporting information.
  https://github.com/JuusolaLab/Hyperacute_Stereopsis_paper
Copyright information: © 2022 the Author(s). This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).
  https://creativecommons.org/licenses/by/4.0/