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

Author:

Kemppainen Joni1ORCID,Scales Ben1ORCID,Razban Haghighi Keivan1ORCID,Takalo Jouni1,Mansour Neveen1ORCID,McManus James1,Leko Gabor2,Saari Paulus3ORCID,Hurcomb James1ORCID,Antohi Andra1ORCID,Suuronen Jussi-Petteri45ORCID,Blanchard Florence1,Hardie Roger C.6ORCID,Song Zhuoyi1789ORCID,Hampton Mark10,Eckermann Marina11ORCID,Westermeier Fabian12ORCID,Frohn Jasper11ORCID,Hoekstra Hugo13ORCID,Lee Chi-Hon14ORCID,Huttula Marko3ORCID,Mokso Rajmund15,Juusola Mikko116ORCID

Affiliation:

1. Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, United Kingdom

2. Department of Image Processing and Computer Graphics, University of Szeged, H-6701 Szeged, Hungary

3. Nano and Molecular Systems, University of Oulu, Oulu FIN-90041, Finland

4. European Synchrotron Radiation Facility, 38043 Grenoble, France

5. Xploraytion GmbH, D-10625, Berlin, Germany

6. Department of Physiology Development and Neuroscience, Cambridge University, Cambridge CB2 3EG, United Kingdom

7. Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai 200433, China

8. Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Ministry of Education, Fudan University, Shanghai 200433, China

9. Ministry of Education Frontiers Center for Brain Science, Fudan University, Shanghai 200433, China

10. University of Sheffield Advanced Manufacturing Research Centre, Sheffield S9 1ZA, United Kingdom

11. Institut für Röntgenphysik, Georg August Universität Göttingen, 37077 Göttingen, Germany

12. Deutsches Elektronen-Synchrotron, 22607 Hamburg, Germany

13. Faculty of Electrical Engineering, Mathematics, and Computer Science, University of Twente, UT7522 NB Enschede, The Netherlands

14. Institute of Cellular and Organismic Biology, Academia Sinica, Taipei 11529, Taiwan

15. MAX IV Laboratory, Lund University, SE-221 00 Lund, Sweden

16. National Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China

Abstract

Significance To move efficiently, animals must continuously work out their x,y,z positions with respect to real-world objects, and many animals have a pair of eyes to achieve this. How photoreceptors actively sample the eyes’ optical image disparity is not understood because this fundamental information-limiting step has not been investigated in vivo over the eyes’ whole sampling matrix. This integrative multiscale study will advance our current understanding of stereopsis from static image disparity comparison to a morphodynamic active sampling theory. It shows how photomechanical photoreceptor microsaccades enable Drosophila superresolution three-dimensional vision and proposes neural computations for accurately predicting these flies’ depth-perception dynamics, limits, and visual behaviors.

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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