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Eye structure shapes neuron function in Drosophila motion vision

View ORCID ProfileArthur Zhao, View ORCID ProfileEyal Gruntman, View ORCID ProfileAljoscha Nern, View ORCID ProfileNirmala A. Iyer, View ORCID ProfileEdward M. Rogers, View ORCID ProfileSanna Koskela, View ORCID ProfileIgor Siwanowicz, View ORCID ProfileMarisa Dreher, View ORCID ProfileMiriam A. Flynn, View ORCID ProfileConnor W. Laughland, View ORCID ProfileHenrique D.F. Ludwig, View ORCID ProfileAlex G. Thomson, View ORCID ProfileCullen P. Moran, View ORCID ProfileBruck Gezahegn, View ORCID ProfileDavi D. Bock, View ORCID ProfileMichael B. Reiser
doi: https://doi.org/10.1101/2022.12.14.520178
Arthur Zhao
1HHMI Janelia Research Campus, USA
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Eyal Gruntman
1HHMI Janelia Research Campus, USA
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Aljoscha Nern
1HHMI Janelia Research Campus, USA
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Nirmala A. Iyer
1HHMI Janelia Research Campus, USA
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Edward M. Rogers
1HHMI Janelia Research Campus, USA
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Sanna Koskela
1HHMI Janelia Research Campus, USA
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Igor Siwanowicz
1HHMI Janelia Research Campus, USA
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Marisa Dreher
1HHMI Janelia Research Campus, USA
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Miriam A. Flynn
1HHMI Janelia Research Campus, USA
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Connor W. Laughland
1HHMI Janelia Research Campus, USA
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Henrique D.F. Ludwig
1HHMI Janelia Research Campus, USA
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Alex G. Thomson
1HHMI Janelia Research Campus, USA
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Cullen P. Moran
1HHMI Janelia Research Campus, USA
2Vanderbilt Eye Institute, USA
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Bruck Gezahegn
1HHMI Janelia Research Campus, USA
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Davi D. Bock
1HHMI Janelia Research Campus, USA
3Department of Neurological Sciences, University of Vermont, USA
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Michael B. Reiser
1HHMI Janelia Research Campus, USA
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Summary

Many animals rely on vision to navigate through their environment. The pattern of changes in the visual scene induced by self-motion is the optic flow1, which is first estimated in local patches by directionally selective (DS) neurons2–4. But how should the arrays of DS neurons, each responsive to motion in a preferred direction at a specific retinal position, be organized to support robust decoding of optic flow by downstream circuits? Understanding this global organization is challenging because it requires mapping fine, local features of neurons across the animal’s field of view3. In Drosophila, the asymmetric dendrites of the T4 and T5 DS neurons establish their preferred direction, making it possible to predict DS responses from anatomy4,5. Here we report that the preferred directions of fly DS neurons vary at different retinal positions and show that this spatial variation is established by the anatomy of the compound eye. To estimate the preferred directions across the visual field, we reconstructed hundreds of T4 neurons in a full brain EM volume6 and discovered unexpectedly stereotypical dendritic arborizations that are independent of location. We then used whole-head μCT scans to map the viewing directions of all compound eye facets and found a non-uniform sampling of visual space that explains the spatial variation in preferred directions. Our findings show that the organization of preferred directions in the fly is largely determined by the compound eye, exposing an intimate and unexpected connection between the peripheral structure of the eye, functional properties of neurons deep in the brain, and the control of body movements.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted December 15, 2022.
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Eye structure shapes neuron function in Drosophila motion vision
Arthur Zhao, Eyal Gruntman, Aljoscha Nern, Nirmala A. Iyer, Edward M. Rogers, Sanna Koskela, Igor Siwanowicz, Marisa Dreher, Miriam A. Flynn, Connor W. Laughland, Henrique D.F. Ludwig, Alex G. Thomson, Cullen P. Moran, Bruck Gezahegn, Davi D. Bock, Michael B. Reiser
bioRxiv 2022.12.14.520178; doi: https://doi.org/10.1101/2022.12.14.520178
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Eye structure shapes neuron function in Drosophila motion vision
Arthur Zhao, Eyal Gruntman, Aljoscha Nern, Nirmala A. Iyer, Edward M. Rogers, Sanna Koskela, Igor Siwanowicz, Marisa Dreher, Miriam A. Flynn, Connor W. Laughland, Henrique D.F. Ludwig, Alex G. Thomson, Cullen P. Moran, Bruck Gezahegn, Davi D. Bock, Michael B. Reiser
bioRxiv 2022.12.14.520178; doi: https://doi.org/10.1101/2022.12.14.520178

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