Synaptic targets of photoreceptors specialized to detect color and skylight polarization in Drosophila
- Freie Universität Berlin, Germany
- Howard Hughes Medical Institute, United States
Abstract
Color and polarization provide complementary information about the world and are detected by specialized photoreceptors. However, the downstream neural circuits that process these distinct modalities are incompletely understood in any animal. Using electron microscopy, we have systematically reconstructed the synaptic targets of the photoreceptors specialized to detect color and skylight polarization in Drosophila, and we have used light microscopy to confirm many of our findings. We identified known and novel downstream targets that are selective for different wavelengths or polarized light, and followed their projections to other areas in the optic lobes and the central brain. Our results revealed many synapses along the photoreceptor axons between brain regions, new pathways in the optic lobes, and spatially segregated projections to central brain regions. Strikingly, photoreceptors in the polarization-sensitive dorsal rim area target fewer cell types, and lack strong connections to the lobula, a neuropil involved in color processing. Our reconstruction identifies shared wiring and modality-specific specializations for color and polarization vision, and provides a comprehensive view of the first steps of the pathways processing color and polarized light inputs.
Data availability
All data generated or analyzed during this study are included in the manuscript and supporting files. Supplementary File 1 and 3 contain all connectivity data. Supplementary File 2 provides images of all EM skeletons.All code and necessary data to perform the analysis and generate the figures of this manuscript will be available from https://github.com/reiserlab.All reconstructed neurons described in the manuscript will be made available at https://fafb.catmaid.virtualflybrain.org/.
Article and author information
Author details
Funding
Howard Hughes Medical Institute
- Kit D Longden
- Aljoscha Nern
- Arthur Zhao
- Miriam A Flynn
- Connor W Laughland
- Bruck Gezahegn
- Henrique DF Ludwig
- Alex G Thomson
- Heather Dionne
- Davi D Bock
- Gerald M Rubin
- Michael B Reiser
Freie Universität Berlin
- Emil Kind
- Gizem Sancer
- Tessa Obrusnik
- Paula G Alarcón
- Mathias F Wernet
Deutsche Forschungsgemeinschaft (WE 5761/2-1)
- Mathias F Wernet
Deutsche Forschungsgemeinschaft (WE 5761/4-1)
- Mathias F Wernet
Air Force Office of Scientific Research (FA9550-19-1-7005)
- Mathias F Wernet
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Ronald L Calabrese, Emory University, United States
Version history
- Preprint posted: May 17, 2021 (view preprint)
- Received: July 1, 2021
- Accepted: December 15, 2021
- Accepted Manuscript published: December 16, 2021 (version 1)
- Accepted Manuscript updated: January 4, 2022 (version 2)
- Version of Record published: January 25, 2022 (version 3)
Copyright
© 2021, Kind et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 2,682
- views
-
- 432
- downloads
-
- 36
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Synaptic targets of photoreceptors specialized to detect color and skylight polarization in Drosophila
eLife 10:e71858.
https://doi.org/10.7554/eLife.71858
Further reading
-
- Cell Biology
- Neuroscience
Mutations in Drosophila Swiss cheese (SWS) gene or its vertebrate orthologue neuropathy target esterase (NTE) lead to progressive neuronal degeneration in flies and humans. Despite its enzymatic function as a phospholipase is well established, the molecular mechanism responsible for maintaining nervous system integrity remains unclear. In this study, we found that NTE/SWS is present in surface glia that forms the blood-brain barrier (BBB) and that NTE/SWS is important to maintain its structure and permeability. Importantly, BBB glia-specific expression of Drosophila NTE/SWS or human NTE in the sws mutant background fully rescues surface glial organization and partially restores BBB integrity, suggesting a conserved function of NTE/SWS. Interestingly, sws mutant glia showed abnormal organization of plasma membrane domains and tight junction rafts accompanied by the accumulation of lipid droplets, lysosomes, and multilamellar bodies. Since the observed cellular phenotypes closely resemble the characteristics described in a group of metabolic disorders known as lysosomal storage diseases (LSDs), our data established a novel connection between NTE/SWS and these conditions. We found that mutants with defective BBB exhibit elevated levels of fatty acids, which are precursors of eicosanoids and are involved in the inflammatory response. Also, as a consequence of a permeable BBB, several innate immunity factors are upregulated in an age-dependent manner, while BBB glia-specific expression of NTE/SWS normalizes inflammatory response. Treatment with anti-inflammatory agents prevents the abnormal architecture of the BBB, suggesting that inflammation contributes to the maintenance of a healthy brain barrier. Considering the link between a malfunctioning BBB and various neurodegenerative diseases, gaining a deeper understanding of the molecular mechanisms causing inflammation due to a defective BBB could help to promote the use of anti-inflammatory therapies for age-related neurodegeneration.
-
- Neuroscience
Natural behaviors have redundancy, which implies that humans and animals can achieve their goals with different strategies. Given only observations of behavior, is it possible to infer the control objective that the subject is employing? This challenge is particularly acute in animal behavior because we cannot ask or instruct the subject to use a particular strategy. This study presents a three-pronged approach to infer an animal’s control objective from behavior. First, both humans and monkeys performed a virtual balancing task for which different control strategies could be utilized. Under matched experimental conditions, corresponding behaviors were observed in humans and monkeys. Second, a generative model was developed that represented two main control objectives to achieve the task goal. Model simulations were used to identify aspects of behavior that could distinguish which control objective was being used. Third, these behavioral signatures allowed us to infer the control objective used by human subjects who had been instructed to use one control objective or the other. Based on this validation, we could then infer objectives from animal subjects. Being able to positively identify a subject’s control objective from observed behavior can provide a powerful tool to neurophysiologists as they seek the neural mechanisms of sensorimotor coordination.
