Synaptic targets of photoreceptors specialized to detect color and skylight polarization in Drosophila

  1. Emil Kind
  2. Kit D Longden
  3. Aljoscha Nern
  4. Arthur Zhao
  5. Gizem Sancer
  6. Miriam A Flynn
  7. Connor W Laughland
  8. Bruck Gezahegn
  9. Henrique DF Ludwig
  10. Alex G Thomson
  11. Tessa Obrusnik
  12. Paula G Alarcón
  13. Heather Dionne
  14. Davi D Bock
  15. Gerald M Rubin
  16. Michael B Reiser
  17. Mathias F Wernet

  • Curated by eLife

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    Evaluation Summary:

    This paper will be of interest to the large class of neuroscientists who perform network analyses and are interested in the processing of visual information. It sets a new standard in connectomic analysis because is combines EM data of a whole fly brain with fluorescent labeling of specific neurons. The key claims of the manuscript are well supported by the data, and the approaches used are thoughtful and rigorous.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

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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.

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  1. Version published to 10.7554/elife.71858 on eLife
  2. eLife

    Evaluation Summary:

    This paper will be of interest to the large class of neuroscientists who perform network analyses and are interested in the processing of visual information. It sets a new standard in connectomic analysis because is combines EM data of a whole fly brain with fluorescent labeling of specific neurons. The key claims of the manuscript are well supported by the data, and the approaches used are thoughtful and rigorous.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

  3. eLife

    Reviewer #1 (Public Review):

    This manuscript summarizes a heroic effort by the Reiser and Wernet labs, and colleagues, a clear and well-balanced manuscript. I have no doubt it will become an important reference for anyone analyzing color or polarized light circuits in Drosophila.

    It is intrinsic to the approach of anatomical connectomic data, that the core of the text is rather descriptive and simply summarizes the quantification and statistical analysis of synaptic connection between individual types of neurons. The most important points that makes this paper so interesting is the following:

    – Many types of neurons within the lamina, medulla, lobula and beyond have been studied for their physiological responses or roles in visual behaviors. Thus, there is a strong framework to which the current study contributes and provides a rather extensive circuit structure.

    – The structure how individual topics as subheading are organized is clear and repetitive. It allows a reader to clearly repeat the content of each section and also to look for relevant information in the respective section.

    – As an elegant way to distinguish between pale and yellow PRs the authors made use of an identified accessory medulla neuron aMe12, which selectively innervates pale but not yellow ommatidial elements.

    – The manuscript provides important information on the circuit architecture, commonalities and differences between pale versus yellow inner PRs (R7 and R8) and the DRA-R7/R8 pairs that provide one core element of polarized light sensing.

    – There are several previously unknown neurons described here. Based on the connections it is possible to speculate about their function.

  4. eLife

    Reviewer #2 (Public Review):

    This comprehensive manuscript can be regarded as an atlas of synaptic connections of photoreceptors specialized to detect color (R7/R8) and skylight polarization (R7/R8 in the dorsal rim area, DRA) in the fruit fly Drosophila. In contrast to previous attempts, the authors used a full-brain EM volume for the reconstruction of the pathways downstream of these photoreceptors and identified so far unknown photoreceptor targets and pathways into the central brain. Besides describing in detail the different targets of R7/R8 and R7/R8-DRA, the authors revealed highly interesting differences between the two pathways. While in the color vision pathway R8 input is dominant, in the polarisation vision pathway R7 input is dominant. Another interesting difference lies in the innervation of the lobula, which is prominent in the color vision pathway and virtually absent in the polarisation vision pathway. Both pathways innervate the central brain (e.g. the anterior optic tubercles), but their axon terminals remain spatially separated showing that polarization and color vision are processes in parallel.

    The study is carefully performed, the methods are described in detail, the results are excellently documented and all conclusions are justified by the data. Furthermore, all data are included in the manuscript and supporting files.

    In summary, I can say that this comprehensive catalog establishes a broad foundation for further studies into the mechanistic basis of color and polarization vision and its contributions to perception and behavior.

    The manuscript has several strengths:

    1. It provides the first connectomic data set for photoreceptors that process skylight information in any insect and will be important for developing refined models of skylight navigation.

    2. It establishes the complete morphology of large, muli-columnar cell types that are targetted by the inner photoreceptors R7 and R8 but had eluded previous connectomic reconstruction efforts.

    3. The EM data were supplemented by analysis on light microscopic level and compared with previous connectivity data from dense reconstructions generated from smaller-scale medulla volumes.

    4. The study discovered important pathways from the inner photoreceptors to the central brain. Completely novel is a pathway formed by only three neurons per brain hemisphere (cell type aMe12) that connects pale R8 photoreceptors with the central brain.

    5. The comparative interplay between data sets provides unique advantages and represents an important step in cross-validating and extending the applicability of all related data sets.

    6. This atlas provides a valuable basis for all researchers interested in color and/or polarization vision.

    Weakness of the study:

    1. As true for all anatomical descriptions, the work is hard to read and understanding requires some prior knowledge.
  5. eLife

    Reviewer #3 (Public Review):

    Connectomics analyses of neural circuit structure provide a durable description of neural anatomy that can both inform our understanding of circuit organization and inspire a wide range of subsequent studies. Here Kind, Longden, Nern, Zhao and colleagues provide a thorough reconstruction of the synaptic partners of a subset of photoreceptors in the Drosophila visual system, a widely used system for understanding circuit development and function. Using a reconstruction strategy that begins with individual photoreceptors and endeavors to identify all of their post-synaptic targets across a large brain volume, this work provides a detailed description of the core circuitry involved in processing spectral and polarized light inputs. A core strength of the work lies in its comprehensive characterization - I agree with the authors that they have achieved their goal of identifying all of the major synaptic partners of these cells, as the analysis is very carefully laid out and the data are thoroughly described. A second strength of the work is that, like the best of studies in the connectomics field, it opens up a number of intriguing experimental directions for future work, and presents the data in a form that can be readily accessed by future investigators. I therefore believe that the work will be widely used by a growing field.

  6. Version published to 10.1101/2021.05.17.444480v2 on bioRxiv
  7. Version published to 10.1101/2021.05.17.444480v1 on bioRxiv