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Anatomical Reconstruction and Functional Imaging Reveal an Ordered Array of Skylight Polarization Detectors in Drosophila

Weir, Peter T. and Henze, Miriam J. and Bleul, Christiane and Baumann-Klausener, Franziska and Labhart, Thomas and Dickinson, Michael H. (2016) Anatomical Reconstruction and Functional Imaging Reveal an Ordered Array of Skylight Polarization Detectors in Drosophila. Journal of Neuroscience, 36 (19). pp. 5397-5404. ISSN 0270-6474. PMCID PMC4863064. doi:10.1523/JNEUROSCI.0310-16.2016. https://resolver.caltech.edu/CaltechAUTHORS:20160517-082346810

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Abstract

Many insects exploit skylight polarization as a compass cue for orientation and navigation. In the fruit fly, Drosophila melanogaster, photoreceptors R7 and R8 in the dorsal rim area (DRA) of the compound eye are specialized to detect the electric vector (e-vector) of linearly polarized light. These photoreceptors are arranged in stacked pairs with identical fields of view and spectral sensitivities, but mutually orthogonal microvillar orientations. As in larger flies, we found that the microvillar orientation of the distal photoreceptor R7 changes in a fan-like fashion along the DRA. This anatomical arrangement suggests that the DRA constitutes a detector for skylight polarization, in which different e-vectors maximally excite different positions in the array. To test our hypothesis, we measured responses to polarized light of varying e-vector angles in the terminals of R7/8 cells using genetically encoded calcium indicators. Our data confirm a progression of preferred e-vector angles from anterior to posterior in the DRA, and a strict orthogonality between the e-vector preferences of paired R7/8 cells. We observed decreased activity in photoreceptors in response to flashes of light polarized orthogonally to their preferred e-vector angle, suggesting reciprocal inhibition between photoreceptors in the same medullar column, which may serve to increase polarization contrast. Together, our results indicate that the polarization-vision system relies on a spatial map of preferred e-vector angles at the earliest stage of sensory processing.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1523/JNEUROSCI.0310-16.2016DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4863064/PubMed CentralArticle
ORCID:
AuthorORCID
Weir, Peter T.0000-0003-3111-7829
Henze, Miriam J.0000-0002-0563-2539
Labhart, Thomas0000-0002-7768-002X
Dickinson, Michael H.0000-0002-8587-9936
Additional Information:© 2016 the authors. For the first six months after publication SfN’s license will be exclusive. Beginning six months after publication the Work will be made freely available to the public on SfN’s website to copy, distribute, or display under a Creative Commons Attribution 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/). Received January 27, 2016. Revision received April 4, 2016. Accepted April 6, 2016. This work was supported by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under Award U01NS090514 (M.H.D.), the National Science Foundation under Grant No. 1352707 (M.H.D.), the Paul G. Allen Family Foundation (M.H.D.), and the German National Merit Foundation (Studienstiftung des deutschen Volkes; M.J.H.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. We thank S. Sommer and J. Smolka for advice on statistics, M. Wernet for providing prh1-eGFP transgenic flies, B. Schnell for valuable discussions, and two anonymous reviewers for constructive comments. The authors declare no competing financial interests.
Funders:
Funding AgencyGrant Number
NIHU01NS090514
NSFIOS-1352707
Paul G. Allen Family FoundationUNSPECIFIED
Studienstiftung des deutschen VolkesUNSPECIFIED
Subject Keywords:insect; navigation; polarization opponency; polarized light; vision
Issue or Number:19
PubMed Central ID:PMC4863064
DOI:10.1523/JNEUROSCI.0310-16.2016
Record Number:CaltechAUTHORS:20160517-082346810
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20160517-082346810
Official Citation:Anatomical Reconstruction and Functional Imaging Reveal an Ordered Array of Skylight Polarization Detectors in Drosophila Peter T. Weir, Miriam J. Henze, Christiane Bleul, Franziska Baumann-Klausener, Thomas Labhart, and Michael H. Dickinson The Journal of Neuroscience, 11 May 2016, 36(19):5397-5404; doi:10.1523/JNEUROSCI.0310-16.2016
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:67149
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:17 May 2016 15:52
Last Modified:27 Apr 2022 23:09

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