Anatomical reconstruction and functional imaging reveal an ordered array of skylight polarization detectors in Drosophila

Weir, Peter T., Henze, Miriam J., Bleul, Christiane, Baumann-Klausener, Franziska, 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: 5397-5404. doi:10.1523/JNEUROSCI.0310-16.2016

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Author Weir, Peter T.
Henze, Miriam J.
Bleul, Christiane
Baumann-Klausener, Franziska
Labhart, Thomas
Dickinson, Michael H.
Title Anatomical reconstruction and functional imaging reveal an ordered array of skylight polarization detectors in Drosophila
Formatted title
Anatomical reconstruction and functional imaging reveal an ordered array of skylight polarization detectors in Drosophila
Journal name Journal of Neuroscience   Check publisher's open access policy
ISSN 1529-2401
0270-6474
Publication date 2016-05-11
Year available 2016
Sub-type Article (original research)
DOI 10.1523/JNEUROSCI.0310-16.2016
Open Access Status File (Publisher version)
Volume 36
Issue 19
Start page 5397
End page 5404
Total pages 8
Place of publication Washington, DC United States
Publisher Society for Neuroscience
Language eng
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.

The fly's visual system is an influential model system for studying neural computation, and much is known about its anatomy, physiology, and development. The circuits underlying motion processing have received the most attention, but researchers are increasingly investigating other functions, such as color perception and object recognition. In this work, we investigate the early neural processing of a somewhat exotic sense, called polarization vision. Because skylight is polarized in an orientation that is rigidly determined by the position of the sun, this cue provides compass information. Behavioral experiments have shown that many species use the polarization pattern in the sky to direct locomotion. Here we describe the input stage of the fly's polarization-vision system.
Formatted 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.
Keyword Insect
Navigation
Polarization opponency
Polarized light
Vision
Q-Index Code C1
Q-Index Status Provisional Code
Grant ID U01 NS090514
Institutional Status Non-UQ

Document type: Journal Article
Sub-type: Article (original research)
Collection: Queensland Brain Institute Publications
 
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Created: Tue, 13 Jun 2017, 10:42:29 EST by Kirstie Asmussen on behalf of Queensland Brain Institute