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Articles, Systems/Circuits

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
Journal of Neuroscience 11 May 2016, 36 (19) 5397-5404; DOI: https://doi.org/10.1523/JNEUROSCI.0310-16.2016
Peter T. Weir
1Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125, and
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Miriam J. Henze
2Institute of Molecular Life Sciences, University of Zurich, 8057 Zurich, Switzerland
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Christiane Bleul
2Institute of Molecular Life Sciences, University of Zurich, 8057 Zurich, Switzerland
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Franziska Baumann-Klausener
2Institute of Molecular Life Sciences, University of Zurich, 8057 Zurich, Switzerland
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Thomas Labhart
2Institute of Molecular Life Sciences, University of Zurich, 8057 Zurich, Switzerland
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Michael H. Dickinson
1Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125, and
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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.

SIGNIFICANCE STATEMENT 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.

  • insect
  • navigation
  • polarization opponency
  • polarized light
  • vision
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The Journal of Neuroscience: 36 (19)
Journal of Neuroscience
Vol. 36, Issue 19
11 May 2016
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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, Michael H. Dickinson
Journal of Neuroscience 11 May 2016, 36 (19) 5397-5404; DOI: 10.1523/JNEUROSCI.0310-16.2016

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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, Michael H. Dickinson
Journal of Neuroscience 11 May 2016, 36 (19) 5397-5404; DOI: 10.1523/JNEUROSCI.0310-16.2016
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Keywords

  • insect
  • navigation
  • polarization opponency
  • polarized light
  • vision

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