Abstract
Understanding the mechanisms that link sensory stimuli to animal behavior is a central challenge in neuroscience. The quantitative description of behavioral responses to defined stimuli has led to a rich understanding of different behavioral strategies in many species. One important navigational cue perceived by many vertebrates and insects is the e-vector orientation of linearly polarized light. Drosophila manifests an innate orientation response to this cue (‘polarotaxis’), aligning its body axis with the e-vector field. We have established a population-based behavioral paradigm for the genetic dissection of neural circuits guiding polarotaxis to both celestial as well as reflected polarized stimuli. However, the behavioral mechanisms by which flies align with a linearly polarized stimulus remain unknown. Here, we present a detailed quantitative description of Drosophila polarotaxis, systematically measuring behavioral parameters that are modulated by the stimulus. We show that angular acceleration is modulated during alignment, and this single parameter may be sufficient for alignment. Furthermore, using monocular deprivation, we show that each eye is necessary for modulating turns in the ipsilateral direction. This analysis lays the foundation for understanding how neural circuits guide these important visual behaviors.
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Acknowledgments
The authors thank Thomas Labhart, Bob Schneeveis, and David Profitt for technical assistance. This work was supported by the Helen Hay Whitney Foundation (MFW), the Jane Coffin Childs Foundation (DAC), a Ruth L. Kirschstein Graduate Fellowship Award (MMV), and by an NIH Director’s Pioneer Award (DP1 OD003530) to TRC. This work was also supported by a Burroughs-Wellcome Career Development Award (TRC), a Mcknight Scholar Award (TRC), and Klingenstein Fellowship (TRC), and a Searle Scholar Award (TRC).
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359_2014_910_MOESM1_ESM.tif
Supplemental Fig S1. Experimental setup and procedures. a Schematic of the experimental setup used to present linearly polarized UV light from above to populations of Drosophila, which are illuminated with IR light (red), and are filmed from below (camera). A polarization filter (Polarizer) is facing the flies, with a diffuser facing the light source. IR = infrared light. UV = polarized UV light. b Summary of the stimulus protocol used. Top: A computer-controlled servomotor rotated the polarization filter in 45° increments, remaining still for 5 s at each position. Different motor positions are shown. Below: Polar histograms of fly angular headings are shown for each motor position, and indicate that flies align their body axis with the orientation of the e-vector (double-headed arrows) of linearly polarized light. The orientation of incident e-vectors is symbolized using double-headed arrows. (TIFF 1502 kb)
359_2014_910_MOESM2_ESM.tif
Supplemental Fig S2. Ventral behavior is not mediated by reflections. Series of controls confirming that ventral polarotaxis by flies walking upside down on the ceiling of the arena is not the result of POL stimuli being reflected off the arena floor. A series of modifications was added to the experimental setup (from left to right): the arena floor plate was tilted (either at 30° or 45°), was sanded, replaced by a non-reflecting surface), or by a nylon mesh. In all cases, polarotactic alignment behavior persisted, demonstrating that flies perceived the stimulus directly with their ventral eye. (TIFF 1291 kb)
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Velez, M.M., Wernet, M.F., Clark, D.A. et al. Walking Drosophila align with the e-vector of linearly polarized light through directed modulation of angular acceleration. J Comp Physiol A 200, 603–614 (2014). https://doi.org/10.1007/s00359-014-0910-6
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DOI: https://doi.org/10.1007/s00359-014-0910-6