Differences in Neural Circuitry Guiding Behavioral Responses to Polarized light Presented to Either the Dorsal or Ventral Retina in Drosophila

Abstract

Linearly polarized light (POL) serves as an important cue for many animals, providing navigational information, as well as directing them toward food sources and reproduction sites. Many insects detect the celestial polarization pattern, or the linearly polarized reflections off of surfaces, such as water. Much progress has been made toward characterizing both retinal detectors and downstream circuit elements responsible for celestial POL vision in different insect species, yet much less is known about the neural basis of how polarized reflections are detected. We previously established a novel, fully automated behavioral assay for studying the spontaneous orientation response of Drosophila melanogaster populations to POL stimuli presented to either the dorsal, or the ventral halves of the retina. We identified separate retinal detectors mediating these responses: the ‘Dorsal Rim Area’ (DRA), which had long been implicated in celestial POL vision, as well as a previously uncharacterized ‘ventral polarization area’ (VPA). In this study, we investigate whether DRA and VPA use the same or different downstream circuitry, for mediating spontaneous behavioral responses. We use homozygous mutants, or molecular genetic circuit-breaking tools (silencing, as well as rescue of synaptic activity), in combination with our behavioral paradigm. We show that responses to dorsal versus ventral stimulation involve previously characterized optic lobe neurons, like lamina monopolar cell L2 and medulla cell types Dm8/Tm5c. However, using different experimental conditions, we show that important differences exist between the requirement of these cell types downstream of DRA versus VPA. Therefore, while the neural circuits underlying behavioral responses to celestial and reflected POL cues share important building blocks, these elements play different functional roles within the network.

Keywords::

• Drosophila
• genetics
• behavior
• circuitry

ACKNOWLEDGMENTS

The authors thank Bob Schneeveis David Profitt, and Thomas Labhart for technical assistance. Julian Brown and Damon Clark have provided generous coding support. Marion Silies, Tina Schwabe, past and present members of the Clandinin lab provided tools, reagents, as well as helpful discussion. The Bloomington Fly Stock Center, Jaeseob Kim, Martin Heisenberg, and Chi-Hon Lee provided fly stocks.

Declaration of interest: The author reports no conflicts of interest. The author alone is responsible for the content and writing of the paper.

This work was supported by the Helen Hay Whitney Foundation (MFW), 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).