A visual pathway for skylight polarization processing in Drosophila.

Ben J Hardcastle,Natalie K Boyd,Bao-Chau M Nguyen,Pratyush Kandimalla,Jaison J Omoto,Volker Hartenstein,Mehmet F Keleş,Mark A Frye

doi:10.7554/elife.63225

Abstract

Many insects use patterns of polarized light in the sky to orient and navigate. Here, we functionally characterize neural circuitry in the fruit fly, Drosophila melanogaster, that conveys polarized light signals from the eye to the central complex, a brain region essential for the fly's sense of direction. Neurons tuned to the angle of polarization of ultraviolet light are found throughout the anterior visual pathway, connecting the optic lobes with the central complex via the anterior optic tubercle and bulb, in a homologous organization to the 'sky compass' pathways described in other insects. We detail how a consistent, map-like organization of neural tunings in the peripheral visual system is transformed into a reduced representation suited to flexible processing in the central brain. This study identifies computational motifs of the transformation, enabling mechanistic comparisons of multisensory integration and central processing for navigation in the brains of insects.

Highlights

A critical challenge of active locomotion is knowing the right way to go
Within a narrow strip of skyward-facing ommatidia in each eye, known as the dorsal rim area (DRA), each R7/R8 pair is sensitive to a different angle of polarization (AoP, referred to as the e-vector orientation), organized in a ’polarotopic’ fashion (Figure 1A)
We found that DmDRA1-split driving trans-Tango labeled a population of neurons in the dorsal medulla that project to the small, lateral subunit of the anterior optic tubercle (AOTU) via a fiber bundle in the anterior optic tract (AOT) (Figure 2B), and matched the anatomy of MeTu neurons (Figure 2A)

Summary

Introduction

A critical challenge of active locomotion is knowing the right way to go. Sensorimotor reflexes can influence momentary changes in direction to hold a course or to avoid looming threats, but goaldirected behaviors, such as returning to a previous location from unfamiliar surroundings, require additional information and processing (Braitenberg, 1986; Gomez-Marin et al, 2010). Recent studies in Drosophila have revealed that activity in a network of CX neurons encodes and maintains a representation of the animal’s angular heading relative to its environment (Kim et al, 2017; Seelig and Jayaraman, 2015), with similarity to head-direction cells in vertebrates (Taube et al, 1990) This neural representation of heading can be updated by internal, proprioceptive estimates of self-motion during locomotion, and by external cues, such as moving visual patterns and directional airflow (Fisher et al, 2019; Green et al, 2017; Kim et al, 2019; Okubo et al, 2020; Shiozaki et al, 2020).

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