Polarization Sensitivity in the Vinegar Fly, Drosophila melanogaster

The molecular-genetic model organism of the vinegar fly, Drosophila melanogaster, is widely believed to be a behavioural generalist, merely a local scavenger without much need for navigational skills. However, for nearly 50 years, it has been known that the anatomical substrates for polarization vision in insects, morphologically and molecularly specialized ommatidia in the ‘dorsal rim area’ (DRA), also exist in the adult eye of Drosophila. Furthermore, several independent studies since 1980 have reported behavioural responses of both walking and flying vinegar flies to changing angles of polarization. However, both the ethological meaning of these responses and the underlying circuit mechanisms remained unknown. Over the last 10 years, several studies have now added important new insights, revealing that Drosophila shares all of the basic anatomical, physiological, and behavioural features of polarization vision with its larger relatives. Several anatomical studies have now described those cell types that together form the ‘anterior visual pathway’ (AVP), connecting both eyes with the central complex (CX), where cells strikingly similar to mammalian head-direction cells can be found. This AVP is conserved across insects and receives strong input from the DRA of both eyes. Furthermore, cell types along every stage of the Drosophila AVP were demonstrated to be polarization-sensitive, leading to a representation of skylight information from the optic lobes to the CX. Finally, vinegar flies were shown to be capable of using celestial polarization stimuli as a reference for selecting arbitrary but stable headings, a behaviour resembling those of many other insect species seeking straight courses for dispersal or navigation. Given the molecular-genetic toolkit for manipulating cell types in a reversible and predictable manner, together with more recent full-brain, electron microscopy-based connectomic resources, Drosophila has now emerged as a powerful model system for understanding how a small insect brain processes navigational information from the celestial pattern of polarized skylight.