A Visual Pathway into Central Complex for High-Frequency Motion-Defined Bars in Drosophila

Relative motion breaks a camouflaged target from a same-textured background, thus eliciting discrimination of a motion defined object. Ring (R) neurons are critical components in the Drosophila central complex, which has been implicated in multiple visually guided behaviors. Using two-photon calcium imaging with female flies, we demonstrated that a specific population of R neurons that innervate the superior domain of bulb neuropil, termed superior R neurons, encoded a motion defined bar with high spatial frequency contents. Upstream superior tuberculo-bulbar (TuBu) neurons transmitted visual signals by releasing acetylcholine within synapses connected with superior R neurons. Blocking TuBu or R neurons impaired tracking performance of the bar, which reveals their importance in motion-defined feature encoding. Additionally, the presentation of a low spatial frequency luminance-defined bar evoked consistent excitation in R neurons of the superior bulb, whereas either excited or inhibited responses were evoked in the inferior bulb. The distinct properties of the responses to the two bar stimuli indicate there is a functional division between the bulb subdomains. Moreover, physiological and behavioral tests with restricted lines suggest that R4d neurons play a vital role in tracking motion-defined bars. We conclude that the central complex receives the motion-defined features via a visual pathway from superior TuBu to R neurons and might encode different visual features via distinct response patterns at the population level, thereby driving visually guided behaviors.

Automated summary

Relative motion separates a camouflaged target from its background, leading to discrimination of a motion-defined object. R neurons in the Drosophila central complex, particularly the superior R neurons, play a crucial role in encoding motion features. These neurons receive visual signals from upstream TuBu neurons and their impairment affects tracking performance. Furthermore, the different responses of R neurons in the superior and inferior bulb to different bar stimuli suggest a functional division between the bulb subdomains. R4d neurons are found to be vital in tracking motion-defined bars.