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

Abstract

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.SIGNIFICANCE STATEMENT Animals could discriminate a motion-defined object that is indistinguishable with a same-textured background until it moves, but little is known about the underlying neural mechanisms. In this study, we identified that R neurons and their upstream partners, TuBu neurons, innervating the superior bulb of Drosophila central brain are involved in the discrimination of high-frequency motion-defined bars. Our study provides new evidence that R neurons receive multiple visual inputs from distinct upstream neurons, indicating a population coding mechanism for the fly central brain to discriminate diverse visual features. These results build progress in unraveling neural substrates for visually guided behaviors.