Investigating the Neural Circuits Underlying Binocular Distance Estimation in Drosophila

Abstract

Animals exhibit complex behaviors that require being able to precisely estimate the distance of a visual stimulus from the observer. Although monocular cues, or visual cues from one eye, are oftentimes sufficient for estimating distance, binocular vision facilitates computations like stereopsis to resolve binocular disparities of images seen by each eye and distinguish between stimuli that are truly different sizes or appear as so due to their distance. Thus far, no one has developed circuit-level predictions of stereopsis, bridging together binocular input processing with execution of naturalistic, distance-dependent behaviors. Here, we leverage the Drosophila melanogaster (fruit fly) connectome to investigate how stereopsis may facilitate distance-dependent behaviors, specifically in the context of courtship. Given that Lobula Columnar 14a1 (LC14a1) visual projection neurons connect the two visual processing areas of the brain (lobulae) and map only onto the very edge of the lobulae, which correspond with regions of binocular overlap, we predict these neurons may be involved in comparing binocular disparities for stereopsis computations. We recorded LC14a1 activity in awake, behaving male flies with two-photon calcium imaging and found that these neurons respond to female stimuli presented near the male. We additionally found that silencing LC14a1 neurons with tetanus toxin light chain (TNT) alters song choice at different distances, drives asymmetrical wing extensions during song, and increases lateral speed when circling around the female. Our preliminary results reveal that LC14a1 neurons facilitate courtship behaviors that require precise tracking of female position. These insights bridge together circuit-level predictions of stereopsis and behavioral experiments, demonstrating how neural wiring and circuitry facilitate visuomotor transformations to drive naturalistic, distance-dependent behavior.