Visual recognition of the female body axis drives spatial elements of male courtship in Drosophila melanogaster

Abstract

Like other mating behaviors, the courtship ritual exhibited by male Drosophila towards a virgin female is comprised of spatiotemporal sequences of innate behavioral elements. Yet, the specific stimuli and neural circuits that determine when and where males release individual courtship elements are not well understood. Here, we investigated the role of visual object recognition in the release of specific behavioral elements during bouts of male courtship. By using a computer vision and machine learning based approach for high-resolution analyses of the male courtship ritual, we show that the release of distinct behavioral elements occur at stereotyped locations around the female and depends on the ability of males to recognize visual landmarks present on the female.Specifically, we show that independent of female motion, males utilize unique populations of visual projection neurons to recognize the eyes of a target female, which is essential for the release of courtship behaviors at their appropriate spatial locations. Together, these results provide a mechanistic explanation for how relatively simple visual cues could play a role in driving both spatiallyand temporally-complex social interactions.

Behavioral signatures of structured feature detection during courtship in Drosophila

“…13,[17][18][19][20]23 Besides, specific visual projection neurons have been found to mediate directed courtship. 16,23 Behavioral patterns similar to circling as we define here have been described before in natural 7,18,22,24 or tethered [72][73][74] states in different species. [75][76][77] Under restrained state, earlier studies showed that compromised visual input reduces courtship efficiency, and vision is adequate for the control of courtship tracking 14,72 ; more specifically, both vision and olfaction are implicated in moving behind the female, whereas vision is implicated for courtship near the head.…”

Neural Network Organization for Courtship Song Feature Detection inDrosophila

“…7; see Methods). The two optic glomeruli with the most innervation by our WED/VLP cell classes were LC9 and LC11, both containing small object-detecting visual neurons that might be important for courtship behaviors (Bidaye et al, 2020; Keleş and Frye, 2017; McKinney and Ben-Shahar, 2019). The LC9 glomerulus is exclusively innervated by neurons that prefer pulse stimuli whereas the LC11 glomerulus is mostly innervated by neurons that prefer sine stimuli (Supp.…”

Two Brain Pathways Initiate Distinct Forward Walking Programs in Drosophila

“…To test if P9 receives excitatory functional inputs from pC1 (Koganezawa et al, 2016) or five LC neural classes implicated in object tracking, courtship or figure detection (Keles ¸and Frye, 2017;Kohatsu et al, 2011;Ribeiro et al, 2018;McKinney and Ben-Shahar, 2018;Aptekar et al, 2015), we monitored responses in P9 by GCaMP6s calcium imaging while optogenetically activating upstream candidates with Chrimson. pC1 or LC9 activation produced reliable calcium transients in P9 (Figures 3B and 3C).…”