Neuroethology of cooperative behavior in Drosophila larvae

Cooperative behavior regularly emerges in biological systems. Although widely observed across animal species, cellular and molecular mechanisms underlying the establishment and maintenance of cooperative behaviors remain largely unknown. To characterize how the brain organizes cellular pathways to serve the needs of independent individuals and social groups, we investigated cooperative digging behavior in Drosophila larvae1. An individual larva’s ability to participate in a cooperative burrowing cluster relies on direct visual input as well as visual and social experience during development1. In addition, vision modulates cluster dynamics by promoting coordinated movements between pairs of larvae 1. To determine the specific pathways within the larval visual circuit underlying cooperative social clustering, we examined larval photoreceptors (PRs) and the downstream local interneurons (lOLPs) using anatomical and functional studies. Our results indicate that Rhodopsin 6-expressing-PRs (Rh6-PRs) and lOLPs are required for both cooperative clustering and movement detection2. Remarkably, visual deprivation and social isolation strongly impact the structural and functional connectivity between Rh6-PRs and lOLPs, while at the same time having no effect on the adjacent Rhodopsin 5-expressing PRs (Rh5-PRs)2. Together, our findings demonstrate that a specific larval visual pathway involved in social interactions undergoes experience-dependent modifications during development, suggesting that plasticity in sensory circuits could act as the cellular substrate for social learning. The described model provides an excellent system in which experimentally tractable complex behavior can be matched with a large-scale connectome.