Electrical synapses mediate visual approach behavior

Abstract

Detecting salient visual objects and orienting toward them are commonplace tasks for animals, yet the underlying neural circuits remain poorly understood. The fruit fly is an ideal model for a comprehensive analysis of feature detection mechanisms given its complete synaptic wiring diagrams, robust behavioral assays, and cell-type-specific gene expression datasets. We previously showed that columnar T3 neurons are required for saccadic orientation toward landscape features during flight. Here, we examine how signals downstream of T3 are processed in the central brain. We identify LC17 visual projection neurons as key postsynaptic targets: they receive strong excitatory input from T3, project to premotor brain regions, and are thus positioned to support visual approach. Using in vivo optical physiology and virtual reality behavior, we demonstrate that LC17 neurons are indeed necessary for object tracking during flight. Furthermore, we find that electrical synapses in LC17 are also required for tracking behavior. We show that the innexin Shaking B (shakB) is highly expressed in LC17 and localized to its dendrites, and genetic perturbations confirm its essential role for electrical coupling in this circuit. Our findings reveal mechanisms underlying visual approach, and highlight the interplay between electrical and chemical neurotransmission for rapid object detection and action selection.