A single class of visual neurons drive avoidance flight turns in response to both approaching or horizontally moving objects

Abstract

Visual object detection is crucial for the following behaviors in diverse animal species, including fruit flies: avoiding threats, foraging, and mating. Especially, detecting a looming predator and responding incorrect manner is one of the most critical visuomotor function for survival. Loom detecting neurons have been studied previously in various animals including Drosophila melanogaster. A recent study shows that LPLC2 and LC4 visual neurons respond to a looming pattern in a walking or resting fly. They directly activate the giant fiber descending neurons, which trigger the escape jump for taking-off. For specimens in flight, however, it is unclear which neurons mediate loom-induced escape flight maneuvers. Furthermore, in the case of flying Drosophila, similar escape maneuvers are shown to be executed in response to small horizontally moving objects. However, the neural circuit underneath it remains to be studied. Using thermogenetic inactivation and optogenetic activation screening in conjunction with in-vivo calcium-imaging experiments, we studied visual neurons that were important for visually induced escape flight turns. In particular, we show that LPLC2 neurons respond both to a looming and horizontally moving object and induce escape turns in flying Drosophila. It defines these neurons as an escape-inducing neuron in response to multiple visual features. We also show that the two distinct visual features –– a loom and a horizontally moving spot –– arrive at LPLC2 neurons from two distinct visual structures: the lobula plate for the looming pattern and the lobula for the horizontally moving spot. Together, our findings highlight a shared use of a single class of sensory neurons in multiple motor contexts –– in flight and walking –– as well as in response to multiple visual patterns that are required to cause motor actions of similar characteristics.