Sensory integration by descending interneurons in the flying fruit fly

Abstract

A flying fly relies on many senses, including vision, olfaction, and mechanosensation, to navigate through the world and locate an attractive food source. How are these sensory signals integrated in the central brain and relayed to the motor system to guide behavior? Integration of multiple sensory signals can be performed by descending interneurons, which relay this information to motor systems via circuits in the thoracic ganglion. We have identified a group of three descending interneurons in the fruit fly that integrate information from discrete sets of visual interneurons. Each exhibits a distinct preference for optic flow corresponding to self-motion. We measured the tuning properties of the presynaptic visual interneurons, and found that a simple linear model based on these inputs can explain much of the response of the descending interneurons. Projection patterns of the three descending interneurons in the thoracic ganglion suggest that they deliver self-motion information to circuits that control movement of the head, wings, and abdomen. We monitored the output of these motor systems during tethered flight and found evidence that suggests that these three neurons are involved in distinct motor programs. This circuit may play a crucial role in sensory-motor tranformations used to guide stable flight, and provides insight into strategies employed by other flying insects.

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