Fruit Fly Navigation in the Presence of Visual Compass Cues

Abstract

When moving through dense environments like a forest or traversing sparse landscapes like a desert, animals use bright, reliable visual cues like the position of the Sun or the polarisation pattern of the Sky to get their bearings. The architecture of the brains of tiny fruit flies suggests that they too might use multiple visual “compass” cues to determine their heading direction. We asked whether fruit flies can use gradients of light intensity (which mimic the sky) to navigate. We presented flies with sinusoidal intensity gradients in a virtual reality arena and found that flies maintain arbitrary but consistent heading directions over several minutes. The higher the contrast modulation of the intensity gradient, the straighter the flies were able to walk. We imaged neurons in the central brain of the fly which carry an internal representation of heading direction and found that the stability of the internal representation is correlated with the ability of the fly to maintain a straight course. When we genetically silenced these neurons, flies could no longer choose arbitrary headings but instead fixated towards the dark part of the gradients. Flies that were initially shown a small bright disk that simulated the sun had more stable internal representations and were more likely to choose arbitrary headings. They were also able to maintain a straight course even when the sun and gradient cues were put in conflict with each other. Together, our experiments highlight how animals navigate in the presence of unreliable and conflicting visual cues in their natural environment.