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Fundamentals of thermosensory navigation in Drosophila

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Processing of sensory information in the brain is a pervasive and fundamental phenomenon across animal species and is involved in both "hard-wired" innate responses as well as learned and adaptive behaviors. Here, I show that the avoidance of hot temperature, a simple innate behavior, contains unexpected plasticity and complex processing in Drosophila. First, I demonstrate that the hot receptor neurons of the antenna and their molecular heat sensor, Gr28B.d, are essential for flies to produce escape turns away from heat. By integrating modeling of the thermal environment with behavioral data, I show that even minute temperature differences (0.1°C-1.0°C) between the antennae are sufficient to determine turning direction. Based on these measurements, I evolve a fly/vehicle model with two symmetrical sensors and motors (a "Braitenberg vehicle") which closely approximates basic fly thermotaxis. Critical differences between real flies and the hard-wired vehicle reveal that fly heat avoidance involves decision-making, relies on rapid learning, and is robust to new conditions, features generally associated with more complex behavior. Next, I show that the innocuous heat sensors are also involved in processing of diffuse thermal signals, and identify key neural circuitry enabling flies to chart a course away from dangerous heat. By comparing fly behavior with that of a modified vehicle model, I find that separate but interacting processing underlies navigation of steep and shallow thermal gradients.

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