Thermosensory perception regulates speed of movement in response to temperature changes in Drosophila melanogaster

Temperature influences the physiology and behavior of all organisms. For ectotherms, which lack central temperature regulation, temperature adaptation requires sheltering from or moving to a heat source. As temperature constrains the rate of metabolic reactions, it can directly affect ectotherm physiology and thus behavioral performance. This direct effect is particularly relevant for insects, as their small bodies readily equilibrate with ambient temperature. In fact, models of enzyme kinetics applied to insect behavior predict performance at different temperatures suggesting that thermal physiology governs behavior. However, insects also possess thermosensory neurons critical for locating preferred temperatures, showing cognitive control. This suggests that temperature-related behavior can emerge directly from a physiological effect, indirectly as a consequence of thermosensory processing, or through a combination of both. To separate the roles of thermal physiology and cognitive control, we developed an arena that allows fast temperature changes in time and space, and in which animals' movements are automatically quantified. We exposed wild-type Drosophila melanogaster and thermosensory receptor mutants to a dynamic temperature environment and tracked their movements. The locomotor speed of wild-type flies closely matched models of enzyme kinetics, but the behavior of thermosensory mutants did not. Mutations in thermosensory receptor gene dTrpA1 (Transient Receptor Potential A1) expressed in the brain resulted in a complete lack of response to temperature changes, while mutations in peripheral thermosensory receptor gene Gr28b(D) resulted in a diminished response. We conclude that flies react to temperature through cognitive control, informed by interactions between various thermosensory neurons, the behavioral output of which resembles models of enzyme kinetics.