In Drosophila, rapid temperature changes are detected at the periphery by dedicated receptors forming a simple sensory map for hot and cold in the brain1. However, flies show a host of complex innate and learned responses to temperature, indicating that they are able to extract a range of information from this simple input. Here we define the anatomical and physiological repertoire for temperature representation in the Drosophila brain. First, we use a photolabelling strategy2 to trace the connections that relay peripheral thermosensory information to higher brain centres, and show that they largely converge onto three target regions: the mushroom body, the lateral horn (both of which are well known centres for sensory processing) and the posterior lateral protocerebrum, a region we now define as a major site of thermosensory representation. Next, using in vivo calcium imaging3, we describe the thermosensory projection neurons selectively activated by hot or cold stimuli. Fast-adapting neurons display transient ON and OFF responses and track rapid temperature shifts remarkably well, while slow-adapting cell responses better reflect the magnitude of simple thermal changes. Unexpectedly, we also find a population of broadly tuned cells that respond to both heating and cooling, and show that they are required for normal behavioural avoidance of both hot and cold in a simple two-choice temperature preference assay. Taken together, our results uncover a coordinated ensemble of neural responses to temperature in the Drosophila brain, demonstrate that a broadly tuned thermal line contributes to rapid avoidance behaviour, and illustrate how stimulus quality, temporal structure, and intensity can be extracted from a simple glomerular map at a single synaptic station.
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We thank V. Ruta and B. Noro for providing PA-GFP flies and reagents, and especially G. Rubin for providing access to the FlyLight collection before publication. We are grateful to N. Ryba, D. Yarmolinsky, C. Zuker and members of the Gallio laboratory for critical comments on the manuscript. Z. Turan and A. Kuang provided technical assistance and we thank C. Ulmer and a number of undergraduate students for fly husbandry. This work was supported by NIH grant 1R01NS086859-01 (to M.G.) and by training grant 2T32MH067564 (to D.D.F.).
Extended data figures
This file contains Supplementary Tables listing the genotypes relevant to this study.
About this article
Scientific Reports (2019)