Early Integration of Temperature and Humidity Stimuli in the Drosophila Brain

Dominic D. Frank, Anders Enjin, Genevieve C. Jouandet, Emanuela E. Zaharieva, Alessia Para, Marcus C. Stensmyr*, Marco Gallio

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

74 Scopus citations

Abstract

The Drosophila antenna contains receptor neurons for mechanical, olfactory, thermal, and humidity stimuli. Neurons expressing the ionotropic receptor IR40a have been implicated in the selection of an appropriate humidity range [1, 2], but although previous work indicates that insect hygroreceptors may be made up by a “triad” of neurons (with a dry-, a cold-, and a humid-air-responding cell [3]), IR40a expression included only cold- and dry-air cells. Here, we report the identification of the humid-responding neuron that completes the hygrosensory triad in the Drosophila antenna. This cell type expresses the Ir68a gene, and Ir68a mutation perturbs humidity preference. Next, we follow the projections of Ir68a neurons to the brain and show that they form a distinct glomerulus in the posterior antennal lobe (PAL). In the PAL, a simple sensory map represents related features of the external environment with adjacent “hot,” “cold,” “dry,” and “humid” glomeruli—an organization that allows for both unique and combinatorial sampling by central relay neurons. Indeed, flies avoided dry heat more robustly than humid heat, and this modulation was abolished by silencing of dry-air receptors. Consistently, at least one projection neuron type received direct synaptic input from both temperature and dry-air glomeruli. Our results further our understanding of humidity sensing in the Drosophila antenna, uncover a neuronal substrate for early sensory integration of temperature and humidity in the brain, and illustrate the logic of how ethologically relevant combinations of sensory cues can be processed together to produce adaptive behavioral responses.

Original languageEnglish (US)
Pages (from-to)2381-2388.e4
JournalCurrent Biology
Volume27
Issue number15
DOIs
StatePublished - Aug 7 2017

Funding

We wish to thank R. Benton for providing fly strains and reagents, Chao Wei for help with microscopy, and Tom Bozza and members of the Gallio and Stensmyr labs for valuable comments. Work in the Gallio lab is supported by NIH grant R01NS086859 (M.G.), the Pew Charitable Trust (M.G.), and NIH grant F31NS093873 (D.D.F.). Work in the Stensmyr lab is funded by the Crafoord Foundation (M.C.S.), Vetenskapsrådet (M.C.S.), Birgit och Sven Håkan Ohlssons Stiftelse (M.C.S.), Astrid och Gustaf Kaleens Fond (A.E.), Kungliga Fysiografiska Sallskapet (A.E.), and Wenner-Gren Stiftelse (A.E.).

Keywords

  • Drosophila melanogaster
  • humidity
  • hygrosensation
  • ionotropic receptor
  • multisensory integration
  • posterior antennal lobe
  • saccculus
  • temperature
  • thermosensation

ASJC Scopus subject areas

  • General Biochemistry, Genetics and Molecular Biology
  • General Agricultural and Biological Sciences

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