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Early Integration of Temperature and Humidity Stimuli in the Drosophila Brain

Frank, Dominic D; Enjin, Anders LU ; Jouandet, Genevieve C.; Zaharieva, Emanuela E; Para, Alessia; Stensmyr, Marcus C. LU and Gallio, Marco (2017) In Current Biology
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 [], 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 []), 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... (More)

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 [], 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 []), 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. Frank et al. describe humid-air receptors in the fly antenna. Previous work identified dry-air receptors, and they now show that humid and dry cells converge with thermosensory neurons in the brain, creating a sensory map for environmental parameters. They also describe second-order neurons that sample multiple modalities for early integration.

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author
organization
publishing date
type
Contribution to journal
publication status
epub
subject
keywords
Drosophila melanogaster, Humidity, Hygrosensation, Ionotropic receptor, Multisensory integration, Posterior antennal lobe, Saccculus, Temperature, Thermosensation
in
Current Biology
publisher
Elsevier
external identifiers
  • scopus:85025432905
  • wos:000407034300035
ISSN
0960-9822
DOI
10.1016/j.cub.2017.06.077
language
English
LU publication?
yes
id
385f3842-5799-4565-9495-28f20e398cee
date added to LUP
2017-07-31 13:26:05
date last changed
2017-09-18 11:40:33
@article{385f3842-5799-4565-9495-28f20e398cee,
  abstract     = {<p>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 [], 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 []), 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. Frank et al. describe humid-air receptors in the fly antenna. Previous work identified dry-air receptors, and they now show that humid and dry cells converge with thermosensory neurons in the brain, creating a sensory map for environmental parameters. They also describe second-order neurons that sample multiple modalities for early integration.</p>},
  author       = {Frank, Dominic D and Enjin, Anders and Jouandet, Genevieve C. and Zaharieva, Emanuela E and Para, Alessia and Stensmyr, Marcus C. and Gallio, Marco},
  issn         = {0960-9822},
  keyword      = {Drosophila melanogaster,Humidity,Hygrosensation,Ionotropic receptor,Multisensory integration,Posterior antennal lobe,Saccculus,Temperature,Thermosensation},
  language     = {eng},
  month        = {07},
  publisher    = {Elsevier},
  series       = {Current Biology},
  title        = {Early Integration of Temperature and Humidity Stimuli in the Drosophila Brain},
  url          = {http://dx.doi.org/10.1016/j.cub.2017.06.077},
  year         = {2017},
}