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 language | English (US) |
|---|---|
| Pages (from-to) | 2381-2388.e4 |
| Journal | Current Biology |
| Volume | 27 |
| Issue number | 15 |
| DOIs | |
| State | Published - Aug 7 2017 |
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Keywords
- Drosophila melanogaster
- humidity
- hygrosensation
- ionotropic receptor
- multisensory integration
- posterior antennal lobe
- saccculus
- temperature
- thermosensation
ASJC Scopus subject areas
- Biochemistry, Genetics and Molecular Biology(all)
- Agricultural and Biological Sciences(all)
Cite this
}
Early Integration of Temperature and Humidity Stimuli in the Drosophila Brain. / Frank, Dominic D.; Enjin, Anders; Jouandet, Genevieve C.; Zaharieva, Emanuela E.; Para, Alessia; Stensmyr, Marcus C.; Gallio, Marco.
In: Current Biology, Vol. 27, No. 15, 07.08.2017, p. 2381-2388.e4.Research output: Contribution to journal › Article
TY - JOUR
T1 - Early Integration of Temperature and Humidity Stimuli in the Drosophila Brain
AU - Frank, Dominic D.
AU - Enjin, Anders
AU - Jouandet, Genevieve C.
AU - Zaharieva, Emanuela E.
AU - Para, Alessia
AU - Stensmyr, Marcus C.
AU - Gallio, Marco
PY - 2017/8/7
Y1 - 2017/8/7
N2 - 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.
AB - 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.
KW - Drosophila melanogaster
KW - humidity
KW - hygrosensation
KW - ionotropic receptor
KW - multisensory integration
KW - posterior antennal lobe
KW - saccculus
KW - temperature
KW - thermosensation
UR - http://www.scopus.com/inward/record.url?scp=85025432905&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85025432905&partnerID=8YFLogxK
U2 - 10.1016/j.cub.2017.06.077
DO - 10.1016/j.cub.2017.06.077
M3 - Article
C2 - 28736172
AN - SCOPUS:85025432905
VL - 27
SP - 2381-2388.e4
JO - Current Biology
JF - Current Biology
SN - 0960-9822
IS - 15
ER -