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
27(15).
p.4-2388
- 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.
(Less)
- author
- Frank, Dominic D
; Enjin, Anders
LU
; Jouandet, Genevieve C.
; Zaharieva, Emanuela E
; Para, Alessia
; Stensmyr, Marcus C.
LU
and Gallio, Marco
- organization
- publishing date
- 2017-08
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- Drosophila melanogaster, Humidity, Hygrosensation, Ionotropic receptor, Multisensory integration, Posterior antennal lobe, Saccculus, Temperature, Thermosensation
- in
- Current Biology
- volume
- 27
- issue
- 15
- pages
- 4 - 2388
- publisher
- Elsevier
- external identifiers
-
- scopus:85025432905
- wos:000407034300035
- pmid:28736172
- 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
- 2024-03-31 13:55:42
@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}},
keywords = {{Drosophila melanogaster; Humidity; Hygrosensation; Ionotropic receptor; Multisensory integration; Posterior antennal lobe; Saccculus; Temperature; Thermosensation}},
language = {{eng}},
number = {{15}},
pages = {{4--2388}},
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}},
doi = {{10.1016/j.cub.2017.06.077}},
volume = {{27}},
year = {{2017}},
}