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Chemical signatures of human odour generate a unique neural code in the brain of Aedes aegypti mosquitoes

View ORCID ProfileZhilei Zhao, View ORCID ProfileJessica L. Zung, View ORCID ProfileAlexis L. Kriete, View ORCID ProfileAzwad Iqbal, View ORCID ProfileMeg A. Younger, View ORCID ProfileBenjamin J. Matthews, View ORCID ProfileDorit Merhof, View ORCID ProfileStephan Thiberge, View ORCID ProfileMartin Strauch, View ORCID ProfileCarolyn S. McBride
doi: https://doi.org/10.1101/2020.11.01.363861
Zhilei Zhao
1Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08544 USA
2Bezos Center for Neural Circuit Dynamics, Princeton University, Princeton, NJ 08544 USA
3Department of Ecology & Evolutionary Biology, Princeton University, Princeton, NJ 08544 USA
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  • For correspondence: csm7@princeton.edu zhileiz@princeton.edu
Jessica L. Zung
1Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08544 USA
3Department of Ecology & Evolutionary Biology, Princeton University, Princeton, NJ 08544 USA
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Alexis L. Kriete
1Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08544 USA
3Department of Ecology & Evolutionary Biology, Princeton University, Princeton, NJ 08544 USA
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Azwad Iqbal
1Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08544 USA
3Department of Ecology & Evolutionary Biology, Princeton University, Princeton, NJ 08544 USA
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Meg A. Younger
4Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY 10065 USA
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Benjamin J. Matthews
4Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY 10065 USA
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Dorit Merhof
5Institute of Imaging & Computer Vision, RWTH Aachen University, 52074 Aachen, Germany
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Stephan Thiberge
1Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08544 USA
2Bezos Center for Neural Circuit Dynamics, Princeton University, Princeton, NJ 08544 USA
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Martin Strauch
5Institute of Imaging & Computer Vision, RWTH Aachen University, 52074 Aachen, Germany
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Carolyn S. McBride
1Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08544 USA
2Bezos Center for Neural Circuit Dynamics, Princeton University, Princeton, NJ 08544 USA
3Department of Ecology & Evolutionary Biology, Princeton University, Princeton, NJ 08544 USA
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  • For correspondence: csm7@princeton.edu zhileiz@princeton.edu
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Abstract

A globally invasive form of the mosquito Aedes aegypti specializes in biting humans, making it an efficient vector of dengue, yellow fever, Zika, and chikungunya viruses. Host-seeking females strongly prefer human odour over the odour of non-human animals, but exactly how they distinguish the two is not known. Vertebrate odours are complex blends of volatile chemicals with many shared components, making discrimination an interesting sensory coding challenge. Here we show that human and animal odour blends evoke activity in unique combinations of olfactory glomeruli within the Aedes aegypti antennal lobe. Human blends consistently activate a ‘universal’ glomerulus, which is equally responsive to diverse animal and nectar-related blends, and a more selective ‘human-sensitive’ glomerulus. This dual signal robustly distinguishes humans from animals across concentrations, individual humans, and diverse animal species. Remarkably, the human-sensitive glomerulus is narrowly tuned to the long-chain aldehydes decanal and undecanal, which we show are consistently enriched in (though not specific to) human odour and which likely originate from unique human skin lipids. We propose a model of host-odour coding wherein normalization of activity in the human-sensitive glomerulus by that in the broadly-tuned universal glomerulus generates a robust discriminatory signal of the relative concentration of long-chain aldehydes in a host odour blend. Our work demonstrates how animal brains may distil complex odour stimuli of innate biological relevance into simple neural codes and reveals novel targets for the design of next-generation mosquito-control strategies.

Competing Interest Statement

Princeton University has filed a patent (US 62/705,910, status pending) for using synthetic blends that mimic the response to human odour in the mosquito brain as mosquito attractants, listing C.S.M. and Z.Z. as inventors. Other authors declare no competing interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted November 02, 2020.
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Chemical signatures of human odour generate a unique neural code in the brain of Aedes aegypti mosquitoes
Zhilei Zhao, Jessica L. Zung, Alexis L. Kriete, Azwad Iqbal, Meg A. Younger, Benjamin J. Matthews, Dorit Merhof, Stephan Thiberge, Martin Strauch, Carolyn S. McBride
bioRxiv 2020.11.01.363861; doi: https://doi.org/10.1101/2020.11.01.363861
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Chemical signatures of human odour generate a unique neural code in the brain of Aedes aegypti mosquitoes
Zhilei Zhao, Jessica L. Zung, Alexis L. Kriete, Azwad Iqbal, Meg A. Younger, Benjamin J. Matthews, Dorit Merhof, Stephan Thiberge, Martin Strauch, Carolyn S. McBride
bioRxiv 2020.11.01.363861; doi: https://doi.org/10.1101/2020.11.01.363861

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