Paper

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

Zung, Jessica L, Zhao, Zhilei, Iqbal, Azwad, Kriete, Alexis L, Strauch, Martin, Matthews, Benjamin J, Merhof, Dorit, Younger, Meg A, Mcbride, Carolyn S, Thiberge, Stephan

2020

Overview

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.

• Publisher: Cold Spring Harbor Laboratory Press,Cold Spring Harbor Laboratory
• Subject: Aedes aegypti / Aldehydes / Antennal lobe / Attractants / Biting / Dengue fever / Lipids / Mosquitoes / Nectar / Neural coding / Neuroscience / Olfactory discrimination / Olfactory discrimination learning / Olfactory glomeruli / Yellow fever