Journal of Chemical Ecology

, Volume 44, Issue 12, pp 1120–1126 | Cite as

Neuronal Responses of Antennal Olfactory Sensilla to Insect Chemical Repellents in the Yellow Fever Mosquito, Aedes aegypti

  • Zhou Chen
  • Feng Liu
  • Nannan LiuEmail author


The yellow fever mosquito, Aedes aegypti, is a vector of many human diseases such as yellow fever, dengue fever, and Zika. As insecticide resistance has been widely reported, chemical repellents have been adopted as alternative options for mosquito and mosquito-borne disease control. This study characterized the responses of olfactory receptor neurons (ORNs) in different types of antennal olfactory sensilla in Ae. aegypti to 48 chemicals that exhibited repellent activity in various insect species. Both excitatory and inhibitory responses were observed from ORNs in response to these chemicals and differential tuning properties were also observed among ORNs. Remarkable excitatory responses were recorded from the ORNs in sensilla SST1, SST2, SBTI, SBTII, and LST2, while inhibitory activities were detected from a neuron in sensillum SST2 in response to several terpene/terpenoid compounds. Moreover, the temporal dynamics of neuronal responses were found to be compound-specific and concentration-dependent. Hierarchical cluster analysis and principal component analysis of the response to each compound across ORNs in seven types of olfactory sensilla in Ae. aegypti revealed that odor reception depended not only on chemical class but also specific chemical structure. Results of this study give new insights into the sensory physiology of Aedes mosquitoes to the chemical repellents and should contribute to the development of new repellent reagents for human protection.


Aedes aegypti Single sensillum recording Olfactory receptor neuron Inhibitory neuron Odor space 



This project was supported by Award Alabama Agricultural Experiment Station (AAES) Multistate/Hatch Grants ALA08-045 and ALA015-1-10026 to N.L. The Orlando strain used in this study was a generous gift from Dr. James Becnel (USDA, ARS, Mosquito and Fly Research Unit). The authors thank two anonymous reviewers for their valuable comments on the manuscript.

Authors’ contributions

Conceived and designed the study: NL, ZC, and F.L. Performed the experiments: ZC. Prepared the materials: NL. Wrote the paper: NL, ZC, and FL.


This project was supported by Award Alabama Agricultural Experiment Station (AAES) Multistate/Hatch Grants ALA08–045 and ALA015–1-10026 to N.L.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interests.

Supplementary material

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ESM 1 (DOCX 40 kb)


  1. Ansari MA, Vasudevan P, Tandon M, Razdan RK (2000) Larvicidal and mosquito repellent action of peppermint (Mentha piperita) oil. Bioresour Technol 71:267–271CrossRefGoogle Scholar
  2. Boeckh J, Kaissling KE, Schneider D (1965) Insect olfactory receptors. Cold Spring Harb Symp Quant Biol 30:263–280CrossRefGoogle Scholar
  3. Campbell C, Gries R, Gries G (2011) Forty-two compounds in eleven essential oils elicit antennal responses from Aedes aegypti. Entomol Exp Appl 138:21–32CrossRefGoogle Scholar
  4. Cao LH, Yang D, Wu W, Zeng X, Jing BY, Li MT, Qin SS, Tang C, Tu YH, Luo DG (2017) Odor-evoked inhibition of olfactory sensory neurons drives olfactory perception in Drosophila. Nat Commun 8:1–13CrossRefGoogle Scholar
  5. Carey AF, Wang G, Su CY, Laurence JZ, Carlson JR (2010) Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464:66–71CrossRefGoogle Scholar
  6. De Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30:537–552CrossRefGoogle Scholar
  7. DeGennaro M, McBride CS, Seeholzer L, Nakagawa T, Dennis EJ, Goldman C, Jasinskiene N, James AA, Vosshall LB (2013) Orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET. Nature 498:487–491CrossRefGoogle Scholar
  8. Den Otter CJ, Behan M, Maes FW (1980) Single cell responses in female Pieris brassicae (Lepidoptera: Pieridae) to plant volatiles and conspecific egg odours. J Insect Physiol 26:465–472CrossRefGoogle Scholar
  9. Fradin MS, Day JF (2002) Comparative efficacy of insect repellents against mosquito bites. N Engl J Med 347:13–18CrossRefGoogle Scholar
  10. Gertler S (1946) Nu, nu-diethylbenzamide as an insect repelle. US Pat 2,408,389. Washington DC: U.S. Patent and Trademark OfficeGoogle Scholar
  11. Ghaninia M, Ignell R, Hansson BS (2007) Functional classification and central nervous projections of olfactory receptor neurons housed in antennal trichoid sensilla of female yellow fever mosquitoes, Aedes aegypti. Eur J Neurosci 26:1611–1623CrossRefGoogle Scholar
  12. Gubler DJ (2004) The changing epidemiology of yellow fever and dengue, 1900 to 2003: full circle? Comp Immunol Microbiol Infect Dis 27:319–330CrossRefGoogle Scholar
  13. Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125:143–160CrossRefGoogle Scholar
  14. Hill S, Hansson BS, Ignell R (2009) Characterization of antennal trichoid sensilla from female southern house mosquito, Culex quinquefasciatus say. Chem Senses 34:231–252CrossRefGoogle Scholar
  15. Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66CrossRefGoogle Scholar
  16. Joseph RM, Carlson JR (2015) Drosophila chemoreceptors: a molecular interface between the chemical world and the brain. Trends Genet 31:683–695CrossRefGoogle Scholar
  17. Laurent G, Wehr M, Davidowitz H (1996) Temporal representations of odors in an olfactory network. J Neurosci 16:3837–3847CrossRefGoogle Scholar
  18. Lei H, Christensen TA, Hildebrand JG (2004) Spatial and temporal organization of ensemble representations for different odor classes in the moth antennal lobe. J Neurosci 24:11108–11119CrossRefGoogle Scholar
  19. Liu N (2015) Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu Rev Entomol 60:537–559CrossRefGoogle Scholar
  20. Liu F, Liu N (2015) Human odorant reception in the common bed bug, Cimex lectularius. Sci Rep 5:15558CrossRefGoogle Scholar
  21. Liu F, Chen L, Appel AG, Liu N (2013) Olfactory responses of the antennal trichoid sensilla to chemical repellents in the mosquito, Culex quinquefasciatus. J Insect Physiol 59:1169–1177CrossRefGoogle Scholar
  22. Liu F, Haynes KF, Appel AG, Liu N (2014) Antennal olfactory sensilla responses to insect chemical repellents in the common bed bug, Cimex lectularius. J Chem Ecol 40:522–533CrossRefGoogle Scholar
  23. Liu F, Xiong C, Liu N (2017) Chemoreception to aggregation pheromones in the common bed bug, Cimex lectularius. Insect Biochem Mol Biol 82:62–73CrossRefGoogle Scholar
  24. Marchette N, Garcia R, Rudnick A (1969) Isolation of Zika virus from Aedes aegypti mosquitoes in Malaysia. Am J Trop Med Hyg 18:411–415CrossRefGoogle Scholar
  25. Matthews BJ, McBride CS, DeGennaro M, Despo O, Vosshall LB (2016) The neurotranscriptome of the Aedes aegypti mosquito. BMC Genomics 17:32CrossRefGoogle Scholar
  26. McBride CS, Baier F, Omondi AB, Spitzer SA, Lutomiah J, Sang R, Ignell R, Vosshall LB (2014) Evolution of mosquito preference for humans linked to an odorant receptor. Nature 515:222–227CrossRefGoogle Scholar
  27. McIver S (1978) Structure of sensilla trichodea of female Aedes aegypti with comments on innervation of antennal sensilla. J Insect Physiol 24:383–390CrossRefGoogle Scholar
  28. Monath TP (2001) Yellow fever: an update. Lancet Infect Dis 1:11–20CrossRefGoogle Scholar
  29. Nakagawa T, Sakurai T, Nishioka T (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307:1638–1642CrossRefGoogle Scholar
  30. Qiu Y, Van Loon JJ, Takken W, Meijerink J, Smid HM (2006) Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae. Chem Senses 31:845–863CrossRefGoogle Scholar
  31. Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1006CrossRefGoogle Scholar
  32. Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odor discrimination on desynchronization of odor–encoding neural assemblies. Nature 390:70–74CrossRefGoogle Scholar
  33. Trongtokit Y, Rongsriyam Y, Komalamisra N, Apiwathnasorn C (2005) Comparative repellency of 38 essential oils against mosquito bites. Phytother Res 19:303–309CrossRefGoogle Scholar
  34. Ufkes LL, Grams GW (2007) The isolation and identification of volatile insect repellents from the fruit of the Osage orange (Maclura pomifera). J Essent Oil Res 19:167–170CrossRefGoogle Scholar
  35. von Butenandt A, Beckmann R, Stamm D, Hecker E (1959) Über den Sexual-Lockstoff des Seidenspinners Bombyx mori. Reindarstellung und Konstitution. Z Naturforsch 14b:283–284Google Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Entomology & Plant PathologyAuburn UniversityAuburnUSA

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