title: Olfactory learning and memory in the disease vector mosquito Aedes aegypti.
abstract: Olfactory learning in blood-feeding insects, such as mosquitoes, could play an important role in host preference and disease transmission. However, standardised protocols allowing testing of their learning abilities are currently lacking, and how different olfactory stimuli are learned by these insects remains unknown. Using a Pavlovian conditioning paradigm, we trained individuals and groups of Aedes aegypti mosquitoes to associate an odorant conditioned stimulus (CS) with a blood-reinforced thermal stimulus (unconditioned stimulus; US). Results showed, first, that mosquitoes could learn the association between L-lactic acid and the US, and retained the association for at least 24 h. Second, the success of olfactory conditioning was dependent upon the CS--some odorants that elicited indifferent responses in naïve mosquitoes, such as L-lactic acid and 1-octen-3-ol, were readily learned, whereas others went from aversive to attractive after training (Z-3-hexen-1-ol) or were untrainable (β-myrcene and benzyl alcohol). Third, we examined whether mosquitoes' ability to learn could interfere with the action of the insect repellent DEET. Results demonstrated that pre-exposure and the presence of DEET in the CS reduced the aversive effects of DEET. Last, the nature of the formed memories was explored. Experiments using cold-shock treatments within the first 6 h post-training (for testing anaesthesia-resistant memory) and a protein synthesis inhibitor (cycloheximide; to disrupt the formation of long-term memory) both affected mosquitoes' performances. Together, these results show that learning is a crucial component in odour responses in A. aegypti, and provide the first evidence for the functional role of different memory traces in these responses.
authors.affiliation: Department of Biology, University of Washington, Seattle, WA 98195, USA.
authors.forename: Clément
authors.initials: C
authors.lastname: Vinauger
authors.affiliation: Department of Biology, University of Washington, Seattle, WA 98195, USA.
authors.forename: Eleanor K
authors.initials: EK
authors.lastname: Lutz
authors.affiliation: Department of Biology, University of Washington, Seattle, WA 98195, USA jriffell@u.washington.edu.
authors.forename: Jeffrey A
authors.initials: JA
authors.lastname: Riffell
mesh_terms: D000330:Aedes / Q000502:physiology*; D000818:Animals; D002245:Carbon Dioxide / Q000378:metabolism*; D003214:Conditioning, Classical; D003671:DEET / Q000494:pharmacology; D005260:Female; D006801:Humans; D007302:Insect Repellents / Q000494:pharmacology; D019344:Lactic Acid / Q000378:metabolism*; D007858:Learning; D008568:Memory / Q000187:drug effects; D009812:Odorants
chemical_list: D007302:Insect Repellents; D003671:DEET; D002245:Carbon Dioxide; D019344:Lactic Acid
keywords: Aedes aegypti; Appetitive conditioning; Disease vector; Long-term memory; Olfactory learning
references.citation: J Exp Biol. 2011 Sep 15;214(Pt 18):3032-8
references.pmid: 21865515
references.citation: Ann Trop Med Parasitol. 1957 Jun;51(2):159-69
references.pmid: 13445076
references.citation: PLoS One. 2013;8(2):e54438
references.pmid: 23437043
references.citation: Med Vet Entomol. 2001 Jun;15(2):197-203
references.pmid: 11434554
references.citation: Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):338-42
references.pmid: 8990210
references.citation: Theor Popul Biol. 1988 Feb;33(1):31-53
references.pmid: 2897726
references.citation: Annu Rev Entomol. 1999;44:131-57
references.pmid: 9990718
references.citation: Acta Trop. 2012 Apr;122(1):24-8
references.pmid: 22138145
references.citation: Experientia. 1990 Jul 15;46(7):660-70
references.pmid: 1973656
references.citation: J Chem Ecol. 2002 Jan;28(1):131-43
references.pmid: 11871395
references.citation: Trans R Soc Trop Med Hyg. 2000 May-Jun;94(3):238-42
references.pmid: 10974986
references.citation: J Neurosci. 2003 Nov 19;23(33):10495-502
references.pmid: 14627633
references.citation: Ann Intern Med. 1998 Jun 1;128(11):931-40
references.pmid: 9634433
references.citation: Nat Rev Drug Discov. 2003 Apr;2(4):267-77
references.pmid: 12669026
references.citation: Med Vet Entomol. 2006 Jun;20(2):157-65
references.pmid: 16871700
references.citation: Trans R Soc Trop Med Hyg. 2001 Nov-Dec;95(6):587-90
references.pmid: 11816426
references.citation: Science. 1968 Sep 27;161(3848):1346-7
references.pmid: 5673445
references.citation: Annu Rev Neurosci. 1988;11:329-52
references.pmid: 3284445
references.citation: J Exp Biol. 2005 Aug;208(Pt 15):2963-72
references.pmid: 16043601
references.citation: Acta Trop. 2009 May-Jun;110(2-3):148-58
references.pmid: 18983971
references.citation: Trends Parasitol. 2002 Oct;18(10):429-33
references.pmid: 12377586
references.citation: Cell. 1994 Oct 7;79(1):35-47
references.pmid: 7923375
references.citation: J Exp Biol. 2013 Jan 15;216(Pt 2):218-23
references.pmid: 22996441
references.citation: Proc Natl Acad Sci U S A. 2008 Sep 9;105(36):13598-603
references.pmid: 18711137
references.citation: Am J Trop Med Hyg. 1978 Jul;27(4):827-31
references.pmid: 686250
references.citation: Med Vet Entomol. 1996 Jul;10(3):269-76
references.pmid: 8887339
references.citation: Parasitology. 2000 Mar;120 ( Pt 3):319-27
references.pmid: 10759090
references.citation: PLoS Biol. 2010 Aug 31;8(8):
references.pmid: 20824161
references.citation: Fitoterapia. 2007 Jul;78(5):359-64
references.pmid: 17512681
references.citation: PLoS One. 2010 Aug 11;5(8):e12138
references.pmid: 20725637
references.citation: Med Vet Entomol. 2003 Dec;17(4):457-60
references.pmid: 14651662
references.citation: J Exp Biol. 2013 Mar 1;216(Pt 5):892-900
references.pmid: 23408803
references.citation: Med Vet Entomol. 2002 Mar;16(1):91-8
references.pmid: 11963986
references.citation: Bull World Health Organ. 1973 May;48(5):623-9
references.pmid: 4544150
references.citation: Proc Natl Acad Sci U S A. 2011 May 10;108(19):8026-9
references.pmid: 21518875
references.citation: Bioinspir Biomim. 2008 Sep;3(3):034001
references.pmid: 18591738
references.citation: Nature. 2013 Jun 27;498(7455):487-91
references.pmid: 23719379
references.citation: Malar J. 2012 Jan 27;11:27
references.pmid: 22284012
references.citation: Biol Lett. 2007 Apr 22;3(2):113-6
references.pmid: 17251119
references.citation: Nature. 2011 Sep 21;478(7370):511-4
references.pmid: 21937991
references.citation: J Insect Physiol. 2008 Jul;54(7):1184-92
references.pmid: 18634791
references.citation: Mem Inst Oswaldo Cruz. 2003 Jul;98(5):665-72
references.pmid: 12973535
references.citation: Trans R Soc Trop Med Hyg. 1986;80(1):69-77
references.pmid: 3727001
references.citation: Chem Senses. 2004 Nov;29(9):833-41
references.pmid: 15574819
references.citation: Trends Parasitol. 2001 Dec;17(12):578-81
references.pmid: 11756041
references.citation: Cell. 2014 Feb 27;156(5):1060-71
references.pmid: 24581501
references.citation: J Exp Biol. 2011 Sep 15;214(Pt 18):3039-45
references.pmid: 21865516
references.citation: Curr Biol. 2005 Sep 6;15(17):R700-13
references.pmid: 16139203
references.citation: Ciba Found Symp. 1996;200:132-44; discussion 144-8, 178-83
references.pmid: 8894295
references.citation: J Insect Physiol. 2011 Oct;57(10):1431-6
references.pmid: 21801727
references.citation: Naturwissenschaften. 2006 Nov;93(11):551-6
references.pmid: 16924477