Associative learning in the dengue vector mosquito, Aedes aegypti: Avoidance of a previously attractive odor or surface color that is paired with an aversive stimulus

Journal of Experimental Biology

Volumn 216, Issue 2, 2013, Pages 218-223

  Menda, Gil ^a   Uhr, Joshua H ^a   Wyttenbach, Robert A ^a   Vermeylen, Françoise M ^a   Smith, David M ^a   Harrington, Laura C ^a   Hoy, Ronald R ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Conditioning; Inhibitory avoidance; Passive avoidance

Indexed keywords

1 OCTEN 3 OL; 1-OCTEN-3-OL; OCTANOL;

AEDES; ANIMAL; ARTICLE; AVOIDANCE BEHAVIOR; COLOR; DENGUE; DISEASE CARRIER; DISEASE TRANSMISSION; ELECTRIC SHOCK; FEMALE; HUMAN; INSTRUMENTAL CONDITIONING; MALE; METABOLISM; ODOR; PHYSIOLOGY; SURFACE PROPERTY;

AEDES; ANIMALS; AVOIDANCE LEARNING; COLOR; CONDITIONING, OPERANT; DENGUE; ELECTROSHOCK; FEMALE; HUMANS; INSECT VECTORS; MALE; OCTANOLS; ODORS; SURFACE PROPERTIES;

AEDES AEGYPTI; ANOPHELES GAMBIAE; CHIKUNGUNYA VIRUS; CULEX PIPIENS QUINQUEFASCIATUS; DROSOPHILA MELANOGASTER; HEXAPODA;

EID: 84871791888     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.074898     Document Type: Article

References (46)

1. Alonso, W. J. and Schuck-Paim, C. (2006). The-ghosts' that pester studies on learning in mosquitoes: guidelines to chase them off. Med. Vet. Entomol. 20, 157-165
2. Alonso, W. J., Wyatt, T. D. and Kelly, D. W. (2003). Are vectors able to learn about their hosts? A case study with Aedes aegypti mosquitoes. Mem. Inst. Oswaldo Cruz 98, 665-672 (Pubitemid 38019590)
3. Bitterman, M. E., Menzel, R., Fietz, A. and Schäfer, S. (1983). Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psychol. 97, 107-119
4. Charlwood, J. D., Graves, P. M. and Marshall, T. F. (1988). Evidence for a-memorized' home range in Anopheles farauti females from Papua New Guinea. Med. Vet. Entomol. 2, 101-108
5. Chilaka, N., Perkins, E. and Tripet, F. (2012). Visual and olfactory associative learning in the malaria vector Anopheles gambiae sensu stricto. Malar. J. 11, 27.
6. Clements, A. (1992). The Biology of Mosquitoes: Development, Nutrition and Reproduction. London, UK: Chapman and Hall.
7. Davis, R. L. (2005). Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu. Rev. Neurosci. 28, 275-302 (Pubitemid 41098907)
8. Dukas, R. (2008). Evolutionary biology of insect learning. Annu. Rev. Entomol. 53, 145-160 (Pubitemid 351341935)
9. Gilbert, I. and Gouck, H. (1957). Influence of surface color on mosquito landing rates. J. Econ. Entomol. 50, 678-680
10. Giurfa, M. (2007). Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 193, 801-824 (Pubitemid 47124969)
11. Giurfa, M. and Sandoz, J. C. (2012). Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honeybees. Learn. Mem. 19, 54-66
12. Grant, A. J. and Dickens, J. C. (2011). Functional characterization of the octenol receptor neuron on the maxillary palps of the yellow fever mosquito, Aedes aegypti. PLoS ONE 6, e21785.
13. Gubler, D. J. (1998). Dengue and dengue hemorrhagic fever. Clin. Microbiol. Rev. 11, 480-496 (Pubitemid 28379096)
14. Harrington, L. C., Edman, J. D. and Scott, T. W. (2001). Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? J. Med. Entomol. 38, 411-422 (Pubitemid 33614607)
15. Hii, J. L., Chew, M., Sang, V. Y., Munstermann, L. E., Tan, S. G., Panyim, S. and Yasothornsrikul, S. (1991). Population genetic analysis of host seeking and resting behaviors in the malaria vector, Anopheles balabacensis (Diptera: Culicidae). J. Med. Entomol. 28, 675-684
16. Holliday, M. and Hirsch, J. (1986). A comment on the evidence for learning in Diptera. Behav. Genet. 16, 439-447
17. Honjo, K. and Furukubo-Tokunaga, K. (2009). Distinctive neuronal networks and biochemical pathways for appetitive and aversive memory in Drosophila larvae. J. Neurosci. 29, 852-862
18. Jhumur, U. S., Dötterl, S. and Jürgens, A. (2006). Naive and conditioned responses of Culex pipiens pipiens biotype molestus (Diptera: Culicidae) to flower odors. J. Med. Entomol. 43, 1164-1170 (Pubitemid 44862948)
19. Kaur, J. S., Lai, Y. L. and Giger, A. D. (2003). Learning and memory in the mosquito Aedes aegypti shown by conditioning against oviposition deterrence. Med. Vet. Entomol. 17, 457-460 (Pubitemid 38448906)
20. Keene, A. C. and Waddell, S. (2007). Drosophila olfactory memory: single genes to complex neural circuits. Nat. Rev. Neurosci. 8, 341-354 (Pubitemid 46652464)
21. Ligon, B. L. (2006). Reemergence of an unusual disease: the chikungunya epidemic. Semin. Pediatr. Infect. Dis. 17, 99-104 (Pubitemid 43963533)
22. McCall, P. J. and Eaton, G. (2001). Olfactory memory in the mosquito Culex quinquefasciatus. Med. Vet. Entomol. 15, 197-203 (Pubitemid 32614530)
23. McCall, P. J. and Kelly, D. W. (2002). Learning and memory in disease vectors. Trends Parasitol. 18, 429-433
24. McCall, P. J., Mosha, F. W., Njunwa, K. J. and Sherlock, K. (2001). Evidence for memorized site-fidelity in Anopheles arabiensis. Trans. R. Soc. Trop. Med. Hyg. 95, 587-590 (Pubitemid 34202246)
25. McGuire, T. R. (1986). Further evidence for learning in Diptera: a reply to Holliday and Hirsch. Behav. Genet. 16, 457-473
26. McIntyre, C. K., Hatfield, T. and McGaugh, J. L. (2002). Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats. Eur. J. Neurosci. 16, 1223-1226 (Pubitemid 35340845)
27. Menzel, R. (1999). Memory dynamics in the honeybee. J. Comp. Physiol. A 185, 323-340 (Pubitemid 29532282)
28. Menzel, R., Manz, G., Menzel, R. and Greggers, U. (2001). Massed and spaced learning in honeybees: the role of CS, US, the intertrial interval, and the test interval. Learn. Mem. 8, 198-208 (Pubitemid 32831364)
29. Mery, F. and Kawecki, T. J. (2005). A cost of long-term memory in Drosophila. Science 308, 1148. (Pubitemid 40696428)
30. Mery, F., Belay, A. T., So, A. K., Sokolowski, M. B. and Kawecki, T. J. (2007). Natural polymorphism affecting learning and memory in Drosophila. Proc. Natl. Acad. Sci. USA 104, 13051-13055 (Pubitemid 351737591)
31. Mwandawiro, C., Boots, M., Tuno, N., Suwonkerd, W., Tsuda, Y. and Takagi, M. (2000). Heterogeneity in the host preference of Japanese encephalitis vectors in Chiang Mai, northern Thailand. Trans. R. Soc. Trop. Med. Hyg. 94, 238-242 (Pubitemid 30406545)
32. Neuser, K., Husse, J., Stock, P. and Gerber, B. (2005). Appetitive olfactory learning in Drosophila larvae: effects of repetition, reward strength, age, gender, assay type and memory span. Anim. Behav. 69, 891-898 (Pubitemid 40419444)
33. Ooi, E.-E., Goh, K.-T. and Gubler, D. J. (2006). Dengue prevention and 35 years of vector control in Singapore. Emerg. Infect. Dis. 12, 887-893 (Pubitemid 43848408)
34. Pearce, J. M. (1987). A model for stimulus generalization in Pavlovian conditioning. Psychol. Rev. 94, 61-73
35. Quinn, W. G., Harris, W. A. and Benzer, S. (1974). Conditioned behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 71, 708-712
36. Roussel, E., Padie, S. and Giurfa, M. (2012). Aversive learning overcomes appetitive innate responding in honeybees. Anim. Cogn. 15, 135-141
37. Sanford, M. R. and Tomberlin, J. K. (2011). Conditioning individual mosquitoes to an odor: sex, source, and time. PLoS ONE 6, e24218.
38. Shafir, S., Menda, G. and Smith, B. H. (2005). Caste-specific differences in risk sensitivity in honeybees, Apis mellifera. Anim. Behav. 69, 859-868 (Pubitemid 40413315)
39. Swaminathan, S. and Khanna, N. (2009). Dengue: recent advances in biology and current status of translational research. Curr. Mol. Med. 9, 152-173
40. Takken, W. and Kline, D. L. (1989). Carbon dioxide and 1-octen-3-ol as mosquito attractants. J. Am. Mosq. Control Assoc. 5, 311-316
41. Tomberlin, J. K., Rains, G. C., Allan, S. A., Sanford, M. R. and Lewis, W. J. (2006). Associative learning of odor with food-or blood-meal by Culex quinquefasciatus Say (Diptera: Culicidae). Naturwissenschaften 93, 551-556
42. Tully, T. (1986). Measuring learning in individual flies is not necessary to study the effects of single-gene mutations in Drosophila: a reply to Holliday and Hirsch. Behav. Genet. 16, 449-455
43. Vinauger, C., Buratti, L. and Lazzari, C. R. (2011). Learning the way to blood: first evidence of dual olfactory conditioning in a blood-sucking insect, Rhodnius prolixus. II. Aversive learning. J. Exp. Biol. 214, 3039-3045
44. Webster, D. P., Farrar, J. and Rowland-Jones, S. (2009). Progress towards a dengue vaccine. Lancet Infect. Dis. 9, 678-687
45. World Health Organization (1997). Vector Surveillance and Control Dengue Haemorrhagic Fever: Diagnosis, Treatment, Prevention and Control. Geneva, CH: World Health Organization.
46. World Health Organization (2002). Dengue and Dengue Haemorrhagic Fever. Geneva, CH: World Health Organization.