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

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

doi:10.1242/jeb.074898

Cited by 32 publications

(27 citation statements)

References 44 publications

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“…In contrast to previously published studies (e.g. Chilaka et al, 2012;Menda et al, 2013) where all the individuals of trained groups were tested simultaneously and without distinction of trained versus untrained animals in the same cohort, our experimental procedures allowed us to discard unfed females, thus only testing individuals that were actually subjected to the temporal contingency between US and CS during training.…”

Section: Research Articlementioning

confidence: 99%

“…In addition, as discussed above, these results suggest that mosquitoes' learning ability might also play a crucial role in the efficiency of odorantbased insect repellents. Finally, it is worth mentioning that this is only the third study to investigate associative learning in A. aegypti (Alonso et al, 2003;Menda et al, 2013), despite its potential vectorial importance. This work also sets the bases for future work on mosquitoes that would unravel what stimuli are adequate as CS or US, characterise their learning abilities, and determine the effects of physiological state (i.e.…”

Section: Consequences Of Learningmentioning

confidence: 99%

“…During the last decade or so, increasing attention has been devoted towards unravelling the learning abilities of haematophagous insects, including mosquitoes (Mwandawiro et al, 2000;McCall and Eaton, 2001;McCall and Kelly, 2002;Kaur et al, 2003;Alonso and Schuck-Paim, 2006;Tomberlin et al, 2006;Bouyer et al, 2007;Vinauger et al, 2011a;Vinauger et al, 2011b;Vinauger et al, 2012;Vinauger et al, 2013;Chilaka et al, 2012;Menda et al, 2013). Regarding mosquitoes, a handful of studies have provided direct or indirect evidence suggesting that learning abilities could be involved in host preference, choice of oviposition sites, and home range [for a detailed review, see references above and McCall and Kelly (McCall and Kelly, 2002) and Menda et al (Menda et al, 2013)].…”

mentioning

confidence: 99%

“…Regarding mosquitoes, a handful of studies have provided direct or indirect evidence suggesting that learning abilities could be involved in host preference, choice of oviposition sites, and home range [for a detailed review, see references above and McCall and Kelly (McCall and Kelly, 2002) and Menda et al (Menda et al, 2013)]. While indicative of the potential for learning, these studies lacked precise temporal and quantitative control of the conditioned and unconditioned stimuli when training groups of individuals, and therefore do not allow further investigation of the mechanisms underlying these cognitive abilities (Rescorla, 1988).…”

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confidence: 99%

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Olfactory learning and memory in the disease vector mosquito,Aedes aegypti

Vinauger

Lutz

Riffell

2014

Journal of Experimental Biology

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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 posttraining (for testing anaesthesia-resistant memory) and a protein synthesis inhibitor (cycloheximide; to disrupt the formation of longterm 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.

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Section: Research Articlementioning

confidence: 99%

Section: Consequences Of Learningmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Olfactory learning and memory in the disease vector mosquito,Aedes aegypti

Vinauger

Lutz

Riffell

2014

Journal of Experimental Biology

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“…However, until recently, such abilities had not been clearly experimentally evinced, to the extent of making some authors wonder whether haematophagous insects could learn anything from their hosts (Alonso et al, 2003). In recent years, the number of studies devoted to analysing the learning ability of disease vector insects has increased regarding mosquitoes (McCall and Eaton, 2001;McCall and Kelly, 2002;Kaur et al, 2003;Alonso and Schuck-Paim, 2006;Tomberlin et al, 2006;Chilaka et al, 2012;Menda et al, 2013;Vinauger et al, 2014), tsetse flies (Bouyer et al, 2007) and triatomine bugs (Vinauger et al, 2011a(Vinauger et al, ,b, 2012(Vinauger et al, , 2013. These studies provided direct or indirect evidence of learning ability, but as far as we know none of them dived deeper into the characterisation of how learning and memory could be modulated by endogenous factors.…”

Section: Introductionmentioning

confidence: 99%

Circadian modulation of learning abilities in a disease vector insect,Rhodnius prolixus

Vinauger

Lazzari

2015

Journal of Experimental Biology

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Despite the drastic consequences it may have on the transmission of parasites, the ability of disease vectors to learn and retain information has just begun to be characterised. The kissing bug Rhodnius prolixus, a vector of Chagas disease, is an excellent model, particularly because conditioning the proboscis extension response (PER) constitutes a valuable paradigm to study their cognitive abilities under carefully controlled conditions. Another characteristic of these bugs is the temporal organisation of their different activities in a bimodal endogenous daily rhythm. This offers the opportunity to address the implication of the circadian system in learning and memory. Using aversive conditioning of the PER, we tested whether the ability of kissing bugs to learn and remember information varies during the day. We found that bugs perform well during the night, but not during the day: their ability to acquire information -but not their ability to retrieve it -is modulated by time. When the bugs were kept under constant conditions in order to analyse the origin of this rhythm, the rhythm continued to free run, showing its endogenous and truly circadian nature. These results are the first to evince the effect of the circadian system on the learning abilities of disease vectors and one of the few in insects in general.

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Bioactivities and modes of action of VUAA1

Liu

Démares

Norris

et al. 2020

Pest Management Science

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BACKGROUND The compound 2‐((4‐ethyl‐5‐(pyridin‐3‐yl)‐4H‐1,2,4‐triazol‐3‐yl)thio)‐N‐(4‐ethylphenyl) acetamide (VUAA1) is reported to be an odorant receptor co‐receptor (Orco) agonist in insects with potential use as an insect repellent. For this study, the biological activity of VUAA1 was investigated in several bioassays with Aedes aegypti, including adult contact, spatial repellency, and larval repellency assays, as well as topical, injection, and feeding toxicity assays. Neurophysiological action was further explored by analysis of fruit fly central nervous system firing, cockroach axon recordings, patch clamp analysis of Kv2 potassium channel, and acetylcholinesterase inhibition studies. Finally, the metabolic impact on the toxicity of VUAA1 was explored by applying it in combination with established metabolic synergists. RESULTS In repellency and bite protection screens, VUAA1 showed little activity against adult mosquitoes, apparently due to its low volatility, since its effectiveness was increased by heating or mixing with transfluthrin acid and citronella oil. It did produce measurable repellency of mosquito larvae that was more potent than N,N‐diethyl‐m‐toluamide (DEET). Overall, VUAA1 showed low acute toxicity to both insects and mice, and it was weakly synergized by triphenyl phosphate. There was no observed cross‐resistance in a pyrethroid‐resistant strain of Anopheles gambiae. VUAA1 showed a two‐phase effect on the central nervous system, with neuroexcitation at 1 μmol L‐1 and an inhibitory effect at 100 μmol L‐1 that may relate to block of Kv2 potassium channels. CONCLUSIONS VUAA1 presented low toxicity, similar to other insect repellents. Its limited solubility, low volatility, and resulting poor adult repellency without additional adjuvants may restrict the utility of VUAA1 in typical public health applications. © 2020 Society of Chemical Industry

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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

Cited by 32 publications

References 44 publications

Olfactory learning and memory in the disease vector mosquito,Aedes aegypti

Olfactory learning and memory in the disease vector mosquito,Aedes aegypti

Circadian modulation of learning abilities in a disease vector insect,Rhodnius prolixus

Bioactivities and modes of action of VUAA1

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