Sensory discrimination between aversive salty and bitter tastes in an haematophagous insect.
Rhodnius prolixus
behavioural plasticity
gustatory aversion
learning
taste discrimination
Journal
The European journal of neuroscience
ISSN: 1460-9568
Titre abrégé: Eur J Neurosci
Pays: France
ID NLM: 8918110
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
25
09
2019
revised:
07
02
2020
accepted:
09
02
2020
pubmed:
13
2
2020
medline:
22
6
2021
entrez:
13
2
2020
Statut:
ppublish
Résumé
Sensory aversion is essential for avoiding prospective dangers. We studied the chemical perception of aversive compounds of different gustatory modalities (salty, bitter) in the haematophagous bug, Rhodnius prolixus. Over a walking arena, insects avoided a substrate embedded with 1M NaCl or KCl if provided with water as an alternative. However, no preferences were expressed when both salts were opposed to each other. A pre-exposure to amiloride interfered with the repellency of NaCl and KCl equally, suggesting that amiloride-sensitive receptors are involved in the detection of both salts. Discriminative experiments were then performed to determine whether R. prolixus can distinguish between these salts. An aversive operant conditioning involving either NaCl or KCl modulated the repellency of the conditioned salt, but also of the novel salt. Repellency levels of both salts were rigid to a chemical pre-exposure to any of both salts. When gustatory modalities were crossed by presenting as a choice NaCl and a bitter molecule as caffeine (Caf), no innate preferences were expressed. Aversive operant conditionings with either NaCl or Caf rendered unspecific changes in the repellency of both compounds. A chemical pre-exposure to Caf modulated the response to Caf but not to NaCl, suggesting the existence of two independent neural pathways for the detection of salts and bitter compounds. Overall results suggest that R. prolixus cannot discriminate molecules of the same gustatory modality (i.e. salty), but can distinguish between salty and bitter tastes. The potential use of aversive gustatory stimuli as a complement of commercially available olfactory repellents is discussed.
Substances chimiques
Sodium Chloride
451W47IQ8X
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1867-1880Subventions
Organisme : Consejo Nacional de Investigaciones Científicas y Técnicas
ID : PIP 11220110101053
Pays : International
Organisme : Universidad de Buenos Aires
Pays : International
Organisme : Fondo para la Investigación Científica y Tecnológica
ID : PICT 2013-1253
Pays : International
Informations de copyright
© 2020 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
Références
Alonso, W. J., & Schuck-Paim, C. (2006). The ghosts that pester studies on learning in mosquitoes: Guidelines to chase them off. Medical and Veterinary Entomology, 20, 157-165. https://doi.org/10.1111/j.1365-2915.2006.00623.x
Alonso, W. J., Wyatt, T. D., & Kelly, D. W. (2003). Are vectors able to learn about their hosts? A case study with Aedes aegypti mosquitoes. Memórias do Instituto Oswaldo Cruz, 98, 665-672. https://doi.org/10.1590/S0074-02762003000500014
Asparch, Y., Pontes, G., Masagué, S., Minoli, S., & Barrozo, R. B. (2016). Kissing bugs can generalize and discriminate between different bitter compounds. Journal of Physiology-Paris, 110, 99-106. https://doi.org/10.1016/j.jphysparis.2016.11.006
Barrozo, R. B. (2019). Food recognition in hematophagous insects. Current Opinion in Insect Science, 34, 55-60.
Battesti, M., Moreno, C., Joly, D., & Mery, F. (2015). Biased social transmission in Drosophila oviposition choice. Behavioral Ecology and Sociobiology, 69, 83-87. https://doi.org/10.1007/s00265-014-1820-x
Bernays, E., & Graham, M. (1988). On the evolution of host specificity in phytophagous arthropods. Ecology, 69(4), 886-892. https://doi.org/10.2307/1941237
Cano, A., Pontes, G., Sfara, V., Anfossi, D., & Barrozo, R. B. (2017). Nitric oxide contributes to high-salt perception in a blood-sucking insect model. Scientific Reports, 7, 15551. https://doi.org/10.1038/s41598-017-15861-0
Chapman, R. F. (2003). Contact chemoreception in feeding by phytophagous insects. Annual Review of Entomology, 48, 455-484.
Chilaka, N., Perkins, E., & Tripet, F. D. (2012). Visual and olfactory associative learning in the malaria vector Anopheles gambiae sensu stricto. Malaria Journal, 11, 1-11. https://doi.org/10.1186/1475-2875-11-27
de Brito Sanchez, M. G. (2011). Taste perception in honey bees. Chemical Senses, 36, 675-692. https://doi.org/10.1093/chemse/bjr040
de Brito Sanchez, M. G., Lorenzo, E., Su, S., Liu, F., Zhan, Y., & Giurfa, M. (2014). The tarsal taste of honey bees: Behavioral and electrophysiological analyses. Frontiers in Behavioural Neurosciences, 8, 25.
Freeman, E. G., & Dahanukar, A. (2015). Molecular neurobiology of Drosophila taste. Current Opinion in Neurobiology, 34, 140-148. https://doi.org/10.1016/j.conb.2015.06.001
Friend, W. G., & Smith, J. J. (1977). Factors affecting feeding by bloodsucking insects. Annual Review of Entomology, 22, 309-331. https://doi.org/10.1146/annurev.en.22.010177.001521
Fuji, S., Yavuz, A., Slone, J., Jagge, C., Song, X., & Amrein, H. (2015). Drosophila sugar receptors in sweet taste perception, olfaction, and internal nutrient sensing. Current Biology, 25(5), 621-627. https://doi.org/10.1016/j.cub.2014.12.058
Galun, R., Avi-Dor, Y., & Bar-Zeev, M. (1963). Feeding response in Aedes aegypti: Stimulation by adenosine triphosphate. Science, 142(3600), 1674-1675.
Giraud, M., Hotier, L., Giurfa, M., & de Brito Sanchez, M. G. (2018). Aversive gustatory learning and perception in honey bees. Scientific Reports, 8, 1343. https://doi.org/10.1038/s41598-018-19715-1
Glendinning, J. I., Davis, A., & Rai, M. (2006). Temporal coding mediates discrimination of “bitter” taste stimuli by an insect. Journal of Neuroscience, 26, 8900-8908.
Glendinning, J. I., Davis, A., Ramaswamy, S., Ramswamy, S., & Ramaswamy, S. (2002). Contribution of different taste cells and signaling pathways to the discrimination of “bitter” taste stimuli by an insect. Journal of Neuroscience, 22, 7281-7287.
Guerrieri, F., Schubert, M., Sandoz, J. C., & Giurfa, M. (2005). Perceptual and neural olfactory similarity in honeybees. PLoS Biology, 3(4), e60 https://doi.org/10.1371/journal.pbio.0030060
Hiroi, M., Meunier, N., Marion-Poll, F., & Tanimura, T. (2004). Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. Journal of Neurobiology, 61, 333-342.
Jaenike, J. (1982). Environmental modification of oviposition behavior in Drosophila. American Naturalist, 119, 784-802. https://doi.org/10.1086/283955
Kari, J., Almaas, T. J., Marion-Poll, F., & Mustaparta, H. (2007). Electrophysiological characterization of responses from gustatory receptor neurons of sensilla chaetica in the moth Heliothis virescens. Chemical Senses, 32(9), 863-879. https://doi.org/10.1093/chemse/bjm057
Kaur, J. S., Lai, Y. L., & Giger, A. D. (2003). Learning and memory in the mosquito Aedes aegypti shown by conditioning against oviposition deterrence. Medical and Veterinary Entomology, 17, 457-460. https://doi.org/10.1111/j.1365-2915.2003.00455.x
Kellenberger, S., & Schild, L. (2002). Epithelial sodium channel/degenerin family of ion channels: A variety of functions for a shared structure. Physiological Reviews, 82, 735-767. https://doi.org/10.1152/physrev.00007.2002
Kessler, S., González, J., Vlimant, M., Glauser, G., & Guerin, P. M. (2014). Quinine and artesunate inhibit feeding in the African malaria mosquito Anopheles gambiae: The role of gustatory organs within the mouthparts. Physiological Entomology, 39, 172-182.
Laska, M., Galizia, G., Giurfa, M., & Menzel, R. (1999). Olfactory discrimination ability and odor structure-activity relationships in honeybees. Chemical Senses, 24(4), 429-438. https://doi.org/10.1093/chemse/24.4.429
Lazzari, C. R. (1992). Circadian organization of locomotion activity in the haematophagous bug Triatoma infestans. Journal of Insect Physiology, 38, 895-903. https://doi.org/10.1016/0022-1910(92)90101-I
Liman, E. R., Zhang, Y. V., & Montell, C. (2014). Peripheral coding of taste. Neuron, 81, 984-1000. https://doi.org/10.1016/j.neuron.2014.02.022
Ling, F., Dahanukar, A., Weiss, L. A., Kwon, J. Y., & Carlson, J. R. (2014). The molecular and cellular basis of taste coding in the legs of drosophila. Journal of Neuroscience, 34, 7148-7164.
Masek, P., & Scott, K. (2010). Limited taste discrimination in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 107, 14833-14838. https://doi.org/10.1073/pnas.1009318107
McCall, P. J., & Eaton, G. (2001). Olfactory memory in the mosquito Culex quinquefasciatus. Medical and Veterinary Entomology, 15, 197-203.
McCall, P. J., & Kelly, D. W. (2002). Learning and memory in disease vectors. Trends in Parasitology, 18, 429-433. https://doi.org/10.1016/S1471-4922(02)02370-X
McCall, P. J., Mosha, F. W., Njunwa, K. J., & Sherlock, K. (2001). Evidence for memorized site-fidelity in Anopheles arabiensis. Transactions of the Royal Society of Tropical Medicine and Hygiene, 95, 587-590. https://doi.org/10.1016/S0035-9203(01)90087-2
McGann, J. P. (2017). Poor human olfaction is a 19th-century myth. Science, 80, 356. https://doi.org/10.1126/science.aam7263
Menda, G., Uhr, J. H., Wyttenbach, R. A., Vermeylen, F. M., Smith, D. M., Harrington, L. C., & Hoy, R. R. (2012). 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, 216, 218-223.
Mengoni, S. L., Lorenzo-Figueiras, A. N., & Minoli, S. A. (2017). Experience-dependent modulation of the attraction to faeces in the kissing bug Triatoma infestans. Journal of Insect Physiology, 98, 23-28. https://doi.org/10.1016/j.jinsphys.2016.10.018
Mesquita, R. D., Vionette-, R. J., Lowenberger, C., Rivera-pomar, R., Monteiro, A., Minx, P., … Lawson, P. L. (2015). Genome of Rhodnius prolixus, an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection. Proceedings of the National Academy of Sciences of the United States of America, 112, 14936-14941.
Minoli, S., Cano, A., Pontes, G., Magallanes, A., Roldan, N., & Barrozo, R. B. (2018). Learning spatial aversion is sensory-specific in the hematophagous insect Rhodnius prolixus. Front. Psychol., 9, 989. https://doi.org/10.3389/fpsyg.2018.00989
Minoli, S., Palottini, F., & Manrique, G. (2013). The main component of an alarm pheromone of kissing bugs plays multiple roles in the cognitive modulation of the escape response. Frontiers in Behavioural Neurosciences, 7, 77. https://doi.org/10.3389/fnbeh.2013.00077
Mwandawiro, C., Boots, M., Tuno, N., Suwonkerd, W., Tsuda, Y., & Takagi, M. (2000). Heterogeneity in the host preference of Japanese encephalitis vectors in Chiang Mai, northern Thailand. Transactions of the Royal Society of Tropical Medicine and Hygiene, 94, 238-242. https://doi.org/10.1016/S0035-9203(00)90303-1
Nielsen, E. T., & Nielsen, A. T. (1953). Field observations on the habits of Aedes Taeniorhynchus. Ecology, 34, 141-156. https://doi.org/10.2307/1930314
Pontes, G., Minoli, S., Ortega Insaurralde, I., de Brito Sanchez, M. G., & Barrozo, R. B. (2014). Bitter stimuli modulates the feeding decision of a blood-sucking insect via two sensory inputs. Journal of Experimental Biology, 217, 3708-3717.
Pontes, G., Pereira, M. H., & Barrozo, R. B. (2017). Salt controls feeding decisions in a blood-sucking insect. Journal of Insect Physiology, 98, 93-100. https://doi.org/10.1016/j.jinsphys.2016.12.002
Sakura, M., Okada, R., & Mizunami, M. (2002). Olfactory discrimination of structurally similar alcohols by cockroaches. Journal of Comparative Physiology A, 188, 787-797. https://doi.org/10.1007/s00359-002-0366-y
Sanford, M. R., & Tomberlin, J. K. (2011). Conditioning individual mosquitoes to an odor: Sex, source, and time. PLoS ONE, 6, e24218. https://doi.org/10.1371/journal.pone.0024218
Singh, R. N. (1997). Neurobiology of the gustatory systems of Drosophila and some terrestrial insects. Microscopy Research and Technique, 39, 547-563. https://doi.org/10.1002/(SICI)1097-0029(19971215)39:6<547:AID-JEMT7>3.0.CO;2-A
Spector, A., Guagliardo, N., & St John, S. (1996). Amiloride disrupts NaCl versus KCl discrimination performance: Implications for salt taste coding in rats. Journal of Neuroscience, 16, 8115-8122. https://doi.org/10.1523/JNEUROSCI.16-24-08115.1996
Spector, A. C., Markison, S., St John, S. J., & Garcea, M. (1997). Sucrose vs. maltose taste discrimination by rats depends on the input of the seventh cranial nerve. American Journal of Physiology, 272, R1210-R1218.
St John, S. J., & Smith, D. V. (2000). Neural representation of salts in the rat solitary nucleus: Brain stem correlates of taste discrimination. Journal of Neurophysiology, 84, 628-638. https://doi.org/10.1152/jn.2000.84.2.628
Tomberlin, J. K., Rains, G. C., Allan, S. A., Sanford, M. R., & Lewis, W. J. (2006). Associative learning of odor with food- or blood-meal by Culex quinquefasciatus Say (Diptera: Culicidae). Naturwissenschaften, 93, 551-556. https://doi.org/10.1007/s00114-006-0143-9
Vinauger, C., Buratti, L., & Lazzari, C. R. (2011a). Learning the way to blood: first evidence of dual olfactory conditioning in a blood-sucking insect, Rhodnius prolixus. I. Appetitive learning. Journal of Experimental Biology, 214, 3032-3038. https://doi.org/10.1242/jeb.056697
Vinauger, C., Buratti, L., & Lazzari, C. R. (2011b). Learning the way to blood: First evidence of dual olfactory conditioning in a blood-sucking insect, Rhodnius prolixus. II. Aversive learning. Journal of Experimental Biology, 214, 3039-3045. https://doi.org/10.1242/jeb.057075
Vinauger, C., Lallement, H., & Lazzari, C. R. (2013). Learning and memory in Rhodnius prolixus: Habituation and aversive operant conditioning of the proboscis extension response. Journal of Experimental Biology, 216, 892-900. https://doi.org/10.1242/jeb.079491
Vinauger, C., & Lazzari, C. R. (2015). Circadian modulation of learning ability in a disease vector insect, Rhodnius prolixus. Journal of Experimental Biology, 218, 3110-3117. https://doi.org/10.1242/jeb.119057
Vinauger, C., Lutz, E. K., & Riffell, J. A. (2014). Olfactory learning and memory in the disease vector mosquito Aedes aegypti. Journal of Experimental Biology, 217, 2321-2330. https://doi.org/10.1242/jeb.101279
Vinauger, C., Pereira, M. H., & Lazzari, C. R. (2012). Learned host preference in a Chagas disease vector, Rhodnius prolixus. Acta Tropica, 122, 24-28. https://doi.org/10.1016/j.actatropica.2011.11.007
Vosshall, L., & Stocker, R. F. (2007). Molecular architecture of smell and taste in Drosophila. Annual Review of Neuroscience, 30, 505-533.
Weiss, L. A., Dahanukar, A., Kwon, J. Y., Banerjee, D., & Carlson, J. R. (2011). The molecular and cellular basis of bitter taste in Drosophila. Neuron, 69, 258-272. https://doi.org/10.1016/j.neuron.2011.01.001
Zhang, Y. V., Ni, J., & Montell, C. (2013). The molecular basis for attractive salt-taste coding in Drosophila. Science, 340, 1334-1338. https://doi.org/10.1126/science.1234133