Parte de libro

Anton, S.; Minoli, S.; Gadenne, C.; Anderson, P. "Modulation of olfactory and gustatory sensitivity mediated by sensory experience in moths: A simple form of social learning?" (2013) Social Learning Theory: Phylogenetic Considerations across Animal, Plant, and Microbial Taxa:147-162
La versión final de este artículo es de uso interno de la institución.


As do vertebrates, insects show a high degree of phenotypic plasticity, which enables them to adapt their behavioural responses to their surrounding world. For example, social insects such as honeybees are able to perform complex learning tasks, similar to vertebrates. Non-social insects such as flies or moths can also associate sensory information with rewards or punishment.Non-associative forms of learning include sensitization and habituation to sensory cues originating from conspecifics or the biotic or abiotic environment. Often sensitization and habituation are the result of multiple exposures to sensory stimuli, but we have evidence in moths that a single exposure can also elicit long-lasting sensitization. The capacity to use sensory experience to adapt responses to social contexts by developing increased sensitivity to salient sensory cues from conspecifics and heterospecifics can be interpreted as a simple form of social learning.We summarize here intra- and cross-modal effects of brief pre-exposure to different stimuli on the behaviour and underlying neural mechanisms in male moths. Moths are an ideal model for this type of approach because different sensory stimuli are well known to trigger a number of well-defined behaviours in different contexts and their nervous system is relatively simple, well-described and accessible.Adult males respond to low doses of highly specific female-produced sex pheromones to find a mating partner and to flower odours to find food sources. Host plant odours can also complement the sex pheromone for a better localization of conspecific females. For feeding, the quality of a food source is evaluated upon contact, where sucrose concentration indicates nutritional value and bitter substances indicate non- palatability or toxicity. Male moths also detect ultrasound emitted by bats, their natural enemies. Behavioural analyses have shown that a brief exposure to any of the mentioned sensory stimuli increases responses to the sex pheromone after 24 hr. In addition, responses to gustatory stimuli are increased by brief pre-exposure to gustatory and pheromone stimuli. These reciprocal effects indicate that the described phenomena represent a form of general sensitization or maturation of the sensory systems, rather than selective attention.Attempts to localize modifications within the nervous system after brief pre-exposure indicate no or rather small changes in peripheral sensory systems caused by intra-modal exposure. In the primary olfactory centre, the antennal lobe, response thresholds of projection neurons to the sex pheromone and plant odours decreased after pre-exposure to the sex pheromone, to a bat-mimicking sound, but not to sucrose. In addition, the part of the antennal lobe processing information on the major sex pheromone compound increased in size after pre-exposure to the sex pheromone, probably indicating an increase in synaptic connections. These neurobiological approaches indicate that intra- and cross-modal effects of sensory pre-exposure might originate from modality-dependent changes at multiple levels within the nervous system. © 2013 Nova Science Publishers, Inc. All rights reserved.


Documento: Parte de libro
Título:Modulation of olfactory and gustatory sensitivity mediated by sensory experience in moths: A simple form of social learning?
Autor:Anton, S.; Minoli, S.; Gadenne, C.; Anderson, P.
Filiación:Laboratoire Récepteurs et Canaux Ioniques Membranaires, INRA/Université d'Angers, UPRES, EA 2647 USC INRA 1330, 49045 Angers, France
Departmento Biodiversidad y Biología Experimental, FCEyN, Universidad de Buenos Aires, Ciudad Universitaria, Buenos Aires, Argentina
Department of Plant, Protection Biology, Swedish University of Agricultural Sciences, 23053 Alnarp, Sweden
Palabras clave:Antennal lobe; Bat sound; Behavioural plasticity; Brief pre-exposure; Noctuid moth; Olfaction; Receptor neuron; Sensitization; Sex pheromone; Taste
Página de inicio:147
Página de fin:162
Título revista:Social Learning Theory: Phylogenetic Considerations across Animal, Plant, and Microbial Taxa
Título revista abreviado:Soc. Learn. Theory: Phylogenetic Considerations across Anim., Plant, and Microbial Taxa


  • Auld, H.L., Punzalan, D., Godin, J.G., Rundle, H.D., Do female fruit flies (Drosophila serrata) copy the mate choice of others? (2009) Behavioural Processes, 82 (1), pp. 78-80
  • Agrawal, A.A., Ecology - Phenotypic plasticity in the interactions and evolution of species (2001) Science, 294 (5541), pp. 321-326
  • Walters, E.T., Illich, P.A., Weeks, J.C., Lewin, M.R., Defensive responses of larval Manduca sexta and their sensitization by noxious stimuli in the laboratory and field (2001) Journal of Experimental Biology, 204 (3), pp. 457-469
  • Rakitin, A., Tomsic, D., Maldonado, H., Habituation and sensitization to an electrical shock in the crab Chasmagnathus (1991) Effect of background illumination, 50 (3), pp. 477-487. , Physiology and Behavior
  • DeBelle, J.S., Heisenberg, M., Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies (1994) Science, 263 (5147), pp. 692-695
  • Fan, R.J., Anderson, P., Hansson, B.S., Behavioural analysis of olfactory conditioning in the moth Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae) (1997) Journal of Experimental Biology, 200 (23), pp. 2969-2976
  • Hartlieb, E., Hansson, B.S., Anderson, P., Sex or food? Appetitive learning of sex odors in a male moth (1999) Naturwissenschaften, 86 (8), pp. 396-399
  • Langridge, E.A., Franks, N.R., Sendova-Franks, A.B., Improvement in collective performance with experience in ants (2004) Behavioral Ecology and Sociobiology, 56 (6), pp. 523-529
  • Chittka, L., Leadbeater, E., Social learning: Public information in insects (2005) Current Biology, 15 (21), pp. R869-R871
  • Franks, N.R., Richardson, T., Teaching in tandem-running ants (2006) Nature, 439 (7073), pp. 153-153
  • Von Frisch, K., Decoding the language of the bee (1974) Science, 185 (4152), pp. 663-668
  • Farina, W.M., Grüter, C., Díaz, P.C., Social learning of floral odours inside the honeybee hive (2005) Proceedings Royal Society B, 272 (1575), pp. 1923-1928
  • Leadbeater, E., Chittka, L., A new mode of information transfer in foraging bumblebees? (2005) Current Biology, 15 (12), pp. R447-R448
  • Worden, B.D., Papaj, D.R., Flower choice copying in bumblebees (2005) Biology Letters, 1 (4), pp. 504-507
  • Nieh, J.C., Barreto, L.S., Contrera, F.A.L., Imperatriz-Fonseca, V.L., Olfactory eavesdropping by a competitively foraging stingless bee, Trigona spinipes (2004) Proceedings Royal Society, B271 (1548), pp. 1633-1640
  • Hebets, E.A., Subadult experience influences adult mate choice in an arthropod: Exposed female wolf spiders prefer males of a familiar phenotype (2003) Proceedings of the National Academy of Sciences USA, 100 (23), pp. 13390-13395
  • Fincke, O.M., Fargevieille, A., Schultz, T.D., Lack of innate preference for morph and species identity in mate-searching Enallagma damselflies (2007) Behavioral Ecology and Sociobiology, 61 (7), pp. 1121-1131
  • Mery, F., Varela, S.A.M., Danchin, E., Blanchet, S., Parejo, D., Coolen, I., Wagner, R.H., Public versus personal information for mate copying in an invertebrate (2009) Current Biology, 19 (9), pp. 730-734
  • Coolen, I., Dangles, O., Casas, J., Social learning in noncolonial insects? (2005) Current Biology, 15 (21), pp. 1931-1935
  • Bailey, N.W., Zuk, M., Field crickets change mating preferences using remembered social information (2009) Biology Letters, 5 (4), pp. 449-451
  • Danchin, E., Giraldeau, L.A., Valone, T.J., Wagner, R.H., Public information: From nosy neighbors to cultural evolution (2004) Science, 305 (5683), pp. 487-491
  • Bittermann, M.E., Menzel, R., Fietz, A., Schäfer, S., Classical conditioning of proboscis extension in honeybee (Apis mellifera) (1983) Journal of Comparative Physiology, A97 (2), pp. 107-119
  • Minoli, S., Kauer, I., Colson, V., Party, V., Renou, M., Anderson, P., Gadenne, C., Anton, S., Brief exposure to sensory cues elicits stimulus-nonspecific general sensitization in an insect (2012) PLoS ONE, 7 (3). , e34141
  • Ljungberg, H., Anderson, P., Hansson, B.S., Physiology and morphology of pheromone-specific sensilla on the antennae of male and female Spodoptera-littoralis (Lepidoptera, Noctuidae) (1993) Journal of Insect Physiology, 39 (3), pp. 253-260
  • Schmidt-Büsser, D., von Arx, M., Guerin, P.M., Host plant volatiles serve to increase the response of male European grape berry moths, Eupoecilia ambiguella, to their sex pheromone (2009) Journal of Comparative Physiology A, 195 (9), pp. 853-864
  • Landolt, P.J., Phillips, T.W., Host plant influences on sex pheromone behavior of phytophagous insects (1997) Annual Review of Entomology, 42, pp. 371-391
  • Varela, N., Avilla, J., Anton, S., Gemeno, C., Synergism of pheromone and host-plant volatile blends in the attraction of Grapholita molesta males Entomol. Exp (2011) Appl, 141 (2), pp. 114-122
  • Duckworth, R.A., The role of behavior in evolution: a search for mechanism (2009) Evolutionay Ecology, 23 (4), pp. 513-531
  • Turlure, C., Van Dyck, H., On the consequences of aggressive male mate-locating behaviour and micro-climate for female host plant use in the butterfly Lycaena hippothoe (2009) Behavioral Ecology and Sociobiology, 63 (11), pp. 1581-1591
  • Keil, T.A., Morphology and development of the peripheral olfactory organs. (1999) Insect Olfaction, pp. 5-48. , Hansson, B. S. (Ed.), Berlin: Springer
  • Anton, S., Homberg, U., Antennal lobe structure. (1999) Insect Olfaction, pp. 98-125. , Hansson, B. S. (Ed.), Berlin: Springer
  • Hansson, B.S., Anton, S., Function and morphology of the antennal lobe: new developments (2000) Annual Review of Entomology, 45, pp. 203-231
  • Renwick, J.A.A., Chew, F.S., Oviposition behavior in lepidoptera (1994) Annual Review of Entomology, 39, pp. 377-400
  • Chapman, R., Chemical Inhibition of Feeding by Phytophagous Insects (1974) Bulletin of Entomological Research, 64 (3), pp. 339-363
  • Amakawa, T., Effects of age and blood sugar levels on the proboscis extension of the blow fly Phormia regina (2001) Journal of Insect Physiology, 47 (2), pp. 195-203
  • Dethier, V.G., Bowdan, E., The effect of alkaloids on sugar receptors and the feeding-behavior of the blowfly (1989) Physiological Entomology, 14 (2), pp. 127-136
  • Le Bourg, E., Hypergravity and aging in Drosophila melanogaster 8 (1996) Proboscis-extension-response threshold to sucrose, 42 (4), pp. 235-240. , Gerontology
  • Surlykke, A., Miller, L.A., Central branching of three sensory axons from a moth ear (Agrotis-segetum, Noctuidae) (1982) Journal of Insect Physiology, 28 (4), pp. 357-364
  • Werner, T.K., Responses of nonflying moths to ultrasound: the threat of gleaning bats (1981) Canadian Journal of Zoology, 59 (3), pp. 525-529
  • Miller, L.A., Surlykke, A., How some insects detect and avoid being eaten by bats: Tactics and countertactics of prey and predator (2001) Bioscience, 51 (7), pp. 570-581
  • Skals, N., Anderson, P., Kanneworff, M., Löfstedt, C., Surlykke, A., Her odours make him deaf: Crossmodal modulation of olfaction and hearing in a male moth (2005) Journal of Experimental Biology, 208 (4), pp. 595-601
  • Kehat, M., Greenberg, S., Tamaki, Y., Field evaluation of the synthetic sex pheromone, as an attractant for males of the cotton leafworm, Spodoptera littoralis (BOISD.), in Israel (1976) Applied Entomology and Zoology, 11 (1), pp. 45-52
  • Barrozo, R.B., Gadenne, C., Anton, S., Switching attraction to inhibition: Mating-induced reversed role of sex pheromone in an insect (2010) Journal of Experimental Biology, 213 (17), pp. 2933-2939
  • Gabel, B., Tansy Flowers Attract European Grapevine Moth Females, LobesiaBotrana Den and Schiff (Lep, Tortricidae) (1992) Journal of Applied Entomology, 113 (2), pp. 153-158
  • Haynes, K.F., Zhao, J.Z., Latif, A., Identification of floral compounds from Abelia grandiflora that stimulate upwind flight in cabbage looper moths (1991) Journal of Chemical Ecology, 17 (3), pp. 637-646
  • Anderson, P., Sadek, M.M., Larsson, M., Hansson, B.S., Thöming, G., Larval host plant experience modulates both mate finding and oviposition choice in a moth (2013) Animal Behavior (accepted for publication)
  • Party, V., Hanot, C., Said, I., Rochat, D., Renou, M., Plant terpenes affect intensity and temporal parameters of pheromone detection in a moth (2009) Chemical Senses, 34 (9), pp. 763-774
  • Rouyar, A., Party, V., Prešern, J., Blejec, A., Renou, M., A general odorant background affects the coding of pheromone stimulus intermittency in specialist olfactory receptor neurones (2011) PLoS ONE, 6 (10). , e26443
  • Anderson, P., Sadek, M.M., Hansson, B.S., Pre-exposure modulates attraction to sex pheromone in a moth (2033) Chemical Senses, 28 (4), pp. 285-291
  • Anderson, P., Hansson, B., Nilsson, U., Han, Q., Sjoholm, M., Skals, N., Anton, S., Increased behavioral and neuronal sensitivity to sex pheromone after brief odor experience in a moth (2007) Chemical Senses, 32 (5), pp. 483-491
  • Anton, S., Evengaard, K., Barrozo, R.B., Anderson, P., Skals, N., Brief predator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect (2011) Proceedings of the National Academy of Sciences US, 108 (8), pp. 3401-3405
  • Sadek, M., Anderson, P., Modulation of reproductive behaviour of Spodoptera littoralis by host and non-host plant leaves (2007) Basic and Applied Ecology, 8, pp. 444-452
  • Anderson, P., Hansson, B.S., Löfqvist, J., Plant-odor-specific receptor neurons on the antennae of female and male Spodoptera littoralis (1995) Physiological Entomology, 20 (3), pp. 189-198
  • Sadek, M.M., Wowern, G.V., Löfstedt, C., Rosén, W., Anderson, P., Modulation of the temporal pattern of calling behavior of female Spodoptera littoralis by exposure to sex pheromone (2012) Journal of Insect Physiology, 58 (1), pp. 61-66
  • Jacquin-Joly, E., Lucas, P., Pheromone reception and transduction: mammals and insects illustrate converging mechanisms across phyla (2005) Current Topics in Neurochemistry, 4, pp. 75-105
  • Guerrieri, F., Gemeno, C., Monsempes, C., Anton, S., Jacquin-Joly, E., Lucas, P., Devaud, J.M., Experience-dependent modulation of antennal sensitivity and input to antennal lobes in male moths (Spodoptera littoralis) pre-exposed to sex pheromone (2012) Journal of Experimental Biology, 215 (13), pp. 2334-2341
  • Legeai, F., Malpel, S., Montagne, N., Monsempes, C., Cousserans, F., Merlin, C., Francois, M.C., Jacquin-Joly, E., An Expressed Sequence Tag collection from the male antennae of the noctuid moth Spodoptera littoralis: A resource for olfactory and pheromone detection research (2011) BMC Genomics, 12 (1), p. 86
  • Joørgensen, K., Kvello, P., Almaas, T.J., Mustaparta, H., Two closely located areas in the suboesophageal ganglion and the tritocerebrum receive projections of gustatory receptor neurons located on the antennae and the proboscis in the moth Heliothis virescens (2006) Journal of Comparative Neurology, 496 (1), pp. 121-134
  • Kvello, P., Jorgensen, K., Mustaparta, H., Integration of taste information in the CN S of the moth Heliothis Virescens (2008) Chemical Senses, 33 (8), pp. S45-S45
  • Barrozo, R.B., Jarriault, D., Simeone, X., Gaertner, C., Gadenne, C., Anton, S., Mating-induced transient inhibition of responses to sex pheromone in a male moth is not mediated by octopamine or serotonin (2010) Journal of Experimental Biology, 213 (7), pp. 1100-1106
  • Dacks, A., Christensen, T.A., Hildebrand, J.G., Modulation of olfactory information processing in the antennal lobe of Manduca sexta by serotonin (2008) Journal of Neurophysiology, 99 (5), pp. 2077-2085
  • Ignell, R., Root, C.M., Birse, R.T., Wang, J.W., Nässel, D.R., Winther, A.M.E., Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila (2009) Proceedings of the National Academy of Sciences USA, 106 (31), pp. 13070-13075
  • Balkenius, A., Bisch-Knaden, S., Hansson, B.S., Interaction of visual and odour cues in the mushroom body of the hawkmoth Manduca sexta (2009) Journal of Experimental Biology, 212 (4), pp. 535-541
  • Nishino, H., Nishikawa, M., Yokohari, F., Mizunami, M., Dual, multilayered somatosensory maps formed by antennal tactile and contact chemosensory afferents in an insect brain (2005) Journal of Comparative Neurology, 493 (2), pp. 291-308
  • Martin, J.P., Beyerlein, A., Dacks, A.M., Reisenman, C.E., Riffell, J.A., Lei, H., Hildebrand, J.G., The neurobiology of insect olfaction: Sensory processing in a comparative context (2011) Progress in Neurobiology, 95 (3), pp. 427-447
  • Van Swinderen, B., Greenspan, R., Salience modulates 20-30 Hz brain activity in Drosophila (2003) Nature Neuroscience, 6 (6), pp. 579-586
  • Wolf, R., Heisenberg, M., On the fine structure of yaw torque in visual flight orientation of Drosophila melanogaster (1980) Journal of Comparative Physiology A, 140 (1), pp. 69-80
  • Bailey, N.W., Mate choice plasticity in the field cricket Teleogryllus oceanicus: effects of social experience in multiple modalities (2011) Behavioral Ecology and Sociobiology, 65 (12), pp. 2269-2278
  • Rutledge, J.M., Miller, A., Uetz, G.W., Exposure to multiple sensory cues as a juvenile affects adult female mate preferences in wolf spiders (2010) Animal Behaviour, 80 (3), pp. 419-426
  • Hammer, M., Menzel, R., Learning and memory in the honeybee (1995) Journal of Neuroscience, 15 (3), pp. 1617-1630


---------- APA ----------
Anton, S., Minoli, S., Gadenne, C. & Anderson, P. (2013) . Modulation of olfactory and gustatory sensitivity mediated by sensory experience in moths: A simple form of social learning?. Social Learning Theory: Phylogenetic Considerations across Animal, Plant, and Microbial Taxa, 147-162.
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Anton, S., Minoli, S., Gadenne, C., Anderson, P. "Modulation of olfactory and gustatory sensitivity mediated by sensory experience in moths: A simple form of social learning?" . Social Learning Theory: Phylogenetic Considerations across Animal, Plant, and Microbial Taxa (2013) : 147-162.
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Anton, S., Minoli, S., Gadenne, C., Anderson, P. "Modulation of olfactory and gustatory sensitivity mediated by sensory experience in moths: A simple form of social learning?" . Social Learning Theory: Phylogenetic Considerations across Animal, Plant, and Microbial Taxa, 2013, pp. 147-162.
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---------- VANCOUVER ----------
Anton, S., Minoli, S., Gadenne, C., Anderson, P. Modulation of olfactory and gustatory sensitivity mediated by sensory experience in moths: A simple form of social learning?. Soc. Learn. Theory: Phylogenetic Considerations across Anim., Plant, and Microbial Taxa. 2013:147-162.
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