Skip to main content
SpringerLink
Log in

Function and central projections of gustatory receptor neurons on the antenna of the noctuid moth Spodoptera littoralis

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Chemosensory information is crucial for most insects to feed and reproduce. Olfactory signals are mainly used at a distance, whereas gustatory stimuli play an important role when insects directly contact chemical substrates. In noctuid moths, although the antennae are the main olfactory organ, they also bear taste sensilla. These taste sensilla detect sugars and hence are involved in appetitive learning but could also play an important role in food evaluation by detecting salts and bitter substances. To investigate this, we measured the responses of individual taste sensilla on the antennae of Spodoptera littoralis to sugars and salts using tip recordings. We also traced the projections of their neuronal axons into the brain. In each sensillum, we found one or two neurons responding to sugars: one NaCl-responsive and one water-sensitive neuron. Responses of these neurons were dose-dependent and similar across different locations on the antenna. Responses were dependent on the sex for sucrose and on both sex and location for glucose and fructose. We did not observe a spatial map for the projections from specific regions of the antennae to the deutocerebrum or the tritocerebrum/suboesophageal ganglion complex. In accordance with physiological recordings, back-fills from individual sensilla revealed up to four axons, in most cases targeting different projection zones.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Accolla R, Bathellier B, Petersen CCH, Carleton A (2007) Differential spatial representation of taste modalities in the rat gustatory cortex. J Neurosci 27:1396–1404

    Article  PubMed  CAS  Google Scholar 

  • Altner H, Sass H, Altner I (1977) Relationship between structure and function of antennal chemoreceptive, hygroreceptive, and thermoreceptive sensilla in Periplaneta americana. Cell Tissue Res 176:389–405

    Article  PubMed  CAS  Google Scholar 

  • Anderson P, Hallberg E (1990) Structure and distribution of tactile and bimodal taste tactile sensilla on the ovipositor, tarsi and antennae of the flour moth, Ephestia kuehniella (Zeller) (Lepidoptera, Pyralidae). Int J Insect Morphol Embryol 19:13–23

    Article  Google Scholar 

  • Barrozo RB, Couton L, Lazzari CR, Insausti TC, Minoli SA, Fresquet N, Rospars JP, Anton S (2009) Arthropod Struct Dev 38:101–110

    Article  PubMed  CAS  Google Scholar 

  • Calas D, Berthier A, Marion-Poll F (2007) Do European corn borer females detect and avoid laying eggs in the presence of 20-Hydroxyecdysone? J Chem Ecol 33:1393–1404

    Article  PubMed  CAS  Google Scholar 

  • Camazine SM, Hildebrand JG (1979) Central projections of antennal sensory neurons in mature and developing Manduca sexta. Soc Neurosci Abstr 5:155

    Google Scholar 

  • Cameron P, Hiroi M, Ngai J, Scott K (2010) The molecular basis for water taste in Drosophila. Nature 465:91–95

    Article  PubMed  CAS  Google Scholar 

  • Chaika SY, Sinitsina EE (1997) Antennal sensory organs of the flour moth Ephestia kuehniella Zell. (Lepidoptera: Pyralidae). Moscow Univ Biol Sci Bull 52:29–35

    Google Scholar 

  • Chapman RF (1982) Chemoreception: the significance of receptor numbers. Adv Insect Physiol 16:247–333

    Article  CAS  Google Scholar 

  • Chapman RF (2003) Contact chemoreception in feeding by phytophagous insects. Annu Rev Entomol 48:455–484

    Article  PubMed  CAS  Google Scholar 

  • Cornford ME, Rowley WA, Klun JA (1973) Scanning electron-microscopy of antennal sensilla of European corn borer, Ostrinia nubilalis Lepidoptera-Pyralidae. Ann Entomol Soc Am 66:1079–1088

    Google Scholar 

  • Cuperus PL (1985) Ultrastructure of antennal sense organs of small ermine moths, Yponomeuta spp (Lepidoptera, Yponomeutidae). Int J Insect Morphol Embryol 14:179–191

    Article  Google Scholar 

  • Dahanukar A, Hallem EA, Carlson JR (2005) Insect chemoreception. Curr Opin Neurobiol 15:423–430

    Article  PubMed  CAS  Google Scholar 

  • Dethier VG (1976) The hungry fly: a physiological study of the behavior associated with feeding. Harvard University Press, Cambridge

    Google Scholar 

  • Edgecomb RS, Murdock LL (1992) Central projections of axons from taste hairs n the labellum and tarsi of the blowfly, Phormia regina Meigen. J Comp Neurol 315:431–444

    Article  PubMed  CAS  Google Scholar 

  • Evans DR, Mellon D (1962) Electrophysiological studies of a water receptor associated with taste sensilla of the blowfly. J Gen Physiol 45:487–500

    Article  PubMed  CAS  Google Scholar 

  • Fan RJ, Anderson P, Hansson BS (1997) Behavioural analysis of olfactory conditioning in the moth Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae). J Exp Biol 200:2969–2976

    PubMed  Google Scholar 

  • Fujishiro N, Kijima H, Morita H (1984) Impulse frequency and action potential amplitude in the labellar chemosensory neurones of Drosophila melanogaster. J Insect Physiol 30:317–325

    Article  Google Scholar 

  • Galizia CG, Menzel R (2001) The role of glomeruli in the neural representation of odours: results from optical recording studies. J Insect Physiol 47:115–130

    Article  PubMed  CAS  Google Scholar 

  • Grant GG, Zhao B, Langevin D (2000) Oviposition response of spruce budworm (Lepidoptera: Tortricidae) to aliphatic carboxylic acids. Environ Entomol 29:164–170

    Article  CAS  Google Scholar 

  • Hansson BS, Anton S (2000) Function and morphology of the antennal lobe: new developments. Annu Rev Entomol 45:203–231

    Article  PubMed  CAS  Google Scholar 

  • Hartlieb E, Anderson P, Hansson BS (1999) Appetitive learning of odours with different behavioural meaning in moths. Physiol Behav 67:671–677

    Article  PubMed  CAS  Google Scholar 

  • Haupt SS (2007) Central gustatory projections and side-specificity of operant antennal muscle conditioning in the honeybee. J Comp Physiol A 193:523–535

    Article  Google Scholar 

  • Heisenberg M (2003) Mushroom body memoir: from maps to models. Nature Rev Neurosci 4:266–275

    Article  CAS  Google Scholar 

  • Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595–631

    Article  PubMed  CAS  Google Scholar 

  • Hiroi M, Marion-Poll F, Tanimura T (2002) Differentiated response to sugars among labellar chemosensilla in Drosophila. Zoolog Sci 19:1009–1018

    Article  PubMed  Google Scholar 

  • Hiroi M, Meunier N, Marion-Poll F, Tanimura T (2004) Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J Neurobiol 61:333–342

    Article  PubMed  Google Scholar 

  • Hodgson ES, Lettvin JY, Roeder KD (1955) Physiology of a primary chemoreceptor unit. Science 122:417–418

    Article  PubMed  CAS  Google Scholar 

  • Homberg U, Christensen TA, Hildebrand JG (1989) Structure and function of the deutocerebrum in insects. Annu Rev Entomol 34:477–501

    Article  PubMed  CAS  Google Scholar 

  • Inoshita T, Tanimura T (2006) Cellular identification of water gustatory receptor neurons and their central projection pattern in Drosophila. Proc Natl Acad Sci USA 103:1094–1099

    Article  PubMed  CAS  Google Scholar 

  • Jørgensen K, Kvello P, Almaas TJ, Mustaparta H (2006) 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. J Comp Neurol 496:121–134

    Article  PubMed  Google Scholar 

  • Jørgensen K, Almaas TJ, Marion-Poll F, Mustaparta H (2007) Electrophysiological characterization of responses from gustatory receptor neurons of sensilla chaetica in the moth Heliothis virescens. Chem Senses 32:863–879

    Article  PubMed  Google Scholar 

  • Kent KS, Hildebrand JG (1987) Cephalic sensory pathways in the central nervous system of larval Manduca sexta (Lepidoptera: Sphingidae). Philos Trans R Soc London B Biol Sci 315:1–36

    Article  PubMed  CAS  Google Scholar 

  • Kloppenburg P (1995) Anatomy of the antennal motoneurons in the brain of the honeybee (Apis mellifera). J Comp Neurol 363:333–343

    Article  PubMed  CAS  Google Scholar 

  • Kloppenburg P, Camazine SM, Sun XJ, Randolph P, Hildebrand JG (1997) Organization of the antennal motor system in the sphinx moth Manduca sexta. Cell Tissue Res 287:425–433

    Article  PubMed  CAS  Google Scholar 

  • Kvello P, Almaas TJ, Mustaparta H (2006) A confined taste area in a lepidopteran brain. Arthrop Struct Dev 35:35–45

    Article  Google Scholar 

  • Kvello P, Jørgensen K, Mustaparta H (2010) Central gustatory neurons integrate taste quality information from four appendages in the moth Heliothis virescens. J Neurophysiol 103:2965–2981

    Article  PubMed  Google Scholar 

  • Lacaille F, Hiroi M, Twele R, Inoshita T, Umemoto D, Maniere G, Marion-Poll F, Ozaki M, Francke W, Cobb M et al (2007) An inhibitory sex pheromone tastes bitter for Drosophila males. PLoS One 2:e661

    Article  PubMed  Google Scholar 

  • Liscia A, Majone R, Solari P, Barbarossa IT, Crnjar R (1998) Sugar response differences related to sensillum type and location on the labella of Protophormia terraenovae: a contribution to spatial representation of the stimulus. J Insect Physiol 44:471–481

    Article  PubMed  CAS  Google Scholar 

  • Maes FW, Den Otter CJ (1976) Relationship between taste cell responses and arrangement of labellar taste setae in the blowfly Calliphora vicina. J Insect Physiol 22:377–384

    Article  PubMed  CAS  Google Scholar 

  • Marella S, Fischler W, Kong P, Asgarian S, Reukhert E, Scott K (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49:285–295

    Article  PubMed  CAS  Google Scholar 

  • Marion-Poll F (1996) Display and analysis of electrophysiological data under MS-Windows. Entomol Exp Appl 80:116–119

    Article  Google Scholar 

  • Marion-Poll F, Van der Pers JNC (1996) Un-filtered recordings from insect taste sensilla. Entomol Exp Appl 80:113–115

    Article  Google Scholar 

  • Masek P, Scott K (2010) Limited taste discrimination in Drosophila. Proc Natl Acad Sci USA 107:14833–14838

    Article  PubMed  CAS  Google Scholar 

  • Menzel R, Muller U (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu Rev Neurosci 19:379–404

    Article  PubMed  CAS  Google Scholar 

  • Merivee E, Renou M, Mänd M, Luik A, Heidemaa M, Ploomi A (2004) Electrophysiological responses to salts from antennal chaetoid taste sensilla of the ground beetle Pterostichus aethiops. J Insect Physiol 50:1001–1013

    Article  PubMed  CAS  Google Scholar 

  • Meunier N, Ferveur JF, Marion-Poll F (2000) Sex-specific non-pheromonal taste receptors in Drosophila. Curr Biol 10:1583–1586

    Article  PubMed  CAS  Google Scholar 

  • Meunier N, Marion-Poll F, Lansky P, Rospars JP (2003a) Estimation of the individual firing frequencies of two neurons recorded with a single electrode. Chem Senses 28:671–679

    Article  PubMed  Google Scholar 

  • Meunier N, Marion-Poll F, Rospars JP, Tanimura T (2003b) Peripheral coding of bitter taste in Drosophila. J Neurobiol 56:139–152

    Article  PubMed  Google Scholar 

  • Mitchell BK, Itagaki H (1992) Interneurons of the subesophageal ganglion of Sarcophaga bullata responding to gustatory and mechanosensory stimuli. J Comp Physiol A 171:213–230

    Article  PubMed  CAS  Google Scholar 

  • Mitchell BK, Itagaki H, Rivet MP (1999) Peripheral and central structures involved in insect gustation. Microsc Res Tech 47:401–415

    Article  PubMed  CAS  Google Scholar 

  • Müller C, Riederer M (2005) Plant surface properties in chemical ecology. J Chem Ecol 31:2621–2651

    Article  PubMed  Google Scholar 

  • Murphey RK, Possidente D, Pollack G, Merritt DJ (1989) Modality-specific axonal projections in the CNS of the flies Phormia and Drosophila. J Comp Neurol 290:185–200

    Article  PubMed  CAS  Google Scholar 

  • Newland PL (1999) Processing of gustatory information by spiking local interneurons in the locust. J Neurophysiol 82:3149–3159

    PubMed  CAS  Google Scholar 

  • Newland PL, Rogers SM, Gaaboub I, Matheson T (2000) Palrallel somatotopic maps of gustatory and mechanosensory neurons in the central nervous system of an insect. J Comp Neurol 425:82–96

    Article  PubMed  CAS  Google Scholar 

  • Nishino H, Nishikawa M, Yokohari F, Mizunami M (2005) Dual, multilayered somatosensory maps formed by antennal tactile and contact chemosensory afferents in an insect brain. J Comp Neurol 493:291–308

    Article  PubMed  Google Scholar 

  • Poitout S, Bues R (1974) Linoleic acid requirement of Lepidoptera reared in artificial medium, Noctuidae, Quadrifinae and Plusiinae: Chrysodeixis chalcites Esp., Autographa gamma L., Macdunnoughia confusa Stph., Trichoplusia ni Hbn. Ann Nutr Aliment 28:173–187

    PubMed  CAS  Google Scholar 

  • Powell G, Maniar SP, Pickett JA, Hardie J (1999) Aphid responses to non-host epicuticular lipids. Entomol Exp Appl 91:115–123

    Article  Google Scholar 

  • Rees CJC (1970) The primary process of reception in the type 3 (‘water’) receptor cell of the fly, Phormia terranovae. Proc R Soc Lond B 174:469–490

    Article  Google Scholar 

  • Renwick JA (1989) Chemical ecology of oviposition in phytophagous insects. Experientia 45:223–228

    Article  CAS  Google Scholar 

  • Rogers SM, Simpson SJ (1999) Chemo-discriminatory neurones in the sub-oesophageal ganglion of Locusta migratoria. Entomol Exp Appl 91:19–28

    Article  Google Scholar 

  • Rospars JP (1983) Invariance and sex-specific variations of the glomerular organization in the antennal lobes of a moth, Mamestra brassicae, and a butterfly, Pieris brassicae. J Comp Neurol 220:80–96

    Article  PubMed  CAS  Google Scholar 

  • Rospars JP (1988) Structure and development of the insect antennodeutocerebral system. Int J Insect Morphol Embryol 17:243–294

    Article  Google Scholar 

  • Schoonhoven LM, van Loon JJA (2002) An inventory of taste in caterpillars: each species its own key. Acta Zool Acad Sci Hung 48:215–263

    Google Scholar 

  • Singh RN (1997) Neurobiology of the gustatory systems of Drosophila and some terrestrial insects. Microsc Res Tech 39:547–563

    Article  PubMed  CAS  Google Scholar 

  • Skiri HT, Ro H, Berg BG, Mustaparta H (2005) Consistent organization of glomeruli in the antennal lobes of related species of heliothine moths. J Comp Neurol 491:367–380

    Article  PubMed  Google Scholar 

  • Steinbauer MJ, Schiestl FP, Davies NW (2004) Monoterpenes and epicuticular waxes help female autumn gum moth differentiate between waxy and glossy Eucalyptus and leaves of different ages. J Chem Ecol 30:1117–1142

    Article  PubMed  CAS  Google Scholar 

  • Stocker RF (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275:3–26

    Article  PubMed  CAS  Google Scholar 

  • Thorne N, Chromey C, Bray S, Amrein H (2004) Taste perception and coding in Drosophila. Curr Biol 14:1065–1079

    Article  PubMed  CAS  Google Scholar 

  • Udayagiri S, Mason CE (1997) Epicuticular wax chemicals in Zea mays influence oviposition in Ostrinia nubilalis. J Chem Ecol 23:1675–1687

    Article  CAS  Google Scholar 

  • Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102:147–159

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Singhvi A, Kong P, Scott K (2004) Taste representations in the Drosophila brain. Cell 117:981–991

    Article  PubMed  CAS  Google Scholar 

  • Wieczorek H, Köppl R (1978) Effect of sugars on the labellar water receptor of the fly. J Comp Physiol A 126:131–136

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a doctoral fellowship to AP from the doctoral school ABIES and the bilateral exchange program Aurora (EGIDE). Romina Barrozo and Sebastian Minoli are acknowledged for help with the figures and Dominique Van Oort for help with the scanning electron microscopy. We thank Delphine Calas-List for helpful comments on the manuscript.

Author information

Author notes

  1. Louise Couton

    Present address: Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, UK

  2. Sylvia Anton

    Present address: Laboratoire RCIM, UPRES-EA 2647, USC INRA 1330, UFR Sciences, Université d’Angers, 2 Boulevard Lavoisier, 49045, Angers, France

Authors and Affiliations

  1. INRA/Université Pierre et Marie Curie, UMR PISC 1272, Centre de Recherches de Versailles, Route de St Cyr, 78026, Versailles cedex, France

    Alexandra Popescu, Louise Couton, Jean-Pierre Rospars, Frédéric Marion-Poll & Sylvia Anton

  2. Department of Biology, Faculty of Natural Sciences and Technology, Norwegian University of Science and Technology, 7491, Trondheim, Norway

    Tor-Jørgen Almaas

  3. Centre for Behaviour and Evolution, Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, NE4 6EJ, UK

    Geraldine A. Wright

  4. Département Sciences de la Vie et Santé, AgroParisTech, 16 rue Claude Bernard, 75231, Paris Cedex 05, France

    Frédéric Marion-Poll

Authors
  1. Alexandra Popescu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Louise Couton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tor-Jørgen Almaas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jean-Pierre Rospars
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Geraldine A. Wright
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Frédéric Marion-Poll
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sylvia Anton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sylvia Anton.

Additional information

F. Marion-Poll and S. Anton share senior authorship.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Popescu, A., Couton, L., Almaas, TJ. et al. Function and central projections of gustatory receptor neurons on the antenna of the noctuid moth Spodoptera littoralis . J Comp Physiol A 199, 403–416 (2013). https://doi.org/10.1007/s00359-013-0803-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-013-0803-0

Keywords

Search

Navigation