Skip to main content
Log in

Olfaction in insects

The primary processes of odor recognition and coding

  • Review article
  • Published:
e-Neuroforum

Summary

Odorants provide insects with crucial information about their environment and trigger various insect behaviors. A remarkably sensitive and selective sense of smell allows the animals to detect extremely low amounts of relevant odorants and thereby recognize, e.g., food, conspecifics, and predators. In recent years, significant progress has been made towards understanding the molecular elements and cellular mechanisms of odorant detection in the antenna and the principles underlying the primary processing of olfactory signals in the brain. These findings show that olfactory hairs on the antenna are specifically equipped with chemosensory detector units. They contain several binding proteins, which transfer odorants to specific receptors residing in the dendritic membrane of olfactory sensory neurons (OSN). Binding of odorant to the receptor initiates ionotropic and/or metabotropic mechanisms, translating the chemical signal into potential changes, which alter the spontaneous action potential frequency in the axon of the sensory neurons. The odor-dependent action potentials propagate from the antennae along the axon to the brain leading to an input signal within the antennal lobe. In the antennal lobe, the first relay station for olfactory information, the input signals are extensively processed by a complex network of local interneurons before being relayed by projection neurons to higher brain centers, where olfactory perception takes place.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Abuin L, Bargeton B, Ulbrich MH, Isacoff EY, Kellenberger S, Benton R (2011) Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69:44–60

    Article  PubMed  CAS  Google Scholar 

  2. Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4:e20

    Article  PubMed  Google Scholar 

  3. Benton R, Vannice KS, Vosshall LB (2007) An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450:289–293

    Article  PubMed  CAS  Google Scholar 

  4. Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136:149–162

    Article  PubMed  CAS  Google Scholar 

  5. Berg BG, Galizia CG, Brandt R, Mustaparta H (2002) Digital atlases of the antennal lobe in two species of tobacco budworm moths, the Oriental Helicoverpa assulta (male) and the American Heliothis virescens (male and female). J Comp Neurol 446:123–134

    Article  PubMed  Google Scholar 

  6. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187

    Article  PubMed  CAS  Google Scholar 

  7. Butenandt A, Beckmann R, Stamm D, Hecker E (1959) Über den Sexuallockstoff des Seidenspinners Bombyx mori, Reindarstellung und Konstitution. Zeitschrift für Naturforschung 14:283–284

    Google Scholar 

  8. Carey AF, Wang G, Su CY, Zwiebel LJ, Carlson JR (2010) Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464:66–71

    Article  PubMed  CAS  Google Scholar 

  9. Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327–338

    Article  PubMed  CAS  Google Scholar 

  10. Croset V, Rytz R, Cummins SF, Budd A, Brawand D, Kaessmann H, Gibson TJ, Benton R (2010) Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet 6:e1001064

    Article  PubMed  Google Scholar 

  11. Distler PG, Boeckh J (1996) Synaptic connection between olfactory receptor cells and uniglomerular projection neurons in the antennal lobe of the American cockroach, Periplaneta americana. J Comp Neurol 370:35–46

    Article  PubMed  CAS  Google Scholar 

  12. Distler PG, Boeckh J (1997a) Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana: I. Uniglomerular projection neurons. J Comp Neurol 378:307–319

    Article  PubMed  CAS  Google Scholar 

  13. Distler PG, Boeckh J (1997b) Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana: II. Local multiglomerular interneurons. J Comp Neurol 383:529–540

    Article  PubMed  CAS  Google Scholar 

  14. Fabre JH (1879) Hochzeitsflüge der Nachtpfauenaugen. In: Bilder aus der Insektenwelt: Übersetzung aus “Souvenirs Entomologiques”I. X. Kosmos, Gesellschaft der Naturfreunde, Paris, Stuttgart, p 80

  15. Fiala A, Spall T, Diegelmann S, Eisermann B, Sachse S, Devaud JM, Buchner E, Galizia CG (2002) Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons. Curr Biol 12:1877–1884

    Article  PubMed  CAS  Google Scholar 

  16. Forstner M, Gohl T, Gondesen I, Raming K, Breer H, Krieger J (2008) Differential expression of SNMP-1 and SNMP-2 proteins in pheromone-sensitive hairs of moths. Chem Senses 33:291–299

    Article  PubMed  CAS  Google Scholar 

  17. Forstner M, Breer H, Krieger J (2009) A receptor and binding protein interplay in the detection of a distinct pheromone component in the silkmoth Antheraea polyphemus. Int J Biol Sci 5:745–757

    PubMed  CAS  Google Scholar 

  18. Galizia CG, Menzel R (2000) Odour perception in honeybees: coding information in glomerular pattern. Curr Opin Neurobiol 10:504–510

    Article  PubMed  CAS  Google Scholar 

  19. Galizia CG, Sachse S, Rappert A, Menzel R (1999) The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat Neurosci 2:473–478

    Article  PubMed  CAS  Google Scholar 

  20. Gohl T, Krieger J (2006) Immunolocalization of a candidate pheromone receptor in the antenna of the male moth, Heliothis virescens. J Inv Neurosci 6:13–21

    Article  CAS  Google Scholar 

  21. Grosse-Wilde E, Svatos A, Krieger J (2006) A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem Senses 31:547–555

    Article  PubMed  CAS  Google Scholar 

  22. Grosse-Wilde E, Gohl T, Bouche E, Breer H, Krieger J (2007) Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. Eur J Neurosci 25:2364–2373

    Article  PubMed  Google Scholar 

  23. Ha TS, Smith DP (2006) A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J Neurosci 26:8727–8733

    Article  PubMed  CAS  Google Scholar 

  24. Ha TS, Smith DP (2009) Odorant and pheromone receptors in insects. Front Cell Neurosci 3:10

    Article  PubMed  Google Scholar 

  25. Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125:143–160

    Article  PubMed  CAS  Google Scholar 

  26. 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 

  27. Huang J, Zhang W, Qiao W, Hu A, Wang Z (2010) Functional connectivity and selective odor responses of excitatory local interneurons in Drosophila antennal lobe. Neuron 67:1021–1033

    Article  PubMed  CAS  Google Scholar 

  28. Joerges J, Küttner A, Galizia CG, Menzel R (1997) Representation of odours and odour mixtures visualized in the honeybee brain. Nature 387:285–288

    Article  CAS  Google Scholar 

  29. Jones WD, Nguyen TAT, Kloss B, Lee KJ, Vosshall LB (2005) Functional conservation of an insect odorant receptor gene across 250 million years of evolution. Current Biology 15:R119–R121

    Article  PubMed  CAS  Google Scholar 

  30. Kreher SA, Kwon JY, Carlson JR (2005) The molecular basis of odor coding in the Drosophila larva. Neuron 46:445–456

    Article  PubMed  CAS  Google Scholar 

  31. Krieger J, Klink O, Mohl C, Raming K, Breer H (2003) A candidate olfactory receptor subtype highly conserved across different insect orders. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189:519–526

    Article  PubMed  CAS  Google Scholar 

  32. Krieger J, Grosse-Wilde E, Gohl T, Dewer YME, Raming K, Breer H (2004) Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). Proc Natl Acad Sci U S A 101:11845–11850

    Article  PubMed  CAS  Google Scholar 

  33. Krieger J, Grosse-Wilde E, Gohl T, Breer H (2005) Candidate pheromone receptors of the silkmoth Bombyx mori. Eur J Neurosci 21:2167–2176

    Article  PubMed  Google Scholar 

  34. Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF (1999) Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405:543–552

    Article  PubMed  CAS  Google Scholar 

  35. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703–714

    Article  PubMed  CAS  Google Scholar 

  36. Laughlin JD, Ha TS, Jones DN, Smith DP (2008) Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133:1255–1265

    Article  PubMed  CAS  Google Scholar 

  37. Mitsuno H, Sakurai T, Murai M, Yasuda T, Kugimiya S, Ozawa R, Toyohara H, Takabayashi J, Miyoshi H, Nishioka T (2008) Identification of receptors of main sex-pheromone components of three Lepidopteran species. Eur J Neurosci 28:893–902

    Article  PubMed  Google Scholar 

  38. Mohl C, Breer H, Krieger J (2002) Species-specific pheromonal compounds induce distinct conformational changes of pheromone binding protein subtypes from Antheraea polyphemus. Invert Neurosci 4:165–174

    Article  PubMed  CAS  Google Scholar 

  39. Nakagawa T, Vosshall LB (2009) Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr Opin Neurobiol 19:284–292

    Article  PubMed  CAS  Google Scholar 

  40. Nakagawa T, Sakurai T, Nishioka T, Touhara K (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307:1638–1642

    Article  PubMed  CAS  Google Scholar 

  41. Ng M, Roorda RD, Lima SQ, Zemelman BV, Morcillo P, Miesenbock G (2002) Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36:463–474

    Article  PubMed  CAS  Google Scholar 

  42. Olsen SR, Wilson RI (2008) Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452:956–960

    Article  PubMed  CAS  Google Scholar 

  43. Qiao H, Xiaoli H, Schymura D, Ban L, Field L, Dani FR, Michelucci E, Caputo B, della Torre A, Iatrou K, Krieger J, Zhou JJ, Pelosi P (2010) Comparative interactions between odorant-binding proteins of Anophels gambiae. Cell Mol Life Sci (in press)

  44. Rogers ME, Sun M, Lerner MR, Vogt RG (1997) Snmp-1, a novel membrane protein of olfactory neurons of the silk moth Antheraea polyphemus with homology to the CD36 family of membrane proteins. J Biol Chem 272:14792–14799

    Article  PubMed  CAS  Google Scholar 

  45. Sachse S, Galizia CG (2002) Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106–1117

    PubMed  Google Scholar 

  46. Sachse S, Rappert A, Galizia CG (1999) The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code. Eur J Neurosci 11:3970–3982

    Article  PubMed  CAS  Google Scholar 

  47. Sakurai T, Nakagawa T, Mitsuno H, Mori H, Endo Y, Tanoue S, Yasukochi Y, Touhara K, Nishioka T (2004) Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc Natl Acad Sci U S A 101:16653–16658

    Article  PubMed  CAS  Google Scholar 

  48. Sandler BH, Nikonova L, Leal WS, Clardy J (2000) Sexual attraction in the silkworm moth: structure of the pheromone-binding-protein-bombykol complex. Chem Biol 7:143–151

    Article  PubMed  CAS  Google Scholar 

  49. Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1006

    Article  PubMed  CAS  Google Scholar 

  50. Silbering AF, Okada R, Ito K, Galizia CG (2008) Olfactory information processing in the Drosophila antennal lobe: anything goes? J Neurosci 28:13075–13087

    Article  PubMed  CAS  Google Scholar 

  51. Silverstein RL, Febbraio M (2009) CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci Signal 2:re3

    Article  PubMed  Google Scholar 

  52. Stengl M (2010) Pheromone transduction in moths. Front Cell Neurosci 4:133

    Article  PubMed  Google Scholar 

  53. Vogt RG (2003) Biochemical diversity of odor detection: OBPs, ODEs and SNMPs. In: Blomquist G, Vogt RG (eds) Insect pheromone biochemistry and molecular biology. The biosynthesis and detection of pheromones and plant volatiles. Elsevier Academic Press, London, pp 391–445

  54. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725–736

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  56. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271–282

    Article  PubMed  CAS  Google Scholar 

  57. Wang G, Carey AF, Carlson JR, Zwiebel LJ (2010) Molecular basis of odor coding in the malaria vector mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 107:4418–4423

    Article  PubMed  CAS  Google Scholar 

  58. Wanner KW, Anderson AR, Trowell SC, Theilmann DA, Robertson HM, Newcomb RD (2007) Female-biased expression of odourant receptor genes in the adult antennae of the silkworm, Bombyx mori. Insect Mol Biol 16:107–119

    Article  PubMed  CAS  Google Scholar 

  59. Wicher D, Schafer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452:1007–1011

    Article  PubMed  CAS  Google Scholar 

  60. Wilson RI, Turner GC, Laurent G (2004) Transformation of olfactory representations in the Drosophila antennal lobe. Science 303:366–370

    Article  PubMed  CAS  Google Scholar 

  61. Wojtasek H, Leal WS (1999) Conformational change in the pheromone-binding protein from Bombyx mori induced by pH and by interaction with membranes. J Biol Chem 274:30950–30956

    Article  PubMed  CAS  Google Scholar 

  62. Xu PX, Atkinson R, Jones DNM, Smith DP (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45:193–200

    Article  PubMed  CAS  Google Scholar 

  63. Yaksi E, Wilson RI (2010) Electrical coupling between olfactory glomeruli. Neuron 67:1034–1047

    Article  PubMed  CAS  Google Scholar 

  64. Zhou JJ (2010) Odorant-binding proteins in insects. Vitam Horm 83:241–272

    Article  PubMed  CAS  Google Scholar 

Download references

Conflict of interest

The corresponding author states that there are no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Silke Sachse.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sachse, S., Krieger, J. Olfaction in insects. e-Neuroforum 2, 49–60 (2011). https://doi.org/10.1007/s13295-011-0020-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13295-011-0020-7

Keywords

Navigation