Journal of Comparative Physiology A

, Volume 194, Issue 5, pp 483–489

Dynamic properties of Drosophila olfactory electroantennograms

  • Julia Schuckel
  • Shannon Meisner
  • Päivi H. Torkkeli
  • Andrew S. French
Original Paper

Abstract

Time-dependent properties of chemical signals are probably crucially important to many animals, but little is known about the dynamics of chemoreceptors. Behavioral evidence of dynamic sensitivity includes the control of moth flight by pheromone plume structure, and the ability of some blood-sucking insects to detect varying concentrations of carbon dioxide, possibly matched to host breathing rates. Measurement of chemoreceptor dynamics has been limited by the technical challenge of producing controlled, accurate modulation of olfactory and gustatory chemical concentrations over suitably wide ranges of amplitude and frequency. We used a new servo-controlled laminar flow system, combined with photoionization detection of surrogate tracer gas, to characterize electroantennograms (EAG) of Drosophila antennae during stimulation with fruit odorants or aggregation pheromone in air. Frequency response functions and coherence functions measured over a bandwidth of 0–100 Hz were well characterized by first-order low-pass linear filter functions. Filter time constant varied over almost a tenfold range, and was characteristic for each odorant, indicating that several dynamically different chemotransduction mechanisms are present. Pheromone response was delayed relative to fruit odors. Amplitude of response, and consequently signal-to-noise ratio, also varied consistently with different compounds. Accurate dynamic characterization promises to provide important new information about chemotransduction and odorant-stimulated behavior.

Keywords

Antenna Chemosensory Noise Odor Frequency response 

Abbreviations

PID

Photoionization detector

EAG

Electroantennogram

ppm

Parts per million

OR

Odorant receptor

References

  1. Alcorta E (1991) Characterization of the electroantennogram in Drosophila melanogaster and its use for identifying olfactory capture and transduction mutants. J Neurophysiol 65:702–714PubMedGoogle Scholar
  2. Barrozo RB, Kaissling KE (2002) Repetitive stimulation of olfactory receptor cells in female silkmoths Bombyx mori L. J Insect Physiol 48:825–834PubMedCrossRefGoogle Scholar
  3. Barrozo RB, Lazzari CR (2006) Orientation response of haematophagous bugs to CO2: the effect of the temporal structure of the stimulus. J Comp Physiol A 192:827–831CrossRefGoogle Scholar
  4. Bau J, Justus KA, Cardé RT (2002) Antennal resolution of pulsed pheromone plumes in three moth species. J Insect Physiol 48:433–442PubMedCrossRefGoogle Scholar
  5. Bendat JS, Piersol AG (1980) Engineering applications of correlation and spectral analysis. Wiley, New York, pp 1–302Google Scholar
  6. Benton R (2007) Sensitivity and specificity in Drosophila pheromone perception. Trends Neurosci 30:512-519PubMedCrossRefGoogle Scholar
  7. Carlsson MA, Hansson BS (2002) Responses in highly selective sensory neurons to blends of pheromone components in the moth Agrotis segetum. J Insect Physiol 48:443–451PubMedCrossRefGoogle Scholar
  8. Cooley JW, Tukey JW (1965) An algorithm for the machine calculation of complex Fourier series. Math Comput 19:297–301CrossRefGoogle Scholar
  9. Dobritsa AA, van der Goes van Naters W, Warr CG, Steinbrecht RA, Carlson JR (2003) Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37:827–841PubMedCrossRefGoogle Scholar
  10. French AS, Meisner S (2007) A new method for wide frequency range dynamic olfactory stimulation and characterization. Chem Senses 32:681–688PubMedCrossRefGoogle Scholar
  11. Geier M, Bosch OJ, Boeckh J (1999) Influence of odour plume structure on upwind flight of mosquitoes towards hosts. J Exp Biol 202:1639–1648PubMedGoogle Scholar
  12. Golomb S (1967) Shift register sequences. Holden-Day, San Francisco, pp 1–224Google Scholar
  13. Hallem EA, Ho MG, Carlson JR (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117:965–979PubMedCrossRefGoogle Scholar
  14. Hazel MH, Ianowski JP, Christensen RJ, Maddrell SH, O’Donnell MJ (2003) Amino acids modulate ion transport and fluid secretion by insect Malpighian tubules. J Exp Biol 206:79–91PubMedCrossRefGoogle Scholar
  15. Hedlund K, Bartelt RJ, Dicke M, Vet LEM (1996) Aggregation pheromones of Drosophila immigrans, D. phalerata, and D. subobscura. J Chem Ecol 22:1835–1844CrossRefGoogle Scholar
  16. Justus KA, Schofield SW, Murlis J, Cardé RT (2002) Flight behaviour of Cadra cautella males in rapidly pulsed pheromone plumes. Physiol Entomol 27:59–66Google Scholar
  17. Justus KA, Cardé RT, French AS (2005) Dynamic properties of antennal responses to pheromone in two moth species. J Neurophysiol 93:2233–2239PubMedCrossRefGoogle Scholar
  18. Juusola M, French AS (1997) The efficiency of sensory information coding by mechanoreceptor neurons. Neuron 18:959–968PubMedCrossRefGoogle Scholar
  19. Juusola M, Niven JE, French AS (2003) Shaker K+ channels contribute early nonlinear amplification to the light response in Drosophila photoreceptors. J Neurophysiol 90:2014–2021PubMedCrossRefGoogle Scholar
  20. Karmeier K, van Hateren JH, Kern R, Egelhaaf M (2006) Encoding of naturalistic optic flow by a population of blowfly motion-sensitive neurons. J Neurophysiol 96:1602–1614PubMedCrossRefGoogle Scholar
  21. Kapitskii SV, Gribakin FG (1992) Electroantennogram of the American cockroach: effect of oxygen and an electrical model. J Comp Physiol A 170:651–663PubMedCrossRefGoogle Scholar
  22. Lucas P, Renou M (1992) Electrophysiological study of the effects of deltamethrin, bioresmethrin, and DDT on the activity of pheromone receptor neurones in two moth species. Pest Biochem Physiol 43:103–115CrossRefGoogle Scholar
  23. Mafra-Neto A, Cardé RT (1995) Influence of plume structure and pheromone concentration on upwind flight of Cadra cautella males. Physiol Entomol 20:117–133CrossRefGoogle Scholar
  24. Marmarelis PZ, Marmarelis VZ (1978) Analysis of physiological systems: the white-noise approach. Plenum Press, New YorkGoogle Scholar
  25. Minor AV, Kaissling KE (2003) Cell responses to single pheromone molecules may reflect the activation kinetics of olfactory receptor molecules. J Comp Physiol A 189:221–230Google Scholar
  26. Murlis J, Elkington JS, Cardé RT (1992) Odor plumes and how insects use them. Annu Rev Entomol 37:505–532CrossRefGoogle Scholar
  27. Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, UrbanaGoogle Scholar
  28. Stensmyr MC, Giordano E, Balloi A, Angioy AM, Hansson BS (2003) Novel natural ligands for Drosophila olfactory receptor neurones. J Exp Biol 206:715–724PubMedCrossRefGoogle Scholar
  29. Vickers NJ, Christensen TA, Baker TC, Hildebrand JG (2001) Odour-plume dynamics influence the brain’s olfactory code. Nature 410:466–470PubMedCrossRefGoogle Scholar
  30. Willis MA, Baker TC (1984) Effects of intermittent and continuous pheromone stimulation on the flight behaviour of the oriental fruit moth, Grapholita molesta. Physiol Entomol 9:341–358CrossRefGoogle Scholar
  31. Yao CA, Ignell R, Carlson JR (2005) Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J Neurosci 25:8359–8367PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Julia Schuckel
    • 1
  • Shannon Meisner
    • 1
  • Päivi H. Torkkeli
    • 1
  • Andrew S. French
    • 1
  1. 1.Department of Physiology and BiophysicsDalhousie UniversityHalifaxCanada

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