Modeling the response of a population of olfactory receptor neurons to an odorant

  • Malin Sandström
  • Anders Lansner
  • Jeanette Hellgren-Kotaleski
  • Jean-Pierre Rospars
Article

Abstract

We modeled the firing rate of populations of olfactory receptor neurons (ORNs) responding to an odorant at different concentrations. Two cases were considered: a population of ORNs that all express the same olfactory receptor (OR), and a population that expresses many different ORs. To take into account ORN variability, we replaced single parameter values in a biophysical ORN model with values drawn from statistical distributions, chosen to correspond to experimental data. For ORNs expressing the same OR, we found that the distributions of firing frequencies are Gaussian at all concentrations, with larger mean and standard deviation at higher concentrations. For a population expressing different ORs, the distribution of firing frequencies can be described as the superposition of a Gaussian distribution and a lognormal distribution. Distributions of maximum value and dynamic range of spiking frequencies in the simulated ORN population were similar to experimental results.

Keywords

Olfaction Sensory coding Olfactory receptor neuron Neural population modeling 

References

  1. Abraham, N. M., Spors, H., Carleton, A., Margrie, T. W., Kuner, T., & Schaefer, A. T. (2004). Maintaining accuracy at the expense of speed: stimulus similarity defines odor discrimination time in mice. Neuron, 44, 865–876.PubMedGoogle Scholar
  2. Bargmann, C. I. (2006). Comparative chemosensation from receptors to ecology. Nature, 444, 295–301. doi:10.1038/nature05402.CrossRefPubMedGoogle Scholar
  3. Bazhenov, M., Stopfer, M., Rabinovich, M., Abarbanel, H. D. J., Sejnowski, T. J., & Laurent, G. (2001). Model of cellular and network mechanisms for odor-evoked temporal patterning in the locust antennal lobe. Neuron, 30, 569–581. doi:10.1016/S0896-6273(01)00286-0.CrossRefPubMedGoogle Scholar
  4. Cleland, T. A., & Linster, C. (1999). Concentration tuning mediated by spare receptor capacity in olfactory sensory neurons: a theoretical study. Neural Computation, 11, 1673–1690. doi:10.1162/089976699300016188.CrossRefPubMedGoogle Scholar
  5. Cleland, T. A., & Linster, C. (2005). Computation in the olfactory system. Chemical Senses, 30, 801–813. doi:10.1093/chemse/bji072.CrossRefPubMedGoogle Scholar
  6. Christensen, T. A., D’Alessandro, G., Lega, J., & Hildebrand, J. G. (2001). Morphometric modeling of olfactory circuits in the insect antennal lobe: I. Simulations of spiking local interneurons. BioSystems, 61, 143–153.Google Scholar
  7. Dougherty, D. P., Wright, G. A., & Yew, A. C. (2005). Computational model of the cAMP-mediated sensory response and calcium-dependent adaptation in vertebrate olfactory receptor neurons. Proceedings of the National Academy of Sciences of the United States of America, 102, 10415–10420. doi:10.1073/pnas.0504099102.CrossRefPubMedGoogle Scholar
  8. Duchamp, A., & Sicard, G. (1984). Influence of stimulus intensity on odour discrimination by olfactory bulb neurons as compared with receptor cells. Chemical Senses, 8, 355–366. doi:10.1093/chemse/8.4.355.CrossRefGoogle Scholar
  9. Duchamp, A., Revial, M. F., Holley, A., & MacLeod, P. (1974). Odor discrimination by frog olfactory receptors. Chemical Senses, 1, 213–233. doi:10.1093/chemse/1.2.213.CrossRefGoogle Scholar
  10. Duchamp-Viret, P., Duchamp, A., & Chaput, M. A. (2003). Single olfactory receptor neurons simultaneously integrate the components of an odour mixture. The European Journal of Neuroscience, 18, 2690–2696. doi:10.1111/j.1460-9568.2003.03001.x.CrossRefPubMedGoogle Scholar
  11. Friedrich, R. W., & Laurent, G. (2004). Dynamics of olfactory bulb input and output activity during odor stimulation in zebrafish. Journal of Neurophysiology, 91, 2658–2669. doi:10.1152/jn.01143.2003.CrossRefPubMedGoogle Scholar
  12. Grosmaître, X., Vassalli, A., Mombaerts, P., Shepherd, G. M., & Ma, M. (2006). Odorant responses of olfactory sensory neurons expressing the odorant receptor MOR23: a patch clamp analysis in gene-targeted mice. Proceedings of the National Academy of Sciences of the United States of America, 103, 1970–1975. doi:10.1073/pnas.0508491103.CrossRefPubMedGoogle Scholar
  13. Hahn, I., Scherer, P. W., & Mozell, M. M. (1994). A mass transport model of olfaction. Journal of Theoretical Biology, 167, 115–128. doi:10.1006/jtbi.1994.1057.CrossRefPubMedGoogle Scholar
  14. Hildebrand, J. G., & Shepherd, G. M. (1997). Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annual Review of Neuroscience, 20, 595–631. doi:10.1146/annurev.neuro.20.1.595.CrossRefPubMedGoogle Scholar
  15. Imanaka, Y., & Takeuchi, H. (2001). Spiking properties of olfactory receptor cells in the slice preparation. Chemical Senses, 26, 1023–1027.Google Scholar
  16. Johnson, B. A., & Leon, M. (2007). Chemotopic odorant coding in a mammalian olfactory system. The Journal of Comparative Neurology, 503, 1–34. doi:10.1002/cne.21396.CrossRefPubMedGoogle Scholar
  17. Kaissling, K.-E. (2001). Olfactory perireceptor and receptor events in moths: a kinetic model. Chemical Senses, 26, 125–150. doi:10.1093/chemse/26.2.125.CrossRefPubMedGoogle Scholar
  18. Kostal, L., Lánský, P., & Rospars, J. P. (2008). Efficient olfactory coding in the pheromone receptor neuron of a moth. PLoS Computational Biology, 4(4), e1000053. doi:10.1371/journal.pcbi.1000053.CrossRefPubMedGoogle Scholar
  19. Laurent, G. (2002). Olfactory network dynamics and the coding of multidimensional signals. Nature Reviews. Neuroscience, 3, 884–895. doi:10.1038/nrn964.CrossRefPubMedGoogle Scholar
  20. Lewcock, J. W., & Reed, R. R. (2004). A feedback mechanism regulates monoallelic odorant receptor expression. Proceedings of the National Academy of Sciences of the United States of America, 101, 1069–1074. doi:10.1073/pnas.0307986100.CrossRefPubMedGoogle Scholar
  21. Martinez, D. (2005). Oscillatory synchronization requires precise and balanced feedback inhibition in a model of the insect antennal lobe. Neural Computation, 17, 2548–2570.Google Scholar
  22. Mombaerts, P. (2004). Odorant receptor gene choice in olfactory sensory neurons: the one receptor - one neuron hypothesis revisited. Current Opinion in Neurobiology, 14, 31–36. doi:10.1016/j.conb.2004.01.014.CrossRefPubMedGoogle Scholar
  23. Mombaerts, P., Wang, F., Dulac, C., Chao, S. K., Nemes, A., Mendelsohn, M., et al. (1996). Visualizing an olfactory sensory map. Cell, 87, 675–686. doi:10.1016/S0092-8674(00)81387-2.CrossRefPubMedGoogle Scholar
  24. Pongracz, F., Firestein, S., & Shepherd, G. M. (1991). Electrotonic structure of olfactory sensory neurons analyzed by intracellular and whole cell patch techniques. Journal of Neurophysiology, 65, 747–758.PubMedGoogle Scholar
  25. Rospars, J.-P., & Fort, J. C. (1994). Coding of odor quality: roles of convergence and inhibition. Network. Computation in Neural Systems, 5, 121–145. doi:10.1088/0954-898X/5/2/001.CrossRefGoogle Scholar
  26. Rospars, J.-P., & Lánský, P. (2004). Stochastic pulse stimulation in chemoreceptors and its properties. Mathematical Biosciences, 188, 133–145. doi:10.1016/j.mbs.2003.08.001.CrossRefPubMedGoogle Scholar
  27. Rospars, J.-P., Lánský, P., Tuckwell, H. C., & Vermeulen, A. (1996). Coding of odor intensity in a steady-state deterministic model of an olfactory receptor neuron. Journal of Computational Neuroscience, 3, 51–72. doi:10.1007/BF00158337.CrossRefPubMedGoogle Scholar
  28. Rospars, J.-P., Lánský, P., Duchamp, A., & Duchamp-Viret, P. (2003). Relation between stimulus and response in frog olfactory receptor neurons in vivo. The European Journal of Neuroscience, 18, 1135–1154. doi:10.1046/j.1460-9568.2003.02766.x.CrossRefPubMedGoogle Scholar
  29. Rospars, J.-P., Lucas, P., & Coppey, M. (2007). Modelling the early steps of transduction in insect olfactory receptor neurons. Bio Systems, 89, 101–109. doi:10.1016/j.biosystems.2006.05.015.PubMedGoogle Scholar
  30. Rospars, J.-P., Lánský, P., Duchamp, A., & Duchamp-Viret, P. (2008). Competitive and noncompetitive odorant interactions in the early neural coding of odorant mixtures. The Journal of Neuroscience, 28, 2659–2666. doi:10.1523/JNEUROSCI.4670-07.2008.CrossRefPubMedGoogle Scholar
  31. Saltelli, A. (2004). Sensitivity analysis in practice: a guide to assessing scientific models. Wiley.Google Scholar
  32. Schaefer, A. T., & Margrie, T. W. (2007). Spatiotemporal representations in the olfactory system. Trends in Neurosciences, 30, 92–100. doi:10.1016/j.tins.2007.01.001.CrossRefPubMedGoogle Scholar
  33. Serizawa, S., Miyamichi, K., Nakatani, H., Suzuki, M., Saito, M., Yoshihara, Y., et al. (2003). Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science, 302, 2088–2094. doi:10.1126/science.1089122.CrossRefPubMedGoogle Scholar
  34. Shykind, B. M. (2005). Regulation of odorant receptors: one allele at a time. Human Molecular Genetics, 14, R33–R39. doi:10.1093/hmg/ddi105.CrossRefPubMedGoogle Scholar
  35. Simoes de Souza, F. M., & Antunes, G. (2007). Biophysics of olfaction. Reports on Progress in Physics, 70, 451–491. doi:10.1088/0034-4885/70/3/R04.CrossRefGoogle Scholar
  36. Strausfeld, N. J., & Hildebrand, J. G. (1999). Olfactory systems: common design, uncommon origins? Current Opinion in Neurobiology, 9, 634–639. doi:10.1016/S0959-4388(99)00019-7.CrossRefPubMedGoogle Scholar
  37. Suzuki, N., Takahata, M., & Sato, K. (2002). Oscillatory current responses of olfactory receptor neurons to odorants and computer simulation based on a cyclic AMP transduction model. Chemical Senses, 27, 789–801. doi:10.1093/chemse/27.9.789.CrossRefPubMedGoogle Scholar
  38. Trotier, D. (1994). Intensity coding in olfactory receptor cells. Seminars in Cell Biology, 5, 47–54.Google Scholar
  39. Vermeulen, A., & Rospars, J.-P. (1998). Dendritic integration in olfactory sensory neurons: a steady-state analysis of how the neuron structure and neuron environment influence the coding of odor intensity. Journal of Computational Neuroscience, 5, 243–266. doi:10.1023/A:1008826827728.Google Scholar
  40. Wise, P. M., Miyazawa, T., Gallagher, M., & Preti, G. (2007). Human odor detection of homologous carboxylic acids and their binary mixtures. Chemical Senses, 32, 475–482. doi:10.1093/chemse/bjm016.CrossRefPubMedGoogle Scholar
  41. Yang, G. C., Scherer, P. W., & Mozell, M. M. (2007). Modeling inspiratory and expiratory steady-state velocity fields in the Sprague-Dawley rat nasal cavity. Chemical Senses, 32, 215–223. doi:10.1093/chemse/bjl047.CrossRefPubMedGoogle Scholar
  42. Zufall, F., & Leinders-Zufall, T. (2000). The cellular and molecular basis of odor adaptation. Chemical Senses, 25, 473–481. doi:10.1093/chemse/25.4.473.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Malin Sandström
    • 1
    • 2
    • 3
  • Anders Lansner
    • 2
    • 3
    • 4
  • Jeanette Hellgren-Kotaleski
    • 2
    • 3
  • Jean-Pierre Rospars
    • 1
    • 5
  1. 1.UMR1272 Physiologie de l’insecteINRAVersaillesFrance
  2. 2.Department of Communication and Computer Science, Computational Biology Group, KTHAlbaNova University CenterStockholmSweden
  3. 3.Stockholm Brain InstituteKarolinska InstituteStockholmSweden
  4. 4.Department of Numerical Analysis and Computer ScienceStockholm UniversityStockholmSweden
  5. 5.Unité Mathématiques et Informatique Appliquées, INRAJouy-en-JosasFrance

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