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Kinetic models of odor transduction implemented as artificial neural networks

Simulations of complex response properties of honeybee olfactory neurons

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Abstract

We present a formal model of olfactory transduction corresponding to the biochemical reaction cascade found in chemosensory neurons. It assumes that odorants bind to receptor proteins which, in turn, activate transducer mechanisms corresponding to second messenger-mediated processes. The model is reformulated as a mathematically equivalent artificial neural network (ANN). To enable comparison of the computational power of our model, previously suggested models of chemosensory transduction are also presented in ANN versions. In ANNs, certain biological parameters, such as rate constants and affinities, are transformed into weights that can be fitted by training with a given experimental data set. After training, these weights do not necessarily equal the real biological parameters, but represent a set of values that is sufficient to simulate an experimental set of data. We used ANNs to simulate data recorded from bee subplacodes and compare the capacity of our model with ANN versions of other models. Receptor neurons of the nonpheromonal, general odor-processing subsystem of the honeybee are broadly tuned, have overlapping response spectra, and show highly nonlinear concentration dependencies and mixture interactions, i.e., synergistic and inhibitory effects. Our full model alone has the necessary complexity to simulate these complex response characteristics. To account for the complex response characteristics of honeybee receptor neurons, we suggest that several different receptor protein types and at least two second messenger systems are necessary that may interact at various levels of the transduction cascade and may eventually have opposing effects on receptor neuron excitability.

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References

  • Ache BW (1993) Towards a common strategy for transducing olfactory information. Semin. Cell Biol 5: 55–63

    Article  Google Scholar 

  • Akers RP, Getz WM (1992) A test of identified response classes among olfactory receptor neurons in the honeybee worker. Chem Senses 17: 191–209

    Google Scholar 

  • Akers RP, Getz WM (1993) Response of olfactory receptor neurons in honeybees to odorants and their binary mixtures. J. Comp. Physiol. 173: 169–185

    Article  Google Scholar 

  • Beidler LM (1962) Taste receptor stimulation. Prog. Biophys. Chem. 12: 107–151

    Google Scholar 

  • Boekhoff I, Tareilus E, Strotmann J, Breer H (1991) Rapid activation of alternative second messenger pathways in olfactory alia from rats by different odorants. EMBOJ 9: 2453–2458

    Google Scholar 

  • Boekhoff I, Seifert E, Göggerle S, Lindemann M, Krüger B-W, Breer H (1993) Pheromone-induced second messenger signaling in insect antennae. Insect Biochem. Mol. Biol. 23: 757–762

    Article  Google Scholar 

  • Breer H, Boekhoff I (1991) Odorants of the same odor class activate different second messenger pathways. Chem Senses 16: 19–29

    Google Scholar 

  • Breer H, Boekhoff I (1992) Second messenger signalling in olfaction. Curr Opin Neurobiol 2: 439–443

    Article  PubMed  Google Scholar 

  • Breer H, Shepherd GM (1993) Implications of the NO/cGMP system for olfaction. Trends Neurosci 16: 5–9

    Article  PubMed  Google Scholar 

  • Breer H, Boekhoff I, Strotmann J, Raming K, Tareilus E (1989) Molecular elements of olfactory signal transduction in insect antennae, in: Schild D (ed). Chemosensory information processing. Springer, Berlin Heidelberg New York, 75–86

    Google Scholar 

  • Breer H, Boekhoff I, Tareilus E (1990) Rapid kinetics of second messenger formation in olfactory transduction. Nature 344: 65–68

    Article  PubMed  Google Scholar 

  • Carr WES, Derby CD (1986) Chemically stimulated feeding behavior in marine animals, the importance of chemical mixtures and the involvement of mixture interactions. J. Chem. Ecol. 12: 987–1009

    Article  Google Scholar 

  • Clapham DE (1994) Direct G-protein activation of ion channels? Annu Rev. Neurosci. 17: 441–464

    Article  PubMed  Google Scholar 

  • Dionne VE (1992) Chemosensory responses in isolated olfactory receptor neurons from Necturus maculosus. J. Gen. Physiol 99: 415–433

    Google Scholar 

  • Dionne VE (1994) Emerging complexity of odor transduction. Proc. Natl. Acad. Sci. USA 91: 6253–6254

    PubMed  Google Scholar 

  • Ennis DM (1991) Molecular mixture models based on competitive and non-competitive agonism. Chem. Senses 16: 1–17

    Google Scholar 

  • Fadool DA, Ache BW (1992) Plasma membrane inositol 1. 4. 5-triphosphate-activated channels mediate signal transduction in lobster olfactory receptor neurons. Neuron 9: 907–918

    Article  PubMed  Google Scholar 

  • Firestein S, Zufall F, Shepard GM (1991) Single odorsensitive channels in olfactory receptor neurons are also gated by cyclic nucleotides. J. Neurosci 11, 3565–3572

    PubMed  Google Scholar 

  • Fujimura K, Yokohari F, Tateda H (1991) Classification of antennal olfactory receptors of the cockroach, Periplaneta americana. L. Zool. Sci. 8: 243–255

    Google Scholar 

  • Getz WM (1991) A neural network for processing olfactory-like stimuli. Bull. Math. Biol. 53: 805–823

    Article  PubMed  Google Scholar 

  • Getz WM, Chapman RF (1987) An odor discrimination model with application to kin recognition in social insects. Int. J. Neurosci. 32: 963–978

    PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Lasareff P (1922) Untersuchungen über die Ionentheorie der Reizung. III. Mitteilung, Ionentheorie der Geschmacksreizung. Arch. Ges. Physiol. 194: 293–297

    Article  Google Scholar 

  • Lucero MT, Horrigan FT, Gilly WF (1992) Electrical responses to chemical stimulation of squid olfactory receptor cells. J. Exp. Biol 162, 231–249

    Google Scholar 

  • Michel WL, Ache BW (1992) Cyclic nucleotides mediate an odor-evoked potassium conductance in lobster olfactory receptor cells. J. Neurosci. 12, 3979–3984

    PubMed  Google Scholar 

  • Michel WL, McClintock TS, Ache BW (1991) Inhibition of lobster olfactory receptor cells by an odor activated potassium conductance. J. Neurophysiol 65, 446–453

    PubMed  Google Scholar 

  • Reed RR (1992) Signaling pathways in odorant detection. Neuron 8: 205–209

    Article  PubMed  Google Scholar 

  • Renquist Y (1919) Über den Geschmack. Scand. Arch. Physiol. 38: 97–201

    Google Scholar 

  • Riedmiller M, Braun H (1993) A direct adaptive method for faster back-propagation learning: the RProp algorithm. In: Ruspini H (eds) Proceedings of the IEEE International Conference on Neural Networks (ICNN), San Francisco, pp 586–591

  • Ronnett GV, Cho H, Hester LD, Wood SF, Snyder SH (1993) Odorants differentially enhance phosphoinositide turnover and adenylyl cylase in olfactory receptor neuronal cultures. J. Neurosci. 13: 1751–1758

    PubMed  Google Scholar 

  • Rumelhart DE, Hinton GE, Williams RJ (1986) Learning internal representations by error propagation. In: Rumelhart DE, McClelland JL (eds) Parallel distributed processing, explorations in the microstructures of cognition, Vol 1. MIT Press, Cambridge, Mass. p 318–362

    Google Scholar 

  • Schneider D, Steinbrecht RA (1968) Checklist of insect olfactory sensilla Symp. Zool. Soc. Lond. 23: 279–297

    Google Scholar 

  • Shepherd GM (1991) Computational structure of the olfactory system. In: Davis JL, Eichenbaum H (eds) Olfaction — a model system for computational neuroscience. MIT Press, Cambridge, Mass p. 3–41

    Google Scholar 

  • Shepherd GM (1994) Discrimination of molecular signals by the olfactory eceptor neuron. Neuron 13: 771–790

    Article  PubMed  Google Scholar 

  • Vareschi E (1971) Duftunterscheidung bei der Honigbiene — Einzelzell-Ableitungen und Verhaltensreaktionen. Z Vergl. Physiol 75: 143–173

    Google Scholar 

  • Vogt RG, Rybczynski R, Lerner MR (1989) The biochemistry of odorant reception and transduction. In: Schild D (ed) Chemosensory information processing, Springer, Berlin Heidelberg New York, p. 33–76

    Google Scholar 

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Malaka, R., Ragg, T. & Hammer, M. Kinetic models of odor transduction implemented as artificial neural networks. Biol. Cybern. 73, 195–207 (1995). https://doi.org/10.1007/BF00201422

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  • DOI: https://doi.org/10.1007/BF00201422

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