Abstract
The coding of odor intensity by an olfactory receptor neuron model was studied under steady-state stimulation. Our model neuron is an elongated cylinder consisting of the following three components: a sensory dendritic region bearing odorant receptors, a passive region consisting of proximal dendrite and cell body, and an axon. First, analytical solutions are given for the three main physiological responses: (1) odorant-dependent conductance change at the sensory dendrite based on the Michaelis-Menten model, (2) generation and spreading of the receptor potential based on a new solution of the cable equation, and (3) firing frequency based on a Lapicque model. Second, the magnitudes of these responses are analyzed as a function of odorant concentration. Their dependence on chemical, electrical, and geometrical parameters is examined. The only evident gain in magnitude results from the activation-to-conductance conversion. An optimal encoder neuron is presented that suggests that increasing the length of the sensory dendrite beyond about 0.3 space constant does not increase the magnitude of the receptor potential. Third, the sensivities of the responses are examined as functions of (1) the concentration at half-maximum response, (2) the lower and upper concentrations actually discriminated, and (3) the width of the dynamic range. The overall gain in sensitivity results entirely from the conductance-to-voltage conversion. The maximum conductance at the sensory dendrite appears to be the main tuning constant of the neuron because it determines the shift toward low concentrations and the increase in dynamic range. The dynamic range of the model cannot exceed 5.7 log units, for a sensitivity increase at low odor concentration is compensated by a sensitivity decrease at high odor concentration.
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References
Av-Ron E (1994) The role of a transient potassium current in a bursting neuron model. J. Math. Biol. 33:71–87.
Boekhoff I, Seifert E, Göggerle S, Lindemann M, Krüger B-W, Breer H (1993) Pheromone-induced second-messenger signaling in insect antennae. Insect Biochem. Molec. Biol. 23:757–762.
Breer H (1994) Odor recognition and second messenger signaling in olfactory receptor neurons. Seminars in Cell Biol. 5:25–32.
Breer H, Boekhoff I, Tareilus E (1990) Rapid kinetics of second messenger formation in olfactory transduction. Nature 345: 65–68.
Bressloff, PC (1995) Dynamics of a compartmental model integrate-and-fire neuron with somatic potential reset. Physica D 80:399–412.
De Kramer JJ (1985) The electrical circuitry of an olfactory sensillum in Antheraea polyphemus. J. Neurosci. 5:2484–2493.
De Kramer JJ, Kaissling K-E, Keil T (1984) Passive electrical properties of insect olfactory sensilla may produce the biphasic shape of spikes. Chem. Senses 8:289–295.
Duchamp-Viret P, Duchamp A, Vigouroux M (1989) Amplifying role of convergence in olfactory system: a comparative study of receptor cell and second order neuron sensitivities. J. Neurophysiol. 61:1085–1094.
Ennis DM (1991) Molecular mixture models based on competitive and non-competitive agonism. Chem. Senses 16:1–17.
Firestein S (1992) Electrical signals in olfactory transduction. Current Opinion Neurobiol. 2:444–448.
Gerstner W, van Hemmen JL (1992) Universality in neural networks: The importance of the ‘mean firing rate’. Biol. Cybern. 67:195–205.
Getchell TV, Shepherd GM (1978) Responses of olfactory receptor cells to step pulses of odour at different concentrations in the salamander. J. Physiol. Lond. 282:521–540
Getz WM, Akers RP (1995) Partitioning non-linearities in the response of honey bee olfactory receptor neurons to binary odors. BioSystems 34:27–40.
Hahn I, Scherer PW, Mozell MM (1994) A mass transport model of olfaction. J. Theor. Biol. 167:115–128.
Kaissling K-E (1969) Kinetics of olfactory receptor potentials. In: C Pfaffman, ed. Olfaction and Taste III. Rockfeller University Press, New York. pp. 52–70.
Kaissling K-E (1971) Insect olfaction. In: LM Beidler, ed. Handbook of sensory physiology. Springer-Verlag, Berlin. pp. 351–431.
Kaissling K-E (1977) Structures of odour molecules and multiple activities of receptor cells. In: J Le Magnen, P MacLeod, eds. Olfaction and Taste VI. IRL, London, pp. 9–16.
Kaissling K-E (1986) Chemo-electrical transduction in insect olfactory receptors. Ann. Rev. Neurosci. 9:121–145.
Kaissling K-E (1987) R.H. Wright lectures on insect olfaction. In: K Colbow, ed. Simon Fraser University, Canada.
Kaissling K-E (1990) Antennae and noses: their sensitivities as molecule detectors. In: Borsellino et al., eds. Sensory transduction. Plenum, New York. pp. 81–97.
Kaissling K-E (1994) Elementary receptor potentials of insect olfactory cells. In: K Kurihara, N Suzuki, H Ogawa, eds. Olfaction and Taste XI, Springer Verlag, Tokyo. pp. 812–815.
Kaissling K-E, Boeckoff I (1993) Transduction and intracellular messengers in pheromone receptor cell of the moth Antheraea polyphemus. In: K Wiese, FG Gribakin, AV Popov, G Renninger, eds. Sensory systems of arthropods. Birkhä user Verlag, Basel. pp. 489–502.
Kaissling K-E, Priesner E (1970) Die Riechschwelle des Seidenspinners. Naturwissenschaften 57:23–28.
Kaissling K-E, Thornson J (1980) Insect olfactory sensilla: Structural, chemical and electrical aspects of the functional organization. In: DB Sattelle, LM Hall, JG Hildebrand, eds. Receptors for neurotransmitters, hormones and pheromones in insects. Elsevier/North-Holland, Amsterdam, pp. 261–282.
Keil T (1984) Reconstruction and morphometry of silkmoth olfactory hairs: A comparative study of sensilla trichodea on the antennae of male Antheraea polyphemus and Antheraea pernyi (Insecta, Lepidoptera). Zoomorphology 104:147–156.
Lamb TD, Pugh EN (1992) G-protein cascades: Gain and kinetics. Trends in Neurosci. 15:291–298.
Lánský P, Rospars J-P (1993) Coding of odor intensity. BioSystems 31:15–38.
Lánský P, Rospars J-P (1995) Ornstein-Uhlenbeck neuron revisited. Biol. Cybern. 72:397–406.
Lánský P, Rospars J-P, Vermeulen A (1994) Basic mechanisms of coding stimulus intensity in the olfactory sensory neuron. Neural Processing Letters 1:9–13.
Lowe G, Gold GH (1995) Olfactory transduction is intrinsically noisy. Proc. Natl. Acad. Sci. 92:7864–7868.
Lundström KI, Karlsson JOG, Svensson SPS, Mårtensson LGE, Elwing H, Ödman S, Andersson RGG (1993) Local and non-local receptor signalling. J. Theor. Biol. 164:135–148.
Lynch JW, Barry PH (1989) Action potentials initiated by single channels opening in a small neuron (rat olfactory receptor). Biophys. J. 55:755–768.
Malaka R, Ragg T, Hammer M (1995) A model of chemosensory reception. In: G Tesawo, D Touretzky, J Alspector, eds. Advances in neural information processing systems, Vol. 7, Morgan Kaufmann, San Mateo.
Menini A, Picco C, Firestein S (1995) Quantal-like current fluctuations induced by odorants in olfactory receptor cells. Nature 373:435–437.
Nicolis G, Prigogine I (1977) Selforganization in nonequilibrium systems. Wiley, New York.
O'Connel RJ, Mozell MM (1969) Quantitative stimulation of frog olfactory receptors. J. Neurophysiol. 32:51–63.
Pongracz F, Firestein S, Shepherd GM (1991) Electrotonic structure of olfactory sensory neurons analyzed by intracellular and whole cell patch techniques. J. Neurophysiol. 65:747–758.
Rall W (1977) Core conductor theory and cable properties of neurons. In: ER Kandel, JM Brookhardt, VB Mountcastle, eds. Handbook of physiology: The nervous system, Vol. 1. Williams and Wilkins, Baltimore, pp. 39–98.
Rall W (1989) Cable theory for dendritic neurons. In: C Koch, I Segev, eds. Methods in neuronal modeling. MIT Press, Cambridge. pp. 9–62.
Rospars J-P, Lánský P (1993) Stochastic model neuron without re-setting of dendritic potential: application to the olfactory system. Biol. Cyb. 69:283–294.
Rospars J-P, Lánský P, Vaillant J, Duchamp-Viret P, Duchamp A (1994) Spontaneous activity of first- and second-order neurons in the frog olfactory system. Brain Res. 662:31–44.
Rovinsky A, Menzinger M (1993) Dynamics of analog-to-frequency transduction by excitable systems: Sensory receptors. J. Chem. Phys. 98:9155–9166.
Schwaber JS, Graves EB, Paton JFR (1993) Computational modeling of neuronal dynamics for systems analysis: application to neurons of the cardiorespiratory NTS in the rat. Brain Res. 604: 126–141.
Segev I (1992) Single neurone models: oversimple, complex and reduced. Trends in Neurosci. 15:414–421.
Segundo JP, Vibert J-F, Pakdaman K, Stiber M, Diez Martínez O (1994) Noise and the neurosciences: a long history, a recent revival and some theory. In: K Pribram, ed. Origins: brain and self-organization. Lawrence Erlbaum, Hillsdale, NJ, pp. 300–331.
Selzer R (1984) On the specificities of antennal olfactory receptor cells of Periplaneta americana. Chem. Senses 8:375–395.
Shepherd GM (1994) Discrimination of molecular signals by the olfactory receptor neuron. Neuron 13:771–790.
Shirsat N, Siddiqi O (1993) Olfaction in invertebrates. Current Opinion Neurobiol. 3:553–557.
Stengl M, Hatt H, Breer H (1992) Peripheral processes in insect olfaction. Ann. Rev. Physiol. 54:665–681.
Tateda H (1967) Sugar receptor and α-amino acid in the rat. In: T Hayashi, ed. Olfaction and Taste II, Pergamon Press. pp. 383–397.
Tuckwell HC (1988) Introduction to theoretical Neurobiology. Cambridge University Press, New York.
Tuckwell HC, Rospars J-P, Vermeulen A, Lánský P (1995) Time-dependent solutions for a cable model of an olfactory receptor neuron. Submitted.
Vareschi E (1971) Duftunterscheidung bei der Honigbiene. Einzelzell-Ableitungen und Verhaltensreaktionen. Z. Vergl. Physiol. 75:143–173.
Vermeulen A, Rospars J-P, Lánský P, Tuckwell HC (1995) Coding of stimulus intensity in an olfactory receptor neuron: role of neuron spatial extension and dendritic backpropagation of action potentials. Bull. Math. Biol. In press.
Wilson MA, Bower JM (1989) The simulation of large-scale neural networks. In: C Koch, I Segev, eds. Methods in neuronal modeling. MIT Press, Cambridge, MA. pp. 291–333.
Yamada WM, Koch C, Adams PR (1989) Multiple channels and calcium dynamics. In: C Koch, I Segev, eds. Methods in neuronal modeling. MIT Press, Cambridge, MA. pp. 97–133.
Yu X, Lewis ER (1989) Studies with spike initiators: linearizations by noise allows continuous signal modulation in neural networks. IEEE Trans. Biomed. Eng. 36:36–43.
Zufall F, Stengl M, Franke C, Hildebrand JG, Hatt H (1991) Ionic currents of cultured olfactory receptor neurons from antennae of male Manduca sexta. J. Neurosci. 11:956–965.
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Rospars, JP., Lánský, P., Tuckwell, H.C. et al. Coding of odor intensity in a steady-state deterministic model of an olfactory receptor neuron. J Comput Neurosci 3, 51–72 (1996). https://doi.org/10.1007/BF00158337
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DOI: https://doi.org/10.1007/BF00158337