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

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.

[1]  Andreas T. Schaefer,et al.  Maintaining Accuracy at the Expense of Speed Stimulus Similarity Defines Odor Discrimination Time in Mice , 2004, Neuron.

[2]  R. Reed,et al.  A feedback mechanism regulates monoallelic odorant receptor expression. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[3]  A. Duchamp,et al.  ODOR DISCRIMINATION BY FROG OLFACTORY RECEPTORS , 1974 .

[4]  H. Takeuchi,et al.  Spiking properties of olfactory receptor cells in the slice preparation. , 2001, Chemical senses.

[5]  Petr Lánský,et al.  Efficient Olfactory Coding in the Pheromone Receptor Neuron of a Moth , 2008, PLoS Comput. Biol..

[6]  J. Hildebrand,et al.  Morphometric modeling of olfactory circuits in the insect antennal lobe: I. Simulations of spiking local interneurons. , 2001, Bio Systems.

[7]  Gilles Laurent,et al.  Olfactory network dynamics and the coding of multidimensional signals , 2002, Nature Reviews Neuroscience.

[8]  Gordon M Shepherd,et al.  Odorant responses of olfactory sensory neurons expressing the odorant receptor MOR23: a patch clamp analysis in gene-targeted mice. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Jean-Pierre Rospars,et al.  Dendritic Integration in Olfactory Sensory Neurons: A Steady-State Analysis of How the Neuron Structure and Neuron Environment Influence the Coding of Odor Intensity , 1998, Journal of Computational Neuroscience.

[10]  J. Rospars,et al.  Competitive and Noncompetitive Odorant Interactions in the Early Neural Coding of Odorant Mixtures , 2008, The Journal of Neuroscience.

[11]  F. Zufall,et al.  The cellular and molecular basis of odor adaptation. , 2000, Chemical senses.

[12]  B. Shykind.  Regulation of odorant receptors: one allele at a time. , 2005, Human molecular genetics.

[13]  A. Yew,et al.  Computational model of the cAMP-mediated sensory response and calcium-dependent adaptation in vertebrate olfactory receptor neurons. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Petr Lánský,et al.  Stochastic pulse stimulation in chemoreceptors and its properties. , 2004, Mathematical biosciences.

[15]  K. Kaissling,et al.  Olfactory perireceptor and receptor events in moths: a kinetic model. , 2001, Chemical senses.

[16]  M. M. Mozell,et al.  A mass transport model of olfaction. , 1994, Journal of theoretical biology.

[17]  Gilles Laurent,et al.  Dynamics of olfactory bulb input and output activity during odor stimulation in zebrafish. , 2004, Journal of neurophysiology.

[18]  J. Rospars,et al.  Relation between stimulus and response in frog olfactory receptor neurons in vivo , 2003, The European journal of neuroscience.

[19]  Masakazu Takahata,et al.  Oscillatory current responses of olfactory receptor neurons to odorants and computer simulation based on a cyclic AMP transduction model. , 2002, Chemical senses.

[20]  G. Shepherd,et al.  Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. , 1997, Annual review of neuroscience.

[21]  Troy W. Margrie,et al.  Spatiotemporal representations in the olfactory system , 2007, Trends in Neurosciences.

[22]  Gabriela Antunes,et al.  Biophysics of olfaction , 2007 .

[23]  Cori Bargmann.  Comparative chemosensation from receptors to ecology , 2006, Nature.

[24]  Thomas A. Cleland,et al.  Concentration Tuning Mediated by Spare Receptor Capacity in Olfactory Sensory Neurons: A Theoretical Study , 1999, Neural Computation.

[25]  Dominique Martinez,et al.  Oscillatory Synchronization Requires Precise and Balanced Feedback Inhibition in a Model of the Insect Antennal Lobe , 2005, Neural Computation.

[26]  G. Sicard,et al.  Influence of stimulus intensity on odour discrimination by olfactory bulb neurons as compared with receptor cells , 1984 .

[27]  Henry C. Tuckwell,et al.  Coding of odor intensity in a steady-state deterministic model of an olfactory receptor neuron , 1996, Journal of Computational Neuroscience.

[28]  Terrence J. Sejnowski,et al.  Model of Cellular and Network Mechanisms for Odor-Evoked Temporal Patterning in the Locust Antennal Lobe , 2001, Neuron.

[29]  G M Shepherd,et al.  Electrotonic structure of olfactory sensory neurons analyzed by intracellular and whole cell patch techniques. , 1991, Journal of neurophysiology.

[30]  G. Preti,et al.  Human odor detection of homologous carboxylic acids and their binary mixtures. , 2007, Chemical senses.

[31]  Stefano Tarantola,et al.  Sensitivity Analysis in Practice: A Guide to Assessing Scientific Models , 2004 .

[32]  Thomas A Cleland,et al.  Computation in the olfactory system. , 2005, Chemical senses.

[33]  P. Duchamp-Viret,et al.  Single olfactory sensory neurons simultaneously integrate the components of an odour mixture , 2003, The European journal of neuroscience.

[34]  M. M. Mozell,et al.  Modeling inspiratory and expiratory steady-state velocity fields in the Sprague-Dawley rat nasal cavity. , 2007, Chemical senses.

[35]  J. Rospars,et al.  Coding of odour quality: roles of convergence and inhibition , 1994 .

[36]  Philippe Lucas,et al.  Modelling the early steps of transduction in insect olfactory receptor neurons , 2007, Biosyst..

[37]  Kazunari Miyamichi,et al.  Negative Feedback Regulation Ensures the One Receptor-One Olfactory Neuron Rule in Mouse , 2003, Science.

[38]  John G Hildebrand,et al.  Olfactory systems: common design, uncommon origins? , 1999, Current Opinion in Neurobiology.

[39]  Richard Axel,et al.  Visualizing an Olfactory Sensory Map , 1996, Cell.

[40]  Peter Mombaerts,et al.  Odorant receptor gene choice in olfactory sensory neurons: the one receptor–one neuron hypothesis revisited , 2004, Current Opinion in Neurobiology.

[41]  D. Trotier,et al.  Intensity coding in olfactory receptor cells. , 1994, Seminars in cell biology.

[42]  Michael Leon,et al.  Chemotopic odorant coding in a mammalian olfactory system , 2007, The Journal of comparative neurology.