Olfactory coding with all-or-nothing glomeruli.

We present a model for olfactory coding based on spatial representation of glomerular responses. In this model distinct odorants activate specific subsets of glomeruli, dependent on the odorant's chemical identity and concentration. The glomerular response specificities are understood statistically, based on experimentally measured distributions of activation thresholds. A simple version of the model, in which glomerular responses are binary (the all-or-nothing model), allows us to account quantitatively for the following results of human/rodent olfactory psychophysics: 1) just noticeable differences in the perceived concentration of a single odor (Weber ratios) are as low as dC/C approximately 0.04; 2) the number of simultaneously perceived odors can be as high as 12; and 3) extensive lesions of the olfactory bulb do not lead to significant changes in detection or discrimination thresholds. We conclude that a combinatorial code based on a binary glomerular response is sufficient to account for several important features of the discrimination capacity of the mammalian olfactory system.

[1]  Willard Van Orman Quine,et al.  Methods of Logic , 1951 .

[2]  E. Adrian,et al.  Sensory messages and sensation; the response of the olfactory organ to different smells. , 1953, Acta physiologica Scandinavica.

[3]  G. Wasserburg,et al.  Olfactory Discrimination in the Rabbit Olfactory Glomerulus , 1966, Science.

[4]  John S. Kauer,et al.  Local sites of activity-related glucose metabolism in rat olfactory bulb during olfactory stimulation , 1975, Brain Research.

[5]  W S Cain Differential sensitivity for smell: "noise" at the nose. , 1977, Science.

[6]  G. Shepherd,et al.  Functional organization of rat olfactory bulb analysed by the 2‐deoxyglucose method , 1979, The Journal of comparative neurology.

[7]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[8]  D. Lancet,et al.  Concentration-dependent changes of perceived odor quality , 1988 .

[9]  M. Devos Standardized human olfactory thresholds , 1990 .

[10]  John S. Kauer,et al.  Contributions of topography and parallel processing to odor coding in the vertebrate olfactory pathway , 1991, Trends in Neurosciences.

[11]  C. Gall,et al.  Odor-induced increases in c-fos mRNA expression reveal an anatomical "unit" for odor processing in olfactory bulb. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[12]  A. Menini,et al.  The relation between stimulus and response in olfactory receptor cells of the tiger salamander. , 1993, The Journal of physiology.

[13]  D. Leopold Olfaction , 1993 .

[14]  Gordon M. Shepherd,et al.  Discrimination of molecular signals by the olfactory receptor neuron , 1994, Neuron.

[15]  W S Cain,et al.  Comparison of models of odor interaction. , 1995, Chemical senses.

[16]  G. Beauchamp,et al.  Tasting and smelling , 1997 .

[17]  R. Friedrich,et al.  Combinatorial and Chemotopic Odorant Coding in the Zebrafish Olfactory Bulb Visualized by Optical Imaging , 1997, Neuron.

[18]  Michael Leon,et al.  Spatial coding of odorant features in the glomerular layer of the rat olfactory bulb , 1998 .

[19]  D. G. Laing,et al.  A Limit in the Processing of Components in Odour Mixtures , 1999, Perception.

[20]  L. Buck,et al.  Combinatorial Receptor Codes for Odors , 1999, Cell.

[21]  J J Hopfield,et al.  Odor space and olfactory processing: collective algorithms and neural implementation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[22]  L. C. Katz,et al.  Optical Imaging of Odorant Representations in the Mammalian Olfactory Bulb , 1999, Neuron.

[23]  William S Cain,et al.  Chemosensory Detectability of 1-Butanol and 2-Heptanone Singly and in Binary Mixtures , 1999, Physiology & Behavior.

[24]  P Duchamp-Viret,et al.  Peripheral Odor Coding in the Rat and Frog: Quality and Intensity Specification , 2000, The Journal of Neuroscience.

[25]  Naoshige Uchida,et al.  Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features , 2000, Nature Neuroscience.

[26]  J. Eberwine,et al.  Expression of mRNAs Encoding for Two Different Olfactory Receptors in a Subset of Olfactory Receptor Neurons , 2000, Journal of neurochemistry.

[27]  R G Shulman,et al.  Assessment and discrimination of odor stimuli in rat olfactory bulb by dynamic functional MRI. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[28]  D. G. Laing,et al.  The analysis of odor mixtures by humans: evidence for a configurational process , 2001, Physiology & Behavior.

[29]  T. Bonhoeffer,et al.  Tuning and Topography in an Odor Map on the Rat Olfactory Bulb , 2001, The Journal of Neuroscience.

[30]  Gustavo Glusman,et al.  The complete human olfactory subgenome. , 2001, Genome research.

[31]  L. Cohen,et al.  Representation of Odorants by Receptor Neuron Input to the Mouse Olfactory Bulb , 2001, Neuron.

[32]  Richard L. Doty,et al.  Psychophysical Measurement of Human Olfactory Function, Including Odorant Mixture Assessment , 2003 .

[33]  B. Slotnick,et al.  Detection and discrimination of carvone enantiomers in rats with olfactory bulb lesions , 2003, Neuroscience.

[34]  B. Slotnick,et al.  Olfactory discrimination of short chain fatty acids in rats with large bilateral lesions of the olfactory bulbs. , 2003, Chemical senses.

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

[36]  Carlos D. Brody,et al.  Simple Networks for Spike-Timing-Based Computation, with Application to Olfactory Processing , 2003, Neuron.

[37]  M. Kendal-Reed,et al.  Human odor detectability: new methodology used to determine threshold and variation. , 2003, Chemical senses.

[38]  Stuart Firestein,et al.  A Code in the Nose , 2004, Science's STKE.

[39]  M. Laska,et al.  Discriminating parts from the whole: determinants of odor mixture perception in squirrel monkeys, Saimiri sciureus , 1993, Journal of Comparative Physiology A.

[40]  Ivan Rodriguez,et al.  Odorant and vomeronasal receptor genes in two mouse genome assemblies. , 2004, Genomics.

[41]  Doron Lancet,et al.  Prediction of the odorant binding site of olfactory receptor proteins by human–mouse comparisons , 2004, Protein science : a publication of the Protein Society.

[42]  Peter Mombaerts,et al.  Genes and ligands for odorant, vomeronasal and taste receptors , 2004, Nature Reviews Neuroscience.

[43]  Andreas Keller,et al.  Human olfactory psychophysics , 2004, Current Biology.

[44]  G. Laurent,et al.  Multiplexing using synchrony in the zebrafish olfactory bulb , 2004, Nature Neuroscience.

[45]  Gordon M Shepherd,et al.  The olfactory glomerulus: A cortical module with specific functions , 2005, Journal of neurocytology.

[46]  Michael T Shipley,et al.  Olfactory Bulb External Tufted Cells Are Synchronized by Multiple Intraglomerular Mechanisms , 2005, The Journal of Neuroscience.

[47]  R. Axel Scents and Sensibility: A Molecular Logic of Olfactory Perception (Nobel Lecture) , 2005 .

[48]  Linda B Buck,et al.  Unraveling the sense of smell (Nobel lecture). , 2005, Angewandte Chemie.

[49]  N. Schoppa,et al.  Synchronization of Olfactory Bulb Mitral Cells by Precisely Timed Inhibitory Inputs , 2006, Neuron.

[50]  Noam Sobel,et al.  The sniff is part of the olfactory percept. , 2006, Chemical senses.

[51]  Kei M. Igarashi,et al.  Maps of odorant molecular features in the Mammalian olfactory bulb. , 2006, Physiological reviews.

[52]  T. Hummel,et al.  Electro-olfactograms are present when odorous stimuli have not been perceived , 2006, Neuroscience Letters.

[53]  Z. Mainen,et al.  Early events in olfactory processing. , 2006, Annual review of neuroscience.

[54]  Michael T Shipley,et al.  Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. , 2006, Seminars in cell & developmental biology.

[55]  Nicolas Fourcaud-Trocmé,et al.  Correlation-induced Synchronization of Oscillations in Olfactory Bulb Neurons , 2022 .

[56]  Brice Bathellier,et al.  Circuit properties generating gamma oscillations in a network model of the olfactory bulb. , 2006, Journal of neurophysiology.

[57]  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.

[58]  Noam Sobel,et al.  A comparison of methods for sniff measurement concurrent with olfactory tasks in humans. , 2006, Chemical senses.

[59]  Doron Lancet,et al.  A probabilistic classifier for olfactory receptor pseudogenes , 2006, BMC Bioinformatics.

[60]  A. Menini,et al.  Ligand specificity of odorant receptors , 2007, Journal of molecular modeling.

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

[62]  Holly F. Goyert,et al.  Characteristic component odors emerge from mixtures after selective adaptation , 2007, Brain Research Bulletin.

[63]  J. White,et al.  Sniffing controls an adaptive filter of sensory input to the olfactory bulb , 2007, Nature Neuroscience.