Anatomical contributions to odorant sampling and representation in rodents: zoning in on sniffing behavior.

Odorant sampling behaviors such as sniffing bring odorant molecules into contact with olfactory receptor neurons (ORNs) to initiate the sensory mechanisms of olfaction. In rodents, inspiratory airflow through the nose is structured and laminar; consequently, the spatial distribution of adsorbed odorant molecules during inspiration is predictable. Physicochemical properties such as water solubility and volatility, collectively called sorptiveness, interact with behaviorally regulable variables such as inspiratory flow rate to determine the pattern of odorant deposition along the inspiratory path. Populations of ORNs expressing the same odorant receptor are distributed in strictly delimited regions along this inspiratory path, enabling different deposition patterns of the same odorant to evoke different patterns of neuronal activation across the olfactory epithelium and in the olfactory bulb. We propose that both odorant sorptive properties and the regulation of sniffing behavior may contribute to rodents' olfactory capacities by this mechanism. In particular, we suggest that the motor regulation of sniffing behavior is substantially utilized for purposes of "zonation" or the direction of odorant molecules to defined intranasal regions and hence toward distinct populations of receptor neurons, pursuant to animals' sensory goals.

[1]  J. D. E. Gabrieli,et al.  Sniffing and smelling: separate subsystems in the human olfactory cortex , 1998, Nature.

[2]  Gordon M Shepherd,et al.  Electrophysiological characterization of rat and mouse olfactory receptor neurons from an intact epithelial preparation , 1999, Journal of Neuroscience Methods.

[3]  Gordon M Shepherd,et al.  High-throughput microarray detection of olfactory receptor gene expression in the mouse. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Z. Mainen,et al.  Speed and accuracy of olfactory discrimination in the rat , 2003, Nature Neuroscience.

[5]  F. Macrides,et al.  Topographic organization of connections between the main olfactory bulb and pars externa of the anterior olfactory nucleus in the hamster , 1984, The Journal of comparative neurology.

[6]  R. Axel,et al.  Odorant Receptors Govern the Formation of a Precise Topographic Map , 1998, Cell.

[7]  P. Sheehe,et al.  A parametric study of the stimulation variables affecting the magnitude of the olfactory nerve response , 1984, The Journal of general physiology.

[8]  S. Firestein,et al.  The olfactory receptor gene superfamily of the mouse , 2002, Nature Neuroscience.

[9]  W. Jennings Analytical Gas Chromatography , 1987 .

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

[11]  Philippe Litaudon,et al.  Respiratory modulation of olfactory neurons in the rodent brain. , 2006, Chemical senses.

[12]  L. Astic,et al.  Analysis of the possible alerting function of the septal organ in rats: A lesional and behavioral study , 1995, Physiology & Behavior.

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

[14]  M. M. Mozell,et al.  Evidence for a Chromatographic Model of Olfaction , 1970, The Journal of general physiology.

[15]  H. Breer,et al.  Subzonal organization of olfactory sensory neurons projecting to distinct glomeruli within the mouse olfactory bulb , 2003, The Journal of comparative neurology.

[16]  M. Leon,et al.  Odorant molecular length: One aspect of the olfactory code , 2000, The Journal of comparative neurology.

[17]  N. Vickers Winging it: moth flight behavior and responses of olfactory neurons are shaped by pheromone plume dynamics. , 2006, Chemical senses.

[18]  L. Astic,et al.  Anatomical mapping of the neuroepithelial projection to the olfactory bulb in the rat , 1986, Brain Research Bulletin.

[19]  L. Buck,et al.  The mouse olfactory receptor gene family , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[20]  D. Purves,et al.  Postnatal construction of neural circuitry in the mouse olfactory bulb , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  T. Knott,et al.  NADPH diaphorase activity in olfactory receptor neurons and their axons conforms to a rhinotopically-distinct dorsal zone of the hamster nasal cavity and main olfactory bulb , 2002, Journal of Chemical Neuroanatomy.

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

[23]  F. Macrides,et al.  The spatial organization of the peripheral olfactory system of the hamster. part I: Receptor neuron projections to the main olfactory bulb , 1994, Brain Research Bulletin.

[24]  A. Berghard,et al.  Odorant‐dependent, spatially restricted induction of c‐fos in the olfactory epithelium of the mouse , 2005, Journal of neurochemistry.

[25]  W. Stewart,et al.  The spatial organization of olfactory nerve projections , 1987, Brain Research.

[26]  Shuichi Hirono,et al.  Topographic representation of odorant molecular features in the rat olfactory bulb. , 2004, Journal of neurophysiology.

[27]  K. Mori,et al.  Grouping and representation of odorant receptors in domains of the olfactory bulb sensory map , 2002, Microscopy research and technique.

[28]  Kei M. Igarashi,et al.  Odor maps in the dorsal and lateral surfaces of the rat olfactory bulb. , 2005, Chemical senses.

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

[30]  David E. Hornung,et al.  A quantitative analysis of sniffing strategies in rats performing odor detection tasks , 1987, Physiology & Behavior.

[31]  Richard Axel,et al.  Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium , 1993, Cell.

[32]  M. Ma,et al.  Molecular Organization of the Olfactory Septal Organ , 2004, The Journal of Neuroscience.

[33]  P. Dalton,et al.  Numerical modeling of turbulent and laminar airflow and odorant transport during sniffing in the human and rat nose. , 2006, Chemical senses.

[34]  N. Onoda Odor-induced fos-like immunoreactivity in the rat olfactory bulb , 1992, Neuroscience Letters.

[35]  M. Leon,et al.  Modular representations of odorants in the glomerular layer of the rat olfactory bulb and the effects of stimulus concentration , 2000, The Journal of comparative neurology.

[36]  Donald A. Wilson,et al.  The fundamental role of memory in olfactory perception , 2003, Trends in Neurosciences.

[37]  Michael Leon,et al.  Effects of functional group position on spatial representations of aliphatic odorants in the rat olfactory bulb , 2005, The Journal of comparative neurology.

[38]  J. Morris,et al.  Advances in biologically based models for respiratory tract uptake of inhaled volatiles. , 1993, Fundamental and applied toxicology : official journal of the Society of Toxicology.

[39]  M. M. Mozell,et al.  The effect of flow rate upon the magnitude of the olfactory response differs for different odorants , 1991 .

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

[41]  T. Knott,et al.  Evidence for the disproportionate mapping of olfactory airspace onto the main olfactory bulb of the hamster , 2004, The Journal of comparative neurology.

[42]  Michael Leon,et al.  Functional mapping of the rat olfactory bulb using diverse odorants reveals modular responses to functional groups and hydrocarbon structural features , 2002, The Journal of comparative neurology.

[43]  J. Lynch,et al.  Calcium-dependent Modulation of the Agonist Affinity of the Mammalian Olfactory Cyclic Nucleotide-gated Channel by Calmodulin and a Novel Endogenous Factor , 1996, The Journal of Membrane Biology.

[44]  J D Gabrieli,et al.  Sniffing longer rather than stronger to maintain olfactory detection threshold. , 2000, Chemical senses.

[45]  M. Koehl,et al.  The fluid mechanics of arthropod sniffing in turbulent odor plumes. , 2006, Chemical senses.

[46]  H. Bostock,et al.  Olfaction and taste III: Edited by Carl Pfaffmann. Rockefeller University Press, New York, 1970 , 1972 .

[47]  K. Mikoshiba,et al.  Functional expression of a mammalian odorant receptor. , 1998, Science.

[48]  M. Leon,et al.  Multidimensional chemotopic responses to n‐aliphatic acid odorants in the rat olfactory bulb , 1999, The Journal of comparative neurology.

[49]  F. Macrides,et al.  Evidence for morphologically, neurochemically and functionally heterogeneous classes of mitral and tufted cells in the olfactory bulb , 1985 .

[50]  Shin Nagayama,et al.  Molecular‐feature domains with posterodorsal–anteroventral polarity in the symmetrical sensory maps of the mouse olfactory bulb: mapping of odourant‐induced Zif268 expression , 2002, The European journal of neuroscience.

[51]  F. Macrides,et al.  The spatial organization of the peripheral olfactory system of the hamster. Part II: Receptor surfaces and odorant passageways within the nasal cavity , 1994, Brain Research Bulletin.

[52]  B. Slotnick,et al.  Detection of propionic acid vapor by rats with lesions of olfactory bulb areas associated with high 2-DG uptake , 1987, Brain Research.

[53]  Dynamic Aspects of Central Olfactory Processing , 1977 .

[54]  Linda B. Buck,et al.  A zonal organization of odorant receptor gene expression in the olfactory epithelium , 1993, Cell.

[55]  B. Slotnick,et al.  Odor Discrimination and Odor Quality Perception in Rats with Disruption of Connections between the Olfactory Epithelium and Olfactory Bulbs , 2002, The Journal of Neuroscience.

[56]  Linda B. Buck,et al.  Information coding in the olfactory system: Evidence for a stereotyped and highly organized epitope map in the olfactory bulb , 1994, Cell.

[57]  H. Breer,et al.  Olfactory receptors in aquatic and terrestrial vertebrates , 1998, Journal of Comparative Physiology A.

[58]  A. Chess,et al.  The family of genes encoding odorant receptors in the channel catfish , 1993, Cell.

[59]  H. Breer,et al.  Olfactory receptors in the mouse septal organ , 2004, Journal of neuroscience research.

[60]  Masatoshi Nei,et al.  Evolutionary dynamics of olfactory receptor genes in fishes and tetrapods , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[61]  Cynthia Friedman,et al.  Different evolutionary processes shaped the mouse and human olfactory receptor gene families. , 2002, Human molecular genetics.

[62]  D. Gilbert,et al.  The OMP–lacZ Transgene Mimics the Unusual Expression Pattern of OR-Z6, a New Odorant Receptor Gene on Mouse Chromosome 6: Implication for Locus-Dependent Gene Expression , 2001, The Journal of Neuroscience.

[63]  H. Breer,et al.  Organization and evolutionary relatedness of OR37 olfactory receptor genes in mouse and human. , 2003, Genomics.

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

[65]  Carrie L Iwema,et al.  Odorant Receptor Expression Patterns Are Restored in Lesion-Recovered Rat Olfactory Epithelium , 2004, The Journal of Neuroscience.

[66]  A. Mackay-Sim,et al.  Cell dynamics in the olfactory epithelium of the tiger salamander: a morphometric analysis , 1988, Experimental Brain Research.

[67]  D. Hornung,et al.  Experimental and numerical determination of odorant solubility in nasal and olfactory mucosa. , 2004, Chemical senses.

[68]  M. M. Mozell,et al.  Olfactory stimulation variables. Which model best predicts the olfactory nerve response? , 1985, The Journal of general physiology.

[69]  Michael Leon,et al.  Local and global chemotopic organization: General features of the glomerular representations of aliphatic odorants differing in carbon number , 2004, The Journal of comparative neurology.

[70]  J. Scott,et al.  Chemical Determinants of the Rat Electro-Olfactogram , 2000, The Journal of Neuroscience.

[71]  K T Morgan,et al.  Computer simulation of inspiratory airflow in all regions of the F344 rat nasal passages. , 1997, Toxicology and applied pharmacology.

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

[73]  Lawrence C Katz,et al.  Functional Topography of Connections Linking Mirror-Symmetric Maps in the Mouse Olfactory Bulb , 2003, Neuron.

[74]  L. Astic,et al.  Analysis of the topographical organization of olfactory epithelium projections in the rat , 1986, Brain Research Bulletin.

[75]  K. Mori,et al.  Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. II. Aromatic compounds. , 1992, Journal of neurophysiology.

[76]  Richard Axel,et al.  Topographic organization of sensory projections to the olfactory bulb , 1994, Cell.

[77]  John D. E. Gabrieli,et al.  Olfaction: The world smells different to each nostril , 1999, Nature.

[78]  Peter Mombaerts,et al.  Odorant Receptor Expression Defines Functional Units in the Mouse Olfactory System , 2002, The Journal of Neuroscience.

[79]  Adam Kepecs,et al.  The sniff as a unit of olfactory processing. , 2006, Chemical senses.

[80]  H. Breer,et al.  Olfactory neurones expressing distinct odorant receptor subtypes are spatially segregated in the nasal neuroepithelium , 1994, Cell and Tissue Research.

[81]  A. Holley,et al.  Convergence in the olfactory system: quantitative aspects of odour sensitivity. , 1978, Journal of theoretical biology.

[82]  K. Imamura,et al.  Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. I. Aliphatic compounds. , 1992, Journal of neurophysiology.

[83]  Michael Leon,et al.  Interactions between odorant functional group and hydrocarbon structure influence activity in glomerular response modules in the rat olfactory bulb , 2005, The Journal of comparative neurology.

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

[85]  David A. Kareken,et al.  Olfactory system activation from sniffing: effects in piriform and orbitofrontal cortex , 2004, NeuroImage.

[86]  M. Bensafi,et al.  Olfactomotor activity during imagery mimics that during perception , 2003, Nature Neuroscience.

[87]  A. Mackay-Sim,et al.  On the Life Span of Olfactory Receptor Neurons , 1991, The European journal of neuroscience.

[88]  Ivan Rodriguez,et al.  Axon Guidance of Mouse Olfactory Sensory Neurons by Odorant Receptors and the β2 Adrenergic Receptor , 2004, Cell.

[89]  Kei M. Igarashi,et al.  Spatial representation of hydrocarbon odorants in the ventrolateral zones of the rat olfactory bulb. , 2005, Journal of neurophysiology.

[90]  Michael Leon,et al.  Olfactory coding in the mammalian olfactory bulb , 2003, Brain Research Reviews.

[91]  E. Orona,et al.  Pattern of rat olfactory bulb mitral and tufted cell connections to the anterior olfactory nucleus pars externa , 1985, The Journal of comparative neurology.

[92]  F. Macrides,et al.  Olfactory Bulb Units: Activity Correlated with Inhalation Cycles and Odor Quality , 1972, Science.

[93]  H Breer,et al.  Local Permutations in the Glomerular Array of the Mouse Olfactory Bulb , 2000, The Journal of Neuroscience.

[94]  Sir Victor Negus Comparative Anatomy and Physiology of the Nose and Paranasal Sinuses , 1959 .

[95]  M. Mezler,et al.  Characteristic features and ligand specificity of the two olfactory receptor classes from Xenopus laevis. , 2001, The Journal of experimental biology.

[96]  Peter Mombaerts,et al.  Specificity of Glomerular Targeting by Olfactory Sensory Axons , 2002, The Journal of Neuroscience.

[97]  Lawrence C. Katz,et al.  Odorant receptors instruct functional circuitry in the mouse olfactory bulb , 2002, Nature.

[98]  M. T. Shipley,et al.  Intrabulbar associational system in the rat olfactory bulb comprises cholecystokinin‐containing tufted cells that synapse onto the dendrites of GABAergic granule cells , 1994, The Journal of comparative neurology.

[99]  M. M. Mozell,et al.  Evidence for Sorption as a Mechanism of the Olfactory Analysis of Vapours , 1964, Nature.

[100]  J. Morris,et al.  Species differences in upper respiratory tract deposition of acetone and ethanol vapors. , 1986, Fundamental and applied toxicology : official journal of the Society of Toxicology.

[101]  Lisa M. D'Souza,et al.  Genome sequence of the Brown Norway rat yields insights into mammalian evolution , 2004, Nature.

[102]  F. Müller,et al.  Phosphorylation of Mammalian Olfactory Cyclic Nucleotide-Gated Channels Increases Ligand Sensitivity , 1998, The Journal of Neuroscience.

[103]  K T Morgan,et al.  Studies of inspiratory airflow patterns in the nasal passages of the F344 rat and rhesus monkey using nasal molds: relevance to formaldehyde toxicity. , 1991, Toxicology and applied pharmacology.

[104]  Hitoshi Sakano,et al.  Continuous and Overlapping Expression Domains of Odorant Receptor Genes in the Olfactory Epithelium Determine the Dorsal/Ventral Positioning of Glomeruli in the Olfactory Bulb , 2005, The Journal of Neuroscience.

[105]  John W. Scott,et al.  Sniffing and spatiotemporal coding in olfaction. , 2006, Chemical senses.

[106]  J W Scott,et al.  Effects of air flow on rat electroolfactogram. , 2000, Chemical senses.

[107]  Thomas A. Cleland,et al.  The anatomical logic of smell , 2005, Trends in Neurosciences.

[108]  M M Mozell,et al.  The interaction of imposed and inherent olfactory mucosal activity patterns and their composite representation in a mammalian species using voltage-sensitive dyes , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[109]  M. M. Mozell,et al.  Chromatographic Separation of Odorants by the Nose: Retention Times Measured across in vivo Olfactory Mucosa , 1973, Science.

[110]  M. T. Shipley,et al.  Centre–surround inhibition among olfactory bulb glomeruli , 2003, Nature.

[111]  A. Farbman,et al.  The effect of unilateral naris occlusion on cell dynamics in the developing rat olfactory epithelium , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[112]  F. Macrides,et al.  Topographic organization of tufted cell axonal projections in the hamster main olfactory bulb: An intrabulbar associational system , 1985, The Journal of comparative neurology.

[113]  J. Maruniak,et al.  Masera's organ responds to odorants , 1986, Brain Research.

[114]  E. Meisami,et al.  A proposed relationship between increases in the number of olfactory receptor neurons, convergence ratio and sensitivity in the developing rat. , 1989, Brain research. Developmental brain research.

[115]  M. Alenius,et al.  Differential function of RNCAM isoforms in precise target selection of olfactory sensory neurons , 2003, Development.

[116]  H. Breer,et al.  A novel brain receptor is expressed in a distinct population of olfactory sensory neurons , 2000, The European journal of neuroscience.

[117]  Michael Leon,et al.  Perceptual Correlates of Neural Representations Evoked by Odorant Enantiomers , 2001, The Journal of Neuroscience.

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

[119]  J. Kauer,et al.  Odorant Response Properties of Convergent Olfactory Receptor Neurons , 1998, The Journal of Neuroscience.

[120]  P Duchamp-Viret,et al.  Amplifying role of convergence in olfactory system a comparative study of receptor cell and second-order neuron sensitivities. , 1989, Journal of neurophysiology.