Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features

Psychophysical studies indicate that structural features of odorants differentially influence their perceived odor. In the olfactory bulb (OB), odorants are represented by ensembles of activated glomeruli. Here we used optical imaging of intrinsic signals to examine how these structural features are represented spatially in the sensory map of the rat OB. We found that the dorsal OB contained two topographically fixed domains; constituent glomeruli in each domain could be activated by odorants with particular functional groups. Within each domain, other structural features such as carbon chain length and branching were represented by local differences in patterns. These results suggest that structural features are categorized into two classes, primary features (functional groups) that characterize each domain, and secondary features that are represented by local positions within each domain. Such hierarchical representations of different structural features correlate well with psychophysical structure–odor relationships.

[1]  G. Laurent Dynamical representation of odors by oscillating and evolving neural assemblies , 1996, Trends in Neurosciences.

[2]  C. Gall,et al.  Functional mapping of odor-activated neurons in the olfactory bulb. , 1995, Chemical senses.

[3]  N. Uchida,et al.  Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. , 1999, Journal of neurophysiology.

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

[5]  W. M. Haynes CRC Handbook of Chemistry and Physics , 1990 .

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

[7]  M. Laska,et al.  Olfactory discrimination ability for homologous series of aliphatic alcohols and aldehydes. , 1999, Chemical senses.

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

[9]  H. Sakano,et al.  Olfactory Neurons Expressing Closely Linked and Homologous Odorant Receptor Genes Tend to Project Their Axons to Neighboring Glomeruli on the Olfactory Bulb , 1999, The Journal of Neuroscience.

[10]  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.

[11]  H. Hayashi,et al.  OCAM: A New Member of the Neural Cell Adhesion Molecule Family Related to Zone-to-Zone Projection of Olfactory and Vomeronasal Axons , 1997, The Journal of Neuroscience.

[12]  G. M. Dyson The Chemical Senses , 1946, Nature.

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

[14]  P. Mombaerts,et al.  Molecular biology of odorant receptors in vertebrates. , 1999, Annual review of neuroscience.

[15]  F. Rawlins,et al.  The Method , 1966, Nature.

[16]  Rainer W. Friedrich,et al.  Chemotopic, Combinatorial, and Noncombinatorial Odorant Representations in the Olfactory Bulb Revealed Using a Voltage-Sensitive Axon Tracer , 1998, The Journal of Neuroscience.

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

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

[19]  J. Amoore,et al.  THE STEROCHEMICAL THEORY OF ODOR. , 1964, Scientific American.

[20]  S. Nakanishi,et al.  Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[21]  R G Shulman,et al.  Dynamic mapping at the laminar level of odor-elicited responses in rat olfactory bulb by functional MRI. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[24]  K. Imamura,et al.  Differential specificities of single mitral cells in rabbit olfactory bulb for a homologous series of fatty acid odor molecules. , 1992, Journal of neurophysiology.

[25]  F R Sharp,et al.  Laminar analysis of 2-deoxyglucose uptake in olfactory bulb and olfactory cortex of rabbit and rat. , 1977, Journal of neurophysiology.

[26]  R. Axel,et al.  A novel multigene family may encode odorant receptors: A molecular basis for odor recognition , 1991, Cell.

[27]  K. Mori,et al.  The olfactory bulb: coding and processing of odor molecule information. , 1999, Science.

[28]  J. Mazziotta,et al.  Brain Mapping: The Methods , 2002 .

[29]  M. Lings,et al.  Articles , 1967, Soil Science Society of America Journal.

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

[31]  H. Sakano,et al.  Functional identification and reconstitution of an odorant receptor in single olfactory neurons. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[32]  L. Buck,et al.  The Molecular Architecture of Odor and Pheromone Sensing in Mammals , 2000, Cell.

[33]  E. Polak Mutiple profile-multiple receptor site model for vertebrate olfaction. , 1973, Journal of theoretical biology.

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

[35]  F Jourdan,et al.  C-fos expression and 2-deoxyglucose uptake in the olfactory bulb of odour-stimulated awake rats. , 1993, Neuroreport.

[36]  L. Astic,et al.  Spatial distribution of [14C]2-deoxyglucose uptake in the olfactory bulbs of rats stimulated with two different odours , 1980, Brain Research.

[37]  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.

[38]  R. C. Weast CRC Handbook of Chemistry and Physics , 1973 .

[39]  H L Klopping,et al.  Olfactory theories and the odors of small molecules. , 1971, Journal of agricultural and food chemistry.

[40]  M. Takeichi,et al.  The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones , 1996, The Journal of cell biology.

[41]  M. Beets,et al.  The molecular parameters of olfactory response. , 1970, Pharmacological reviews.

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

[43]  W. C. Hall,et al.  Efferent projections of the main and the accessory olfactory bulb in the tree shrew (Tupaia glis) , 1977, The Journal of comparative neurology.

[44]  Dietmar Krautwurst,et al.  Identification of Ligands for Olfactory Receptors by Functional Expression of a Receptor Library , 1998, Cell.