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.
Subscribe to Journal
Get full journal access for 1 year
only $4.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Moncrieff, R. W. The Chemical Senses 3rd ed. (Leonard Hill, London, 1967).
Amoore, J. E., Johnston, J. W. Jr. & Rubin, M. The stereochemical theory of odor. Sci. Am. 210, 42–49 (1964).
Beets, M. The molecular parameters of olfactory response. Pharmacol. Rev. 22, 1–34 (1970).
Polak, E. H. Multiple profile-multiple receptor site model for vertebrate olfaction. J. Theor. Biol. 40, 469–484 (1973).
Rupe, H. & von Majewski, K. I. Ueber osmophore gruppen., II. Ueber die darstellung von diazoimiden. (triazoverbindungen). Ber. Dtsch. Chem. Ges. 33, 3401–3410 (1900).
Klopping, H. L. Olfactory theories and the odors of small molecules. J. Agric. Food Chem. 19, 999–1004 (1971).
Macleod, A. J. Chemistry of odours. Symp. Zool. Soc. Lond. 45, 15–34 (1980).
Buck, L. & Axel, R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175–187 (1991).
Mombaerts, P. Molecular biology of odorant receptors in vertebrates. Annu. Rev. Neurosci. 22, 487–509 (1999).
Malnic, B., Hirono, J., Sato, T. & Buck, L. B. Combinatorial receptor codes for odors. Cell 96, 713–723 (1999).
Ressler, K. J., Sullivan, S. L. & Buck, L. B. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79, 1245–1255 (1994).
Vassar, R. et al. Topographic organization of sensory projections to the olfactory bulb. Cell 79, 981–991 (1994).
Mombaerts, P. et al. Visualizing an olfactory sensory map. Cell 87, 675–686 (1996).
Zhao, H. et al. Functional expression of a mammalian odorant receptor. Science 279, 237–242 (1998).
Krautwurst, D., Yau, K.-W. & Reed, R. R. Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell 95, 917–926 (1998).
Touhara, K. et al. Functional identification and reconstitution of an odorant receptor in single olfactory neurons. Proc. Natl. Acad. Sci. USA 96, 4040–4045 (1999).
Buck, L. B. The molecular architecture of odor and pheromone sensing in mammals. Cell 100, 611–618 (2000).
Friedrich, R. & Korsching, S. I. Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18, 737–752 (1997).
Friedrich, R. W. & Korsching, S. I. Chemotopic, combinatorial, and noncombinatorial odorant representations in the olfactory bulb revealed using a voltage-sensitive axon tracer. J. Neurosci. 18, 9977–9988 (1998).
Mori, K., Mataga, N. & Imamura, K. Differential specificities of single mitral cells in rabbit olfactory bulb for a homologous series of fatty acid odor molecules. J. Neurophysiol. 67, 786–789 (1992).
Imamura, K., Mataga, N. & Mori, K. Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. I. Aliphatic compounds. J. Neurophysiol. 68, 1986–2002 (1992).
Johnson, B. A., Woo, C. C., Hingco, E. E., Pham, K. L. & Leon, M. Multidimensional chemotopic responses to n-aliphatic acid odorants in the rat olfactory bulb. J. Comp. Neurol. 409, 529–548 (1999).
Rubin, B. D. & Katz, L. C. Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 23, 499–511 (1999).
Yoshihara, Y. et al. OCAM: A new member of the neural cell adhesion molecule family related to zone-to-zone projection of olfactory and vomeronasal axons. J. Neurosci. 17, 5830–5842 (1997).
Lide, D. R. CRC Handbook of Chemistry and Physics (CRC, Boca Raton, Florida, 1996).
Tsuboi, A. et al. Olfactory neurons expressing closely linked and homologous odorant receptor genes tend to project their axons to neighboring glomeruli on the olfactory bulb. J. Neurosci. 19, 8409–8418 (1999).
Laska, M. & Teubner, P. Olfactory discrimination ability for homologous series of aliphatic alcohols and aldehydes. Chem. Senses 24, 263–270 (1999).
Yang, X. et al. Dynamic mapping at the laminar level of odor-elicited responses in rat olfactory bulb by functional MRI. Proc. Natl. Acad. Sci. USA 92, 3371–3375 (1998).
Sharp, F. R., Kauer, J. S. & Shepherd, G. M. Local sites of activity-related glucose metabolism in rat olfactory bulb during olfactory stimulation. Brain Res. 98, 596–600 (1975).
Sharp, F. R., Kauer, J. S. & Shepherd, G. M. Laminar analysis of 2-deoxyglucose uptake in olfactory bulb and olfactory cortex of rabbit and rat. J. Neurophysiol. 40, 800–813 (1977).
Skeen, L. C. & Hall, W. C. Efferent projections of the main and accessory olfactory bulb in the tree shrew (Tupania glis). J. Comp. Neurol. 172, 1–36 (1977).
Stewart, W. B., Kauer, J. S. & Shepherd, G. M. Functional organization of rat olfactory bulb analyzed by the 2-deoxyglucose method. J. Comp. Neurol. 185, 715–734 (1979).
Jourdan, F., Duveau, A., Astic, L. & Holley, A. Spatial distribution of 2-deoxyglucose uptake in the olfactory bulb of rats stimulated with two different odors. Brain Res. 188, 139–154 (1980).
Sallaz, M. & Jourdan, F. C-fos expression and 2-deoxyglucose uptake in the olfactory bulb of odour-stimulated awake rats. Neuroreport 4, 55–58 (1993).
Guthrie, K. M., Anderson, A. J., Leon, M. & Gall, C. Odor-induced increase in c-fos mRNA expression reveal an anatomical “unit” for odor processing in olfactory bulb. Proc. Natl. Acad. Sci. USA 90, 3329–3333 (1993).
Guthrie, K. M. & Gall, C. Functional mapping of odor-activated neurons in the olfactory bulb. Chem. Senses 20, 271–282 (1995).
Johnson, B. A., Woo, C. C. & Leon, M. Spatial coding of odorant features in the glomerular layer of the rat olfactory bulb. J. Comp. Neurol. 393, 457–471 (1998).
Katoh, K., Koshimoto, H., Tani, A. & Mori, K. Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. II. Aromatic compounds. J. Neurophysiol. 70, 2161–2175 (1993).
Yokoi, M., Mori, K. & Nakanishi, S. Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc. Natl. Acad. Sci. USA 92, 3371–3375 (1995).
Laurent, G. Dynamical representation of odors by oscillating and evolving neural assemblies. Trends Neurosci. 19, 489–496 (1996).
Kashiwadani, H., Sasaki, Y. F., Uchida, N. & Mori, K. Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. J. Neurophysiol. 82, 1786–1792 (1999).
Mori, K., Nagao, H. & Yoshihara, Y. The olfactory bulb: coding and processing of odor molecule information. Science 286, 711–715 (1999).
Bonhoeffer, T. & Grinvald, A. in Brain Mapping. The Method (eds. Toga, A. W. & Mazziotta, J. C.) 55–97 (Academic, San Diego, California, 1995).
Uchida, N., Honjo, Y., Johnson, K. R., Wheelock, M. J. & Takeichi, M. The catenin/cadherin adhesion system is localized in synaptic junction bordering transmitter release zones. J. Cell Biol. 135, 767–779 (1996).
We thank Z. Mainen and S. L. Macknik for comments on the manuscript, H. Kashiwadani and Y. F. Sasaki for help in initial experiments, M. Fukuda, M. Matsumoto and A. Ajima for technical advice and M. Takeichi for the antibody against αN-catenin. We also thank K. Takagi, A. Onuma, H. Osada and J. Ide for advice on odorants and their vapor pressures. This work was supported in part by grants from the Ministry of Education, Science, Sports and Culture in Japan, the Human Frontier Science Program (K.M.) and the Special Postdoctoral Researchers Program in RIKEN (N.U.).
About this article
Cite this article
Uchida, N., Takahashi, Y., Tanifuji, M. et al. Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nat Neurosci 3, 1035–1043 (2000). https://doi.org/10.1038/79857
BMC Biology (2021)
Zukunftsweisende Therapieansätze bei Riechstörungen: elektrische Stimulation, Stammzelltherapie und Transplantation von Riechepithel – eine Übersicht
The functional relevance of olfactory marker protein in the vertebrate olfactory system: a never-ending story
Cell and Tissue Research (2021)
Cell and Tissue Research (2021)
Scientific Reports (2019)