[go: up one dir, main page]
More Web Proxy on the site http://driver.im/
Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Precision and diversity in an odor map on the olfactory bulb

Nature Neuroscience volume 12, pages 210–220 (2009)Cite this article

Abstract

We explored the map of odor space created by glomeruli on the olfactory bulb of both rat and mouse. Identified glomeruli could be matched across animals by their response profile to hundreds of odors. Their layout in different individuals varied by only ∼1 glomerular spacing, corresponding to a precision of 1 part in 1,000. Across species, mouse and rat share many glomeruli with apparently identical odor tuning, arranged in a similar layout. In mapping the position of a glomerulus to its odor tuning, we found only a coarse relationship with a precision of ∼5 spacings. No chemotopic order was apparent on a finer scale and nearby glomeruli were almost as diverse in their odor sensitivity as distant ones. This local diversity of sensory tuning stands in marked distinction from other brain maps. Given the reliable placement of the glomeruli, it represents a feature, not a flaw, of the olfactory bulb.

Access through your institution
Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: SpH and intrinsic signal report the same odor dependence.
Figure 2: Glomeruli can be tagged by their odor responses.
Figure 3: A genetically labeled glomerulus validates the tagging procedure.
Figure 4: Mouse and rat glomeruli are positioned precisely.
Figure 5: Prototype layout of glomeruli in mouse and rat.
Figure 6: A coarse map relates the location of a glomerulus to its odor spectrum.
Figure 7: Local diversity in the map of glomeruli.
Figure 8: Lack of local chemotopy.

Similar content being viewed by others

References

  1. Kaas, J.H. Topographic maps are fundamental to sensory processing. Brain Res. Bull. 44, 107–112 (1997).

    Article  CAS  Google Scholar 

  2. Knudsen, E.I., du Lac, S. & Esterly, S.D. Computational maps in the brain. Annu. Rev. Neurosci. 10, 41–65 (1987).

    Article  CAS  Google Scholar 

  3. Chklovskii, D.B. & Koulakov, A.A. Maps in the brain: what can we learn from them? Annu. Rev. Neurosci. 27, 369–392 (2004).

    Article  CAS  Google Scholar 

  4. Serizawa, S., Miyamichi, K. & Sakano, H. One neuron–one receptor rule in the mouse olfactory system. Trends Genet. 20, 648–653 (2004).

    Article  CAS  Google Scholar 

  5. Mombaerts, P. Molecular biology of odorant receptors in vertebrates. Annu. Rev. Neurosci. 22, 487–509 (1999).

    Article  CAS  Google Scholar 

  6. Imai, T. & Sakano, H. Roles of odorant receptors in projecting axons in the mouse olfactory system. Curr. Opin. Neurobiol. 17, 507–515 (2007).

    Article  CAS  Google Scholar 

  7. Mombaerts, P. Axonal wiring in the mouse olfactory system. Annu. Rev. Cell Dev. Biol. 22, 713–737 (2006).

    Article  CAS  Google Scholar 

  8. 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).

    Article  CAS  Google Scholar 

  9. Belluscio, L. & Katz, L.C. Symmetry, stereotypy, and topography of odorant representations in mouse olfactory bulbs. J. Neurosci. 21, 2113–2122 (2001).

    Article  CAS  Google Scholar 

  10. Meister, M. & Bonhoeffer, T. Tuning and topography in an odor map on the rat olfactory bulb. J. Neurosci. 21, 1351–1360 (2001).

    Article  CAS  Google Scholar 

  11. Oka, Y. et al. Odorant receptor map in the mouse olfactory bulb: in vivo sensitivity and specificity of receptor-defined glomeruli. Neuron 52, 857–869 (2006).

    Article  CAS  Google Scholar 

  12. Schaefer, M.L., Finger, T.E. & Restrepo, D. Variability of position of the P2 glomerulus within a map of the mouse olfactory bulb. J. Comp. Neurol. 436, 351–362 (2001).

    Article  CAS  Google Scholar 

  13. Strotmann, J. et al. Local permutations in the glomerular array of the mouse olfactory bulb. J. Neurosci. 20, 6927–6938 (2000).

    Article  CAS  Google Scholar 

  14. Wachowiak, M. & Cohen, L.B. Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 32, 723–735 (2001).

    Article  CAS  Google Scholar 

  15. 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).

    Article  CAS  Google Scholar 

  16. Johnson, B.A. et al. Functional mapping of the rat olfactory bulb using diverse odorants reveals modular responses to functional groups and hydrocarbon structural features. J. Comp. Neurol. 449, 180–194 (2002).

    Article  Google Scholar 

  17. Johnson, B.A. & Leon, M. Chemotopic odorant coding in a mammalian olfactory system. J. Comp. Neurol. 503, 1–34 (2007).

    Article  CAS  Google Scholar 

  18. Friedrich, R.W. & Korsching, S.I. Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18, 737–752 (1997).

    Article  CAS  Google Scholar 

  19. Uchida, N., Takahashi, Y.K., Tanifuji, M. & Mori, K. Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nat. Neurosci. 3, 1035–1043 (2000).

    Article  CAS  Google Scholar 

  20. Mori, K., Takahashi, Y.K., Igarashi, K.M. & Yamaguchi, M. Maps of odorant molecular features in the mammalian olfactory bulb. Physiol. Rev. 86, 409–433 (2006).

    Article  CAS  Google Scholar 

  21. Potter, S.M. et al. Structure and emergence of specific olfactory glomeruli in the mouse. J. Neurosci. 21, 9713–9723 (2001).

    Article  CAS  Google Scholar 

  22. Zhang, X., Zhang, X. & Firestein, S. Comparative genomics of odorant and pheromone receptor genes in rodents. Genomics 89, 441–450 (2007).

    Article  CAS  Google Scholar 

  23. Takahashi, Y.K., Kurosaki, M., Hirono, S. & Mori, K. Topographic representation of odorant molecular features in the rat olfactory bulb. J. Neurophysiol. 92, 2413–2427 (2004).

    Article  CAS  Google Scholar 

  24. Mori, K. & Shepherd, G.M. Emerging principles of molecular signal processing by mitral/tufted cells in the olfactory bulb. Semin. Cell Biol. 5, 65–74 (1994).

    Article  CAS  Google Scholar 

  25. 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).

    Article  CAS  Google Scholar 

  26. Duchamp, A., Revial, M.F., Holley, A. & MacLeod, P. Odor discrimination by frog olfactory receptors. Chem. Senses 1, 213–233 (1974).

    Article  CAS  Google Scholar 

  27. Malnic, B., Hirono, J., Sato, T. & Buck, L.B. Combinatorial receptor codes for odors. Cell 96, 713–723 (1999).

    Article  CAS  Google Scholar 

  28. Sicard, G. & Holley, A. Receptor cell responses to odorants: similarities and differences among odorants. Brain Res. 292, 283–296 (1984).

    Article  CAS  Google Scholar 

  29. Rubin, B.D. & Katz, L.C. Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 23, 499–511 (1999).

    Article  CAS  Google Scholar 

  30. Shepherd, G.M. & Greer, C.A. Olfactory bulb. in The Synaptic Organization of the Brain (ed. Shepherd, G.M.) 165–216 (Oxford University Press, Oxford, 2004).

    Chapter  Google Scholar 

  31. Wachowiak, M. & Shipley, M.T. Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin. Cell Dev. Biol. 17, 411–423 (2006).

    Article  Google Scholar 

  32. Egger, V. & Urban, N.N. Dynamic connectivity in the mitral cell–granule cell microcircuit. Semin. Cell Dev. Biol. 17, 424–432 (2006).

    Article  Google Scholar 

  33. Pimentel, D.O. & Margrie, T.W. Glutamatergic transmission and plasticity between olfactory bulb mitral cells. J. Physiol. (Lond.) 586, 2107–2119 (2008).

    Article  CAS  Google Scholar 

  34. Luo, M. & Katz, L.C. Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32, 1165–1179 (2001).

    Article  CAS  Google Scholar 

  35. Cleland, T.A., Johnson, B.A., Leon, M. & Linster, C. Relational representation in the olfactory system. Proc. Natl. Acad. Sci. USA 104, 1953–1958 (2007).

    Article  CAS  Google Scholar 

  36. Egana, J.I., Aylwin, M.L. & Maldonado, P.E. Odor response properties of neighboring mitral/tufted cells in the rat olfactory bulb. Neuroscience 134, 1069–1080 (2005).

    Article  CAS  Google Scholar 

  37. Buonviso, N. & Chaput, M.A. Response similarity to odors in olfactory bulb output cells presumed to be connected to the same glomerulus: electrophysiological study using simultaneous single-unit recordings. J. Neurophysiol. 63, 447–454 (1990).

    Article  CAS  Google Scholar 

  38. Willhite, D.C. et al. Viral tracing identifies distributed columnar organization in the olfactory bulb. Proc. Natl. Acad. Sci. USA 103, 12592–12597 (2006).

    Article  CAS  Google Scholar 

  39. Fantana, A.L., Soucy, E.R. & Meister, M. Rat olfactory bulb mitral cells receive sparse glomerular inputs. Neuron 59, 802–814 (2008).

    Article  CAS  Google Scholar 

  40. Bozza, T., McGann, J.P., Mombaerts, P. & Wachowiak, M. In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron 42, 9–21 (2004).

    Article  CAS  Google Scholar 

  41. Albeanu, D.F., Soucy, E., Sato, T.F., Meister, M. & Murthy, V.N. LED arrays as cost effective and efficient light sources for widefield microscopy. PLoS ONE 3, e2146 (2008).

    Article  Google Scholar 

  42. Miesenböck, G., De Angelis, D.A. & Rothman, J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192–195 (1998).

    Article  Google Scholar 

  43. Gurden, H., Uchida, N. & Mainen, Z.F. Sensory-evoked intrinsic optical signals in the olfactory bulb are coupled to glutamate release and uptake. Neuron 52, 335–345 (2006).

    Article  CAS  Google Scholar 

  44. Wachowiak, M. & Cohen, L.B. Correspondence between odorant-evoked patterns of receptor neuron input and intrinsic optical signals in the mouse olfactory bulb. J. Neurophysiol. 89, 1623–1639 (2003).

    Article  Google Scholar 

Download references

Acknowledgements

We thank P. Mombaerts for providing M72-EGFP mice and R. Wilson and N. Uchida for healthy critiques.

Author information

Author notes

  1. Edward R Soucy and Dinu F Albeanu: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Molecular and Cellular Biology and Center for Brain Science, Harvard University, 52 Oxford Street, Cambridge, 02138, Massachusetts, USA

    Edward R Soucy, Dinu F Albeanu, Antoniu L Fantana, Venkatesh N Murthy & Markus Meister

Authors
  1. Edward R Soucy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dinu F Albeanu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antoniu L Fantana
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Venkatesh N Murthy
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Markus Meister
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

E.R.S., D.F.A., V.N.M. and M.M. designed the study, E.R.S., D.F.A. and A.L.F. performed experiments and analysis, E.R.S., D.F.A. and M.M. wrote the manuscript, and V.N.M. and M.M. supervised the project.

Corresponding authors

Correspondence to Venkatesh N Murthy or Markus Meister.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–7, Supplementary Tables 1 and 2 and Supplementary Methods (PDF 9253 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Soucy, E., Albeanu, D., Fantana, A. et al. Precision and diversity in an odor map on the olfactory bulb. Nat Neurosci 12, 210–220 (2009). https://doi.org/10.1038/nn.2262

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2262

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing