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Transformation of odor representations in target areas of the olfactory bulb


The brain generates coherent perceptions of objects from elementary sensory inputs. To examine how higher-order representations of smells arise from the activation of discrete combinations of glomeruli, we analyzed transformations of activity patterns between the zebrafish olfactory bulb and two of its telencephalic targets, Vv and Dp. Vv is subpallial whereas Dp is the homolog of olfactory cortex. Both areas lack an obvious topographic organization but perform complementary computations. Responses to different odors and their mixtures indicate that Vv neurons pool convergent inputs, resulting in broadened tuning curves and overlapping odor representations. Neuronal circuits in Dp, in contrast, produce a mixture of excitatory and inhibitory synaptic inputs to each neuron that controls action potential firing in an odor-dependent manner. This mechanism can extract information about combinations of molecular features from ensembles of active and inactive mitral cells, suggesting that pattern processing in Dp establishes representations of odor objects.

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Figure 1: Odor responses in target areas of the olfactory bulb.
Figure 2: Three-dimensional activity patterns across mitral cells and interneurons (INs) in the olfactory bulb.
Figure 3: Three-dimensional activity patterns in Vv and Dp.
Figure 4: Topological organization and response properties of neurons in different brain areas.
Figure 5: Mixture interactions.
Figure 6: Inhibitory control of action potential initiation in Dp neurons.


  1. 1

    Van Essen, D.C. & Gallant, J.L. Neural mechanisms of form and motion processing in the primate visual system. Neuron 13, 1–10 (1994).

    CAS  Article  Google Scholar 

  2. 2

    Buck, L. & Axel, R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175–187 (1991).

    CAS  Article  Google Scholar 

  3. 3

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

    CAS  Article  Google Scholar 

  4. 4

    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).

    CAS  Article  Google Scholar 

  5. 5

    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).

    CAS  Article  Google Scholar 

  6. 6

    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).

    CAS  Article  Google Scholar 

  7. 7

    Xu, F. et al. Odor maps of aldehydes and esters revealed by functional MRI in the glomerular layer of the mouse olfactory bulb. Proc. Natl. Acad. Sci. USA 100, 11029–11034 (2003).

    CAS  Article  Google Scholar 

  8. 8

    Xu, F., Greer, C.A. & Shepherd, G.M. Odor maps in the olfactory bulb. J. Comp. Neurol. 422, 489–495 (2000).

    CAS  Article  Google Scholar 

  9. 9

    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).

    CAS  Article  Google Scholar 

  10. 10

    Igarashi, K.M. & Mori, K. Spatial representation of hydrocarbon odorants in the ventrolateral zones of the rat olfactory bulb. J. Neurophysiol. 93, 1007–1019 (2005).

    CAS  Article  Google Scholar 

  11. 11

    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).

    CAS  Article  Google Scholar 

  12. 12

    Finger, T.E. The distribution of the olfactory tracts in the bullhead catfish, Ictalurus nebulosus. J. Comp. Neurol. 161, 125–141 (1975).

    CAS  Article  Google Scholar 

  13. 13

    von Bartheld, C.S., Meyer, D.L., Fiebig, E. & Ebbesson, S.O. Central connections of the olfactory bulb in the goldfish, Carassius auratus. Cell Tissue Res. 238, 475–487 (1984).

    CAS  Article  Google Scholar 

  14. 14

    Rink, E. & Wullimann, M.F. Connections of the ventral telencephalon (subpallium) in the zebrafish (Danio rerio). Brain Res. 1011, 206–220 (2004).

    CAS  Article  Google Scholar 

  15. 15

    Levine, R.L. & Dethier, S. The connections between the olfactory bulb and the brain in the goldfish. J. Comp. Neurol. 237, 427–444 (1985).

    CAS  Article  Google Scholar 

  16. 16

    Wong, C.J. Connections of the basal forebrain of the weakly electric fish, Eigenmannia virescens. J. Comp. Neurol. 389, 49–64 (1997).

    CAS  Article  Google Scholar 

  17. 17

    Neville, K.R. & Haberly, L.B. Olfactory cortex. in The Synaptic Organization of the Brain (ed. Shepherd, G.M.) 415–454 (Oxford University Press, Oxford, 2004).

    Chapter  Google Scholar 

  18. 18

    Wilson, D.A., Kadohisa, M. & Fletcher, M.L. Cortical contributions to olfaction: plasticity and perception. Semin. Cell Dev. Biol. 17, 462–470 (2006).

    Article  Google Scholar 

  19. 19

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

    CAS  Article  Google Scholar 

  20. 20

    Illig, K.R. & Haberly, L.B. Odor-evoked activity is spatially distributed in piriform cortex. J. Comp. Neurol. 457, 361–373 (2003).

    Article  Google Scholar 

  21. 21

    Rennaker, R.L., Chen, C.F., Ruyle, A.M., Sloan, A.M. & Wilson, D.A. Spatial and temporal distribution of odorant-evoked activity in the piriform cortex. J. Neurosci. 27, 1534–1542 (2007).

    CAS  Article  Google Scholar 

  22. 22

    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).

    CAS  Article  Google Scholar 

  23. 23

    Zou, Z. & Buck, L.B. Combinatorial effects of odorant mixes in olfactory cortex. Science 311, 1477–1481 (2006).

    CAS  Article  Google Scholar 

  24. 24

    Zou, Z., Li, F. & Buck, L.B. Odor maps in the olfactory cortex. Proc. Natl. Acad. Sci. USA 102, 7724–7729 (2005).

    CAS  Article  Google Scholar 

  25. 25

    Yan, Z. et al. Precise circuitry links bilaterally symmetric olfactory maps. Neuron 58, 613–624 (2008).

    CAS  Article  Google Scholar 

  26. 26

    Schoenfeld, T.A. & Macrides, F. Topographic organization of connections between the main olfactory bulb and pars externa of the anterior olfactory nucleus in the hamster. J. Comp. Neurol. 227, 121–135 (1984).

    CAS  Article  Google Scholar 

  27. 27

    Nikonov, A.A., Finger, T.E. & Caprio, J. Beyond the olfactory bulb: an odotopic map in the forebrain. Proc. Natl. Acad. Sci. USA 102, 18688–18693 (2005).

    CAS  Article  Google Scholar 

  28. 28

    Franks, K.M. & Isaacson, J.S. Strong single-fiber sensory inputs to olfactory cortex: implications for olfactory coding. Neuron 49, 357–363 (2006).

    CAS  Article  Google Scholar 

  29. 29

    Arenkiel, B.R. et al. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54, 205–218 (2007).

    CAS  Article  Google Scholar 

  30. 30

    Yoshida, I. & Mori, K. Odorant category profile selectivity of olfactory cortex neurons. J. Neurosci. 27, 9105–9114 (2007).

    CAS  Article  Google Scholar 

  31. 31

    Barnes, D.C., Hofacer, R.D., Zaman, A.R., Rennaker, R.L. & Wilson, D.A. Olfactory perceptual stability and discrimination. Nat. Neurosci. 11, 1378–1380 (2008).

    CAS  Article  Google Scholar 

  32. 32

    Wullimann, M.F. & Mueller, T. Teleostean and mammalian forebrains contrasted: evidence from genes to behavior. J. Comp. Neurol. 475, 143–162 (2004).

    CAS  Article  Google Scholar 

  33. 33

    Denk, W., Strickler, J.H. & Webb, W.W. Two-photon laser scanning fluorescence microscopy. Science 248, 73–76 (1990).

    CAS  Article  Google Scholar 

  34. 34

    Stosiek, C., Garaschuk, O., Holthoff, K. & Konnerth, A. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl. Acad. Sci. USA 100, 7319–7324 (2003).

    CAS  Article  Google Scholar 

  35. 35

    Yaksi, E. & Friedrich, R.W. Reconstruction of firing rate changes across neuronal populations by temporally deconvolved Ca2+ imaging. Nat. Methods 3, 377–383 (2006).

    CAS  Article  Google Scholar 

  36. 36

    Li, J. et al. Early development of functional spatial maps in the zebrafish olfactory bulb. J. Neurosci. 25, 5784–5795 (2005).

    CAS  Article  Google Scholar 

  37. 37

    Higashijima, S., Masino, M.A., Mandel, G. & Fetcho, J.R. Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator. J. Neurophysiol. 90, 3986–3997 (2003).

    Article  Google Scholar 

  38. 38

    Yaksi, E., Judkewitz, B. & Friedrich, R.W. Topological reorganization of odor representations in the olfactory bulb. PLoS Biol. 5, e178 (2007).

    Article  Google Scholar 

  39. 39

    Willmore, B. & Tolhurst, D.J. Characterizing the sparseness of neural codes. Network 12, 255–270 (2001).

    CAS  Article  Google Scholar 

  40. 40

    Tabor, R., Yaksi, E., Weislogel, J.M. & Friedrich, R.W. Processing of odor mixtures in the zebrafish olfactory bulb. J. Neurosci. 24, 6611–6620 (2004).

    CAS  Article  Google Scholar 

  41. 41

    Friedrich, R.W., Habermann, C.J. & Laurent, G. Multiplexing using synchrony in the zebrafish olfactory bulb. Nat. Neurosci. 7, 862–871 (2004).

    CAS  Article  Google Scholar 

  42. 42

    Friedrich, R.W. & Laurent, G. Dynamic optimization of odor representations in the olfactory bulb by slow temporal patterning of mitral cell activity. Science 291, 889–894 (2001).

    CAS  Article  Google Scholar 

  43. 43

    Tabor, R., Yaksi, E. & Friedrich, R.W. Multiple functions of GABA(A) and GABA(B) receptors during pattern processing in the zebrafish olfactory bulb. Eur. J. Neurosci. 28, 117–127 (2008).

    Article  Google Scholar 

  44. 44

    Hasselmo, M.E., Wilson, M.A., Anderson, B.P. & Bower, J.M. Associative memory function in piriform (olfactory) cortex: computational modeling and neuropharmacology. Cold Spring Harb. Symp. Quant. Biol. 55, 599–610 (1990).

    CAS  Article  Google Scholar 

  45. 45

    Marr, D. Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 262, 23–81 (1971).

    CAS  Article  Google Scholar 

  46. 46

    Luna, V.M. & Schoppa, N.E. GABAergic circuits control input-spike coupling in the piriform cortex. J. Neurosci. 28, 8851–8859 (2008).

    CAS  Article  Google Scholar 

  47. 47

    Perez-Orive, J. et al. Oscillations and sparsening of odor representations in the mushroom body. Science 297, 359–365 (2002).

    CAS  Article  Google Scholar 

  48. 48

    Turner, G.C., Bazhenov, M. & Laurent, G. Olfactory representations by Drosophila mushroom body neurons. J. Neurophysiol. 99, 734–746 (2008).

    Article  Google Scholar 

  49. 49

    Wachowiak, M., Denk, W. & Friedrich, R.W. Functional organization of sensory input to the olfactory bulb glomerulus analyzed by two-photon calcium imaging. Proc. Natl. Acad. Sci. USA 101, 9097–9102 (2004).

    CAS  Article  Google Scholar 

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We thank P. Caroni, T. Oertner, B. Roska and members of the Friedrich laboratory, particularly M. Wiechert, for stimulating discussions and comments on the manuscript. We are grateful to W. Denk for support. This work was supported by the Novartis Research Foundation, the Max Planck Society, the Deutsche Forschungsgemeinschaft (GK 791; SFBs 488, 780; FOR 643), the Minna-James-Heineman Foundation and the Boehringer Ingelheim Fonds (to E.Y. and S.T.B.).

Author information




E.Y. performed widefield imaging experiments, measured three-dimensional activity patterns and performed analyses of three-dimensional activity patterns and single-neuron responses; F.v.S.P. measured responses to binary mixtures, performed pharmacological experiments and electrophysiological recordings, and analyzed the data; J.N. measured responses to binary mixtures; S.T.B. participated in the construction of imaging and odor stimulation equipment and helped with experiments; R.W.F. is the principal investigator, conceived the study, constructed equipment, performed some of the binary mixture experiments, contributed to the data analysis and wrote the manuscript.

Corresponding author

Correspondence to Rainer W Friedrich.

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Yaksi, E., von Saint Paul, F., Niessing, J. et al. Transformation of odor representations in target areas of the olfactory bulb. Nat Neurosci 12, 474–482 (2009).

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