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Dendritic stability in the adult olfactory bulb

Abstract

In many regions of the adult mammalian brain, pronounced changes in synaptic input caused by lesions or severe sensory deprivation induce marked sprouting or retraction of neuronal dendrites. In the adult olfactory bulb, adult neurogenesis produces less pronounced, but continuously ongoing synapse turnover. To test the structural stability of adult dendrites in this context, we used two-photon microscopy to image dendrites of mitral and tufted (M/T) cells over prolonged periods in adult mice. Although pharmacologically increased activity could elicit morphological changes, under natural conditions such as ongoing neurogenesis, an odor-enriched environment or olfactory-based learning, M/T cell dendrites remained highly stable. Thus, in a context of ongoing adult synaptogenesis, dendritic stability could serve as a structural scaffold to maintain the organization of local circuits.

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Figure 1: Two-photon imaging of M/T cells and their apical dendrites in the olfactory bulb of a YFP-G mouse.
Figure 2: Morphological analysis of M/T cell apical dendrites.
Figure 3: Dendritic stability of M/T cell apical dendrites in adult mice.
Figure 4: Dendritic stability of M/T cell apical dendrites following odor enrichment.
Figure 5: Increased activity destabilizes M/T cell apical dendrites.
Figure 6: Intrinsic signal imaging following learning of an olfactory discrimination task.
Figure 7: Dendritic stability following learning of an olfactory discrimination task.

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References

  1. Bailey, C.H. & Kandel, E.R. Structural changes accompanying memory storage. Annu. Rev. Physiol. 55, 397–426 (1993).

    Article  CAS  Google Scholar 

  2. Darian-Smith, C. & Gilbert, C.D. Axonal sprouting accompanies functional reorganization in adult cat striate cortex. Nature 368, 737–740 (1994).

    Article  CAS  Google Scholar 

  3. Nimchinsky, E.A., Sabatini, B.L. & Svoboda, K. Structure and function of dendritic spines. Annu. Rev. Physiol. 64, 313–353 (2002).

    Article  CAS  Google Scholar 

  4. Grutzendler, J., Kasthuri, N. & Gan, W.B. Long-term dendritic spine stability in the adult cortex. Nature 420, 812–816 (2002).

    Article  CAS  Google Scholar 

  5. Trachtenberg, J.T. et al. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420, 788–794 (2002).

    Article  CAS  Google Scholar 

  6. Altman, J. Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J. Comp. Neurol. 137, 433–457 (1969).

    Article  CAS  Google Scholar 

  7. Gage, F.H. Neurogenesis in the adult brain. J. Neurosci. 22, 612–613 (2002).

    Article  CAS  Google Scholar 

  8. Kasowski, H.J., Kim, H. & Greer, C.A. Compartmental organization of the olfactory bulb glomerulus. J. Comp. Neurol. 407, 261–274 (1999).

    Article  CAS  Google Scholar 

  9. Carlen,M. et al. Functional integration of adult-born neurons. Curr. Biol. 12, 606–608 (2002).

    Article  CAS  Google Scholar 

  10. Carleton, A., Petreanu, L.T., Lansford, R., Alvarez-Buylla, A. & Lledo, P.M. Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 6, 507–518 (2003).

    Article  CAS  Google Scholar 

  11. Jontes, J.D. & Smith, S.J. Filopodia, spines, and the generation of synaptic diversity. Neuron 27, 11–14 (2000).

    Article  CAS  Google Scholar 

  12. Acebes, A. & Ferrus, A. Cellular and molecular features of axon collaterals and dendrites. Trends Neurosci. 23, 557–565 (2000).

    Article  CAS  Google Scholar 

  13. Dunaevsky, A. & Mason, C.A. Spine motility: a means towrds an end? Trends Neurosci. 26, 155–160 (2003).

    Article  CAS  Google Scholar 

  14. Shepherd, G.M. & Greer, C.A. Olfactory bulb in The Synaptic Organization of the Brain (ed. Shepherd, G.M.) 159–203 (Oxford Univ. Press, New York, 1998).

    Google Scholar 

  15. Feng,G. et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41–51 (2000).

    Article  CAS  Google Scholar 

  16. Kosaka, K., Aika, Y., Toida, K. & Kosaka, T. Structure of intraglomerular dendritic tufts of mitral cells and their contacts with olfactory nerve terminals and calbindin-immunoreactive type 2 periglomerular neurons. J. Comp. Neurol. 440, 219–235 (2001).

    Article  CAS  Google Scholar 

  17. Samanen, D.W. & Forbes, W.B. Replication and differentiation of olfactory receptor neurons following axotomy in the adult hamster: a morphometric analysis of postnatal neurogenesis. J. Comp. Neurol. 225, 201–211 (1984).

    Article  CAS  Google Scholar 

  18. Mackay-Sim, A. & Kittel, P.W. On the life span of olfactory receptor neurons. Eur. J. Neurosci. 3, 209–215 (1991).

    Article  Google Scholar 

  19. Kempermann, G., Kuhn, H.G. & Gage, F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 386, 493–495 (1997).

    Article  CAS  Google Scholar 

  20. Gould, E. & Gross, C.G. Neurogenesis in adult mammals: some progress and problems. J. Neurosci. 22, 619–623 (2002).

    Article  CAS  Google Scholar 

  21. Rochefort, C., Gheusi, G., Vincent, J.D. & Lledo, P.M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 22, 2679–2689 (2002).

    Article  CAS  Google Scholar 

  22. Cline, H.T. Dendritic arbor development and synaptogenesis. Curr. Opin. Neurobiol. 11, 118–126 (2001).

    Article  CAS  Google Scholar 

  23. Knott, G.W., Quairiaux, C., Genoud, C. & Welker, E. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 34, 265–273 (2002).

    Article  CAS  Google Scholar 

  24. Brennan, P.A., Schellinck, H.M., de la Riva, C., Kendrick, K.M. & Keverne, E.B. Changes in neurotransmitter release in the main olfactory bulb following an olfactory conditioning procedure in mice. Neuroscience 87, 583–590 (1998).

    Article  CAS  Google Scholar 

  25. Brennan, P.A. & Keverne, E.B. Neural mechanisms of mammalian olfactory learning. Prog. Neurobiol. 51, 457–481 (1997).

    Article  CAS  Google Scholar 

  26. Faber, T., Joerges, J. & Menzel, R. Associative learning modifies neural representations of odors in the insect brain. Nat. Neurosci. 2, 74–78 (1999).

    Article  CAS  Google Scholar 

  27. Belluscio, L., Lodovichi, C., Feinstein, P., Mombaerts, P. & Katz, L.C. Odorant receptors instruct functional circuitry in the mouse olfactory bulb. Nature 419, 296–300 (2002).

    Article  CAS  Google Scholar 

  28. 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 

  29. Schellinck, H.M., Forestell, C.A. & LoLordo, V.M. A simple and reliable test of olfactory learning and memory in mice. Chem. Senses 26, 663–672 (2001).

    Article  CAS  Google Scholar 

  30. Purves, D., Hadley, R.D. & Voyvodic, J.T. Dynamic changes in the dendritic geometry of individual neurons visualized over periods of up to three months in the superior cervical ganglion of living mice. J. Neurosci. 6, 1051–1060 (1986).

    Article  CAS  Google Scholar 

  31. Purves, D., Voyvodic, J.T., Magrassi, L. & Yawo, H. Nerve terminal remodeling visualized in living mice by repeated examination of the same neuron. Science 238, 1122–1126 (1987).

    Article  CAS  Google Scholar 

  32. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W.W. & Prasher, D.C. Green fluorescent protein as a marker for gene expression. Science 263, 802–805 (1994).

    Article  CAS  Google Scholar 

  33. Denk, W. & Svoboda, K. Photon upmanship: why multiphoton imaging is more than a gimmick. Neuron 18, 351–357 (1997).

    Article  CAS  Google Scholar 

  34. Scott, E.K. & Luo, L. How do dendrites take their shape? Nat. Neurosci. 4, 359–365 (2001).

    Article  CAS  Google Scholar 

  35. Friedman, H.V., Bresler, T., Garner, C.C. & Ziv, N.E. Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27, 57–69 (2000).

    Article  CAS  Google Scholar 

  36. Wu, G.Y., Zou, D.J., Rajan, I. & Cline, H.T. Dendritic dynamics in vivo change during neuronal maturation. J. Neurosci. 19, 4472–4483 (1999).

    Article  CAS  Google Scholar 

  37. Nguyen, Q.T., Sanes, J.R. & Lichtman, J.W. Pre-existing pathways promote precise projection patterns. Nat. Neurosci. 5, 861–867 (2002).

    Article  CAS  Google Scholar 

  38. Swann, J.W., Al Noori, S., Jiang, M. & Lee, C.L. Spine loss and other dendritic abnormalities in epilepsy. Hippocampus 10, 617–625 (2000).

    Article  CAS  Google Scholar 

  39. Geinisman, Y. Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cereb. Cortex 10, 952–962 (2000).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  41. Spors, H. & Grinvald, A. Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron 34, 301–315 (2002).

    Article  CAS  Google Scholar 

  42. Dudai, Y. Memory: from A to Z (Oxford Univ. Press, New York, 2002).

    Google Scholar 

  43. Wilson, D.A. & Stevenson, R.J. The fundamental role of memory in olfactory perception. Trends Neurosci. 26, 243–247 (2003).

    Article  CAS  Google Scholar 

  44. Maletic-Savatic, M., Malinow, R. & Svoboda, K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923–1927 (1999).

    Article  CAS  Google Scholar 

  45. Engert, F. & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66–70 (1999).

    Article  CAS  Google Scholar 

  46. Zou, Z., Horowitz, L.F., Montmayeur, J.P., Snapper, S. & Buck, L.B. Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature 414, 173–179 (2001).

    Article  CAS  Google Scholar 

  47. Yuste, R. & Bonhoeffer, T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 24, 1071–1089 (2001).

    Article  CAS  Google Scholar 

  48. 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 

  49. Chen, B.E. et al. Imaging high-resolution structure of GFP-expressing neurons in neocortex in vivo. Learn. Mem. 7, 433–441 (2000).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

L.C.K. is an Investigator in the Howard Hughes Medical Institute. Supported by National Institutes of Health grant DC005671. We are grateful to G. Feng (Duke University Medical Center) for providing the YFP–G mice. We are grateful to members of the Katz lab for comments on the manuscript. A.M. is supported by a long-term fellowship of the Human Frontier Science Program.

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Correspondence to Adi Mizrahi.

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Supplementary information

Supplementary Fig. 1.

Quantitative analysis of a mitral cell apical dendrite. (a) Projection image of a single apical tuft of a mitral cell transfected with Sindbis-GFP in the olfactory bulb of an adult mouse. (b) Reconstruction of the complete dendritic tree shown in a. Scale bar: 25μm. (c) Two-dimensional dendrogram of the reconstructed apical dendritic tuft shown in a. (PDF 323 kb)

Supplementary Fig. 2.

Dendritic changes are distributed throughout the glomerular depth. Frequency of the position (glomerular depth) of the dendritic changes (% of total sprouting and pruning events) pooled from all control experiments. The low percent of changes observed in the first 10 μm reflects the less dense dendritic labeling in this region of the glomerulus. (PDF 44 kb)

Supplementary Fig. 3.

Quantitative morphometric comparison (of the number of branching points, total dendritic length and total surface area) between the single complete dendritic tuft (shown in Supplementary Fig. 1) and the dendritic reconstructions from the two-photon experiments (averages ± SEM). In the two-photon experiments we sampled the equivalent of 85%, 50% and 35% of the total number of branches (a), length (b) and surface area (c), respectively, of a single complete M/T dendritic tuft. The relative higher value for the number of branching points probably reflects that our sample mainly contains distal higher order branches where a higher frequency of branching is evident (see dendrogram in Supplementary Fig. 1c). (PDF 54 kb)

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Mizrahi, A., Katz, L. Dendritic stability in the adult olfactory bulb. Nat Neurosci 6, 1201–1207 (2003). https://doi.org/10.1038/nn1133

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