Morphological correlates of functionally defined synaptic vesicle populations (original) (raw)

Nature Neuroscience volume 4, pages 391–395 (2001)Cite this article

Abstract

By combining photoconversion of FM1-43-stained vesicles and electron microscopy of hippocampal synapses, we find evidence that the population of morphologically docked synaptic vesicles corresponds to the release-ready neurotransmitter quanta. Furthermore, those synaptic vesicles that are participating in cycles of exo- and endocytosis tend to be closer to the active zone than vesicles that are being held in reserve.

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

Access options

Subscribe to this journal

Receive 12 print issues and online access

$209.00 per year

only $17.42 per issue

Buy this article

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

Additional access options:

Similar content being viewed by others

References

  1. von Gersdorff, H., Vardi, E., Matthews, G. & Sterling, P. Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released. Neuron 16, 1221–1227 (1996).
    Article CAS Google Scholar
  2. Schikorski, T. & Stevens, C. F. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J. Neurosci. 17, 5858–5867 (1997).
    Article CAS Google Scholar
  3. Murthy, V. N., Sejnowski, T. J. & Stevens, C. F. Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18, 599–612 (1997).
    Article CAS Google Scholar
  4. Cochilla, A. J., Angleson, J. K. & Betz, W. J. Monitoring secretory membrane with FM1-43 fluorescence. Annu. Rev. Neurosci. 22, 1–10 (1999).
    Article CAS Google Scholar
  5. Ryan, T. A., Ziv, N. E. & Smith, S. J. Potentiation of evoked vesicle turnover at individually resolved synaptic boutons. Neuron 17, 125–134 (1996).
    Article CAS Google Scholar
  6. Ryan, T. A., Li, L., Chin, L.-S., Greengard, P. & Smith, S. J. Synaptic vesicle recycling in synapsin I knock-out mice. J. Cell Biol. 134, 1219–1227 (1996).
    Article CAS Google Scholar
  7. Murthy, V. N. & Stevens, C. F. Reversal of synaptic vesicle docking at central synapses. Nat. Neurosci. 2, 503–507 (1999).
    Article CAS Google Scholar
  8. Sandell, J. H. & Masland, R. H. Photoconversion of some fluorescent markers to a diaminobenzidine product. Histochem. Cytochem. 36, 555–559 (1988).
    Article CAS Google Scholar
  9. Henkel, A. W., Lübke, J. & Betz, W. J. FM1-43 dye ultrastructural localization in and release from frog motor nerve terminals. Proc. Natl. Acad. Sci. USA 93, 1918–1923 (1996).
    Article CAS Google Scholar
  10. Boyer, C., Schikorski, T. & Stevens, C. F. Comparison of hippocampal dendritic spines in culture and in brain. J. Neurosci. 18, 5294–5300 (1998).
    Article CAS Google Scholar
  11. Schikorski, T., Braun, N. & Zimmermann, H. Projection of brain stem neurons to the giant electromotoneurons in the cervical spinal cord of the electric catfish malaterurus electricus. Brain Behav. Evol. 43, 306–318 (1994).
    Article CAS Google Scholar
  12. Rosenmund, C. & Stevens, C. F. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16, 1197–1207 (1996).
    Article CAS Google Scholar
  13. Fesce, R., Grohovaz, F., Valtorta, F. & Meldolesi, J. Neurotransmitter release: fusion or 'kiss-and-run'? Trends Cell Biol. 4, 1–4 (1994).
    Article CAS Google Scholar
  14. Stevens, C. F. & Williams, J. H. “Kiss and Run” exocytosis at hippocampal synapses. Proc. Natl. Acad. Sci. USA 97 12828–12833 (2001).
    Article Google Scholar
  15. Fernandez-Chacon, R. & Sudhof, T. C. Genetics of synaptic vesicle function: toward the complete functional anatomy of an organelle. Annu. Rev. Physiol. 61, 753–776 (1999).
    Article CAS Google Scholar
  16. Ryan, T. A., Smith, S. J. & Reuter, H. The timing of synaptic vesicle endocytosis. Proc. Natl. Acad. Sci. USA 93, 5567–5571 (1996).
    Article CAS Google Scholar
  17. Murthy, V. N. & Stevens, C. F. Synaptic vesicles retain their identity through the endocytic cycle. Nature 392, 497–501 (1998).
    Article CAS Google Scholar
  18. Schikorski, T. & Stevens, C. F. Quantitative fine-structural analysis of olfactory cortical synapses. Proc. Natl. Acad. Sci. USA 96, 4107–4112 (1999).
    Article CAS Google Scholar
  19. Kuromi, H. & Kidokoro, Y. Two distinct pools of synaptic vesicles in single presynaptic boutons in a temperature-sensitive Drosophila mutant, shibire. Neuron 20, 917–925 (1998).
    Article CAS Google Scholar

Download references

Author information

Authors and Affiliations

  1. Howard Hughes Medical Institute and Molecular Neurobiology Lab, The Salk Institute, 10010 N. Torrey Pines Road, La Jolla, 92037, California, USA
    Thomas Schikorski & Charles F. Stevens

Authors

  1. Thomas Schikorski
    You can also search for this author inPubMed Google Scholar
  2. Charles F. Stevens
    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence toCharles F. Stevens.

Rights and permissions

About this article

Cite this article

Schikorski, T., Stevens, C. Morphological correlates of functionally defined synaptic vesicle populations.Nat Neurosci 4, 391–395 (2001). https://doi.org/10.1038/86042

Download citation

This article is cited by