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.

  • Brief Communication
  • Published:

A common origin of synaptic vesicles undergoing evoked and spontaneous fusion

Abstract

There is a longstanding controversy on the identity of synaptic vesicles undergoing spontaneous versus evoked release. A recent study, introducing a new genetic probe, suggested that spontaneous release is driven by a resting pool of synaptic vesicles refractory to stimulation. We found that cross-depletion of spontaneously or actively recycling synaptic vesicle pools occurred on stimulation in rat hippocampal neurons and identified the recycling pool as a major source of spontaneous release.

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

Access options

Buy this article

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

Figure 1: Synaptic vesicles labeled by spontaneous or activity-dependent uptake exhibit identical release kinetics on stimulation.
Figure 2: Synaptic vesicles endocytosed spontaneously and on stimulation recycle equally to the recycling (Rc) and resting (Rs) synaptic vesicle pools.
Figure 3: Synaptic vesicles undergoing spontaneous and activity-dependent recycling originate from the recycling pool.

Similar content being viewed by others

References

  1. Katz, B. & Miledi, R. J. Physiol. (Lond.) 203, 689–706 (1969).

    Article  CAS  Google Scholar 

  2. Murthy, V.N. & Stevens, C.F. Nat. Neurosci. 2, 503–507 (1999).

    Article  CAS  Google Scholar 

  3. Lou, X., Scheuss, V. & Schneggenburger, R. Nature 435, 497–501 (2005).

    Article  CAS  Google Scholar 

  4. Prange, O. & Murphy, T.H. J. Neurosci. 19, 6427–6438 (1999).

    Article  CAS  Google Scholar 

  5. Sara, Y., Virmani, T., Deak, F., Liu, X. & Kavalali, E.T. Neuron 45, 563–573 (2005).

    Article  CAS  Google Scholar 

  6. Groemer, T.W. & Klingauf, J. Nat. Neurosci. 10, 145–147 (2007).

    Article  CAS  Google Scholar 

  7. Fredj, N.B. & Burrone, J. Nat. Neurosci. 12, 751–758 (2009).

    Article  Google Scholar 

  8. Angleson, J.K. & Betz, W.J. J. Neurophysiol. 85, 287–294 (2001).

    Article  CAS  Google Scholar 

  9. Adie, E.J. et al. Assay Drug Dev. Technol. 1, 251–259 (2003).

    Article  CAS  Google Scholar 

  10. Howarth, M. & Ting, A.Y. Nat. Protoc. 3, 534–545 (2008).

    Article  CAS  Google Scholar 

  11. Martens, H. et al. J. Neurosci. 28, 13125–13131 (2008).

    Article  CAS  Google Scholar 

  12. Sankaranarayanan, S. & Ryan, T.A. Nat. Neurosci. 4, 129–136 (2001).

    Article  CAS  Google Scholar 

  13. Miesenböck, G., De Angelis, D.A. & Rothman, J.E. Nature 394, 192–195 (1998).

    Article  Google Scholar 

  14. Kim, S.H. & Ryan, T.A. Neuron 67, 797–809 (2010).

    Article  CAS  Google Scholar 

  15. Chung, C., Barylko, B., Leitz, J., Liu, X. & Kavalali, E.T. J. Neurosci. 30, 1363–1376 (2010).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank K. Hardes for culturing hippocampal neurons, H. Martens (Synaptic Systems) for providing antibodies and E. Neher for critical reading of the manuscript. This work was supported by the Deutsche Forschungsgemeinschaft (Kl 1334/1-1 to J.K.). Y.H. is supported by a stipend from the Max Planck foundation and R.S. by a stipend from the International Max Planck Research School in Neurosciences Göttingen.

Author information

Authors and Affiliations

Authors

Contributions

Y.H. and R.S. designed, performed and analyzed the CypHer antibody and spH experiments. M.M. and M.K. designed, performed and analyzed the streptavidin-cypHer experiments. J.K. initialized the project. All of the authors wrote the paper.

Corresponding author

Correspondence to Jürgen Klingauf.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–5, Supplementary Notes 1–3, Supplementary Discussion and Supplementary Methods (PDF 496 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hua, Y., Sinha, R., Martineau, M. et al. A common origin of synaptic vesicles undergoing evoked and spontaneous fusion. Nat Neurosci 13, 1451–1453 (2010). https://doi.org/10.1038/nn.2695

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2695

This article is cited by

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