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.

Septo-hippocampal GABAergic signaling across multiple modalities in awake mice

Subjects

Abstract

Hippocampal interneurons receive GABAergic input from the medial septum. Using two-photon Ca2+ imaging of axonal boutons in hippocampal CA1 of behaving mice, we found that populations of septo-hippocampal GABAergic boutons were activated during locomotion and salient sensory events; sensory responses scaled with stimulus intensity and were abolished by anesthesia. We found similar activity patterns among boutons with common putative postsynaptic targets, with low-dimensional bouton population dynamics being driven primarily by presynaptic spiking.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Functional imaging of SH-GABA boutons in CA1 of behaving mice.
Figure 2: SH-GABA bouton population dynamics.
Figure 3: Factors contributing to bouton population activity patterns.

References

  1. Freund, T.F. & Antal, M. Nature 336, 170–173 (1988).

    CAS  Article  Google Scholar 

  2. Dragoi, G., Carpi, D., Recce, M., Csicsvari, J. & Buzsaki, G. J. Neurosci. 19, 6191–6199 (1999).

    CAS  Article  Google Scholar 

  3. Hangya, B., Borhegyi, Z., Szilágyi, N., Freund, T.F. & Varga, V. J. Neurosci. 29, 8094–8102 (2009).

    CAS  Article  Google Scholar 

  4. Simon, A.P., Poindessous-Jazat, F., Dutar, P., Epelbaum, J. & Bassant, M.H. J. Neurosci. 26, 9038–9046 (2006).

    CAS  Article  Google Scholar 

  5. Hassani, O.K., Lee, M.G., Henny, P. & Jones, B.E. J. Neurosci. 29, 11828–11840 (2009).

    CAS  Article  Google Scholar 

  6. Mercer, L.F. & Remley, N.R. Brain Res. Bull. 4, 483–490 (1979).

    Article  Google Scholar 

  7. Miller, C.L. & Freedman, R. Neuroscience 55, 373–380 (1993).

    CAS  Article  Google Scholar 

  8. Zhang, H., Lin, S.-C. & Nicolelis, M.A. J. Neurophysiol. 106, 2749–2763 (2011).

    Article  Google Scholar 

  9. Chen, T.-W. et al. Nature 499, 295–300 (2013).

    CAS  Article  Google Scholar 

  10. Dombeck, D.A., Harvey, C.D., Tian, L., Looger, L.L. & Tank, D.W. Nat. Neurosci. 13, 1433–1440 (2010).

    CAS  Article  Google Scholar 

  11. Vinogradova, O.S. Prog. Neurobiol. 45, 523–583 (1995).

    CAS  Article  Google Scholar 

  12. Chowdhury, N., Quinn, J.J. & Fanselow, M.S. Behav. Neurosci. 119, 1396–1402 (2005).

    Article  Google Scholar 

  13. Gulyás, A.I., Hájos, N., Katona, I. & Freund, T.F. Eur. J. Neurosci. 17, 1861–1872 (2003).

    Article  Google Scholar 

  14. Lovett-Barron, M. et al. Nat. Neurosci. 15, 423–430 (2012).

    CAS  Article  Google Scholar 

  15. Wickersham, I.R., Finke, S., Conzelmann, K.K. & Callaway, E.M. Nat. Methods 4, 47–49 (2007).

    CAS  Article  Google Scholar 

  16. Wickersham, I.R. et al. Neuron 53, 639–647 (2007).

    CAS  Article  Google Scholar 

  17. Ugolini, G. J. Neurosci. Methods 194, 2–20 (2010).

    Article  Google Scholar 

  18. Watabe-Uchida, M., Zhu, L., Ogawa, S.K., Vamanrao, A. & Uchida, N. Neuron 74, 858–873 (2012).

    CAS  Google Scholar 

  19. McClure, C., Cole, K.L.H., Wulff, P., Klugmann, M. & Murray, A.J. J. Vis. Exp. 57, e3348 (2011).

    Google Scholar 

  20. Wickersham, I.R., Sullivan, H.A. & Seung, H.S. Nat. Protoc. 5, 595–606 (2010).

    CAS  Article  Google Scholar 

  21. Dong, H.W. The Allen Reference Atlas: A Digital Color Brain Atlas of C57BL/6J Male Mouse (John Wiley & Sons, 2008).

  22. Royer, S. et al. Nat. Neurosci. 15, 769–775 (2012).

    CAS  Article  Google Scholar 

  23. Holtmaat, A. et al. Nat. Protoc. 4, 1128–1144 (2009).

    CAS  Article  Google Scholar 

  24. Bouton, M.E. & Bolles, R.C. J. Exp. Psychol. Anim. Behav. Process. 5, 368–378 (1979).

    CAS  Article  Google Scholar 

  25. Dombeck, D.A., Khabbaz, A.N., Collman, F., Adelman, T.L. & Tank, D.W. Neuron 56, 43–57 (2007).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank C. Lacefield for advice on the behavioral apparatus, L. Paninski for advice on the motion correction algorithm, J. Zaremba, N. Danielson, K. Shakman and A. Castro for programming assistance, M. Morishima for help with immunohistochemistry, and B.V. Zemelman for help with mice and viruses. We thank J.C. Magee, S.A. Siegelbaum, L.F. Abbott and T.M. Jessell for comments on the manuscript. The authors thank the GENIE Program and the Janelia Farm Research Campus of the Howard Hughes Medical Institute for the kind gift of the GCaMP variant 354. This work was funded by the Howard Hughes Medical Institute International Student Research Fellowship Program (P.K.), Natural Sciences and Engineering Research Council of Canada Postgraduate Scholarships (P.K. and M.L.-B.), the Searle Scholars Program, the Human Frontier Science Program, and the Kavli Institute at Columbia University (A.L.).

Author information

Authors and Affiliations

Authors

Contributions

P.K. designed and built hardware and software for imaging, behavior and motion-correction, and performed analyses. M.L.-B., G.F.T. and A.L. performed experiments. T.R.R. performed pseudo-type rabies trans-synaptic labeling. All of the authors wrote the manuscript.

Corresponding authors

Correspondence to Patrick Kaifosh or Attila Losonczy.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–12 (PDF 3373 kb)

Supplementary Video 1

The dynamics of GCaMP signals overlayed upon the static tdTomato background can be viewed. Description: Example of time frame images after motion-correction and channel separation detailed in Supplementary Figure 3. (AVI 24412 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kaifosh, P., Lovett-Barron, M., Turi, G. et al. Septo-hippocampal GABAergic signaling across multiple modalities in awake mice. Nat Neurosci 16, 1182–1184 (2013). https://doi.org/10.1038/nn.3482

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3482

Further reading

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