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.

  • Letter
  • Published:

A role for Cajal–Retzius cells and reelin in the development of hippocampal connections

Abstract

DURING development of the nervous system, specific recognition molecules provide the cues necessary for the formation of neural connections. In some regions, guiding cues for axonal pathfinding and target selection are provided by specific cells that exist only transiently during development, such as the floorplate or the cortical subplate1–4. In the hippocampus, distinct groups of fibres innervate different layers5. We have tested the hypothesis that transient neurons in the hippocampus6,7 provide positional information for the targeting of these fibres. Here we report that ablation of Cajal–Retzius cells in organotypic slice cultures of hippocampus prevented the ingrowth of entorhinal but not of commissural afferents. Experiments inhibiting Reelin (an extracellular matrix protein expressed by Cajal–Retzius cells) and analysis of reeler mutant mice showed dramatic abnormalities in the development of entorhinal afferents. Thus Cajal–Retzius cells and reelin are essential for the formation of layer-specific hippocampal connections.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Similar content being viewed by others

References

  1. Kennedy, T. E. & Tessier-Lavigne, M. Curr. Opin. Neurobiol. 5, 83–90 (1995).

    Article  CAS  Google Scholar 

  2. Serafini, T. et al. Cell 78, 409–424 (1994).

    Article  CAS  Google Scholar 

  3. Ghosh, A., Antonini, A., McConnell, S. K. & Shatz, C. J. Nature 347,179–181 (1990).

    Article  ADS  CAS  Google Scholar 

  4. Ghosh, A. & Shatz, C. J. Science 255,1441–1443 (1992).

    Article  ADS  CAS  Google Scholar 

  5. Amaral, D. G. & Witter, M. P. in The Rat Nervous System 2nd edn (ed. Paxinos, G.) 443–493 (Academic, New York, 1995).

    Google Scholar 

  6. Supèr, H. & Soriano, E. J. Comp. Neurol. 344,101–120 (1994).

    Article  Google Scholar 

  7. Soriano, E., Del Río, J. A., Martínez, A. & Supèr, H. J. Comp. Neurol. 342, 571–595 (1994).

    Article  CAS  Google Scholar 

  8. Li, D., Field, P. M., Starega, U., Li, Y. & Raisman, G. Neuroscience 52, 799–813 (1993).

    Article  CAS  Google Scholar 

  9. Frotscher, M. & Heimrich, B. Proc. Natl. Acad. Sci. USA 90,10400–10403 (1993).

    Article  ADS  CAS  Google Scholar 

  10. Soriano, E., Cobas, A. & Fairén A. J. Comp. Neurol. 281, 586–602 (1989).

    Article  CAS  Google Scholar 

  11. Supèr, H., Martínez, A. & Soriano, E. Dev. Brain Res. (in press).

  12. D'Arcangelo, G. et al. Nature 374, 719–723 (1995).

    Article  ADS  CAS  Google Scholar 

  13. Hirotsune, S. et al. Nature Genet. 10, 77–82 (1995).

    Article  CAS  Google Scholar 

  14. Ogawa, M. et al. Neuron 14, 899–912 (1995).

    Article  CAS  Google Scholar 

  15. Cabelli, R. J., Hohn, A. & Shatz, C. J. Science 267,1662–1666 (1995).

    Article  ADS  CAS  Google Scholar 

  16. Cohen-Cory, S. & Fraser, S. E. Nature 378, 192–196 (1995).

    Article  ADS  CAS  Google Scholar 

  17. Kolodkin, A. L., Matthes, D. J. & Goodman, C. S. Cell 75,1389–1399 (1995).

    Article  Google Scholar 

  18. Messersmith, E. K. et al. Neuron 14, 949–959 (1995).

    Article  CAS  Google Scholar 

  19. Cheng, H.-J., Nakamoto, M., Bergemann, A. D. & Flanagan, J. G. Cell 82, 371–381 (1995).

    Article  CAS  Google Scholar 

  20. Drescher, U. et al. Cell 82, 359–370 (1995).

    Article  CAS  Google Scholar 

  21. Goodman, C. S. & Shatz, C. J. Cell 72, 77–98 (1993).

    Article  Google Scholar 

  22. Hermann, K. & Shatz, C. J. Proc. Natl Acad. Sci. USA 92,11244–11248 (1995).

    Article  ADS  Google Scholar 

  23. Stoppini, L, Buchs, P. A. & Muller, D. J. Neurosci. Methods 37,173–182 (1991).

    Article  CAS  Google Scholar 

  24. Gulyás, A. I. et al. Nature 366, 683–687 (1993).

    Article  ADS  Google Scholar 

  25. Vornov, J. J., Tasker, R. C. & Coyle, J. T. Exp. Neurol. 114,11–22 (1991).

    Article  CAS  Google Scholar 

  26. Gavrieli, Y., Sherman, Y. & Ben-Sasson, S. A. J. Cell Biol. 119, 493–501 (1992).

    Article  CAS  Google Scholar 

  27. Soriano, E. & Del Río, J. A. J. Histochem. Cytochem. 39, 255–263 (1991).

    Article  CAS  Google Scholar 

  28. D'Arcangelo, G. et al. J. Neurosci. (in the press).

  29. Guenet, J. L. Mouse News Lett. 41, (1981).

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Del Río, J., Heimrich, B., Borrell, V. et al. A role for Cajal–Retzius cells and reelin in the development of hippocampal connections. Nature 385, 70–74 (1997). https://doi.org/10.1038/385070a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/385070a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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