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Microdomains for neuron–glia interaction: parallel fiber signaling to Bergmann glial cells

Abstract

Astrocytes are considered a reticulate network of cells, through which calcium signals can spread easily. In Bergmann glia, astrocytic cells of the cerebellum, we identified subcellular compartments termed 'glial microdomains'. These elements have a complex surface consisting of thin membrane sheets, contain few mitochondria and wrap around synapses. To test for neuronal interaction with these structures, we electrically stimulated parallel fibers. This stimulation increased intracellular calcium concentration ([Ca2+]i) in small compartments within Bergmann glial cell processes similar in size to glial microdomains. Thus, a Bergmann glial cell may consist of hundreds of independent compartments capable of autonomous interactions with the particular group of synapses that they ensheath.

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Figure 1: Reconstruction of an appendage based on electron microscopic data.
Figure 2: Fine structure of appendages and relation to synapses.
Figure 3: Stimulation of parallel fibers triggers local calcium signals in Bergmann glial cells.
Figure 4: Inhibition of nerve impulse propagation and synaptic transmission blocks glial calcium responses.
Figure 5: Spontaneous activity in Bergmann glia microdomains.

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References

  1. Finkbeiner, S. Calcium waves in astrocytes—filling in the gaps. Neuron 8, 1101–1108 (1992).

    Article  CAS  Google Scholar 

  2. Verkhratsky, A. Orkand, R. K. & Kettenmann, H. Glial calcium: Homeostasis and signalling function. Physiol. Rev. 78, 1–42 (1998).

    Article  Google Scholar 

  3. Hatten, M. E. Riding the glial monorail: a common mechanism for glial–guided neuronal migration in different regions of the developing mammalian brain. Trends Neurosci. 13, 179–184 (1990).

    Article  CAS  Google Scholar 

  4. Chan–Palay, V. & Palay, S. L. High voltage electron microscopy of rapid golgi preparations. Neurons and their processes in the cerebellar cortex of monkey and rat. Z. Anat. Entwicklungsgesch. 137, 125–153 ( 1972).

    Article  Google Scholar 

  5. Müller, T., Möller, T., Berger, T., Schnitzer, J. & Kettenmann, H. Calcium entry through kainate receptors and resulting potassium–channel blockade in Bergmann glial cells. Science 256, 1563– 1566 (1992).

    Article  Google Scholar 

  6. Reichenbach, A. Siegel, D., Senitz, T. & Smith, G. Jr A comparative fractal analysis of various mammalian astroglial cell types. Neuroimage 1, 69–77 (1992).

    Article  CAS  Google Scholar 

  7. Rall, W. et al. Matching dendritic neuron models to experimental data. Physiol. Rev. 72, S159–186 (1992).

    Article  CAS  Google Scholar 

  8. Sweadner, K. J. in Neuroglia (eds. Kettenmann, H. & Ransom, B. R.) 259 –272 (Oxford Univ. Press, New York, 1995).

    Google Scholar 

  9. Rosenthal, M. & Sick, T. J. Glycolytic and oxidative metabolic contributions to potassium ion transport in rat cerebral cortex. Can. J. Physiol. Pharmacol. 70, S165– 169 (1992).

    Article  CAS  Google Scholar 

  10. Konnerth, A., Llano, I. & Armstrong, C. M. Synaptic currents in cerebellar Purkinje cells. Proc. Natl. Acad. Sci. USA 87, 2662– 2665 (1990).

    Article  CAS  Google Scholar 

  11. Kuffler, S. W. Nicholls, J. G. & Orkand, R. K. Physiological properties of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29, 768–787 (1966).

    Article  CAS  Google Scholar 

  12. Verkhratsky, A. & Kettenmann, H. Calcium signalling in glial cells. Trends Neurosci. 19, 346 –352 (1996).

    Article  CAS  Google Scholar 

  13. Müller, T., Möller, T., Neuhaus, J. & Kettenmann, H. Electrical coupling among Bergmann glial cells and its modulation by glutamate receptor activation, Glia 17, 274– 284 (1996).

    Article  Google Scholar 

  14. Clark, B. A. & Barbour, B. Currents evoked in Bergmann glial cells by parallel fibre stimulation in rat cerebellar slices. J. Physiol. (Lond.) 502, 335–350 (1997).

    Article  CAS  Google Scholar 

  15. Sarantis, M. & Attwell, D. Glutamate uptake in mammalian retinal glia is voltage– and potassium–dependent. Brain Res. 516, 322–325 ( 1990).

    Article  CAS  Google Scholar 

  16. Bezzi, P. et al. Prostaglandins stimulate calcium–dependent glutamate release in astrocytes. Nature 391, 281– 285 (1998).

    Article  CAS  Google Scholar 

  17. Kirischuk, S., Kettenmann, H. & Verkhratsky, A. Metabotropic receptors involved in calcium signalling in mouse Bergmann glial cells. J. Physiol. (Lond.) 493, 46 (1996).

    Google Scholar 

  18. Eilers, J., Augustine, G. J. & Konnerth, A. Subthreshold synaptic Ca2+ signalling in fine dendrites and spines of cerebellar Purkinje neurons. Nature 373, 155–158 ( 1995).

    Article  CAS  Google Scholar 

  19. Denk, W., Sugimori, M. & Llinás, R. Two types of calcium response limited to single spines in cerebellar Purkinje cells. Proc. Natl. Acad. Sci. USA 92, 8279–8282 (1995).

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank S. Lyons, A. Konnerth and B. R. Ransom for comments on the manuscript. This work was supported by grants from Deutsche Forschungsgemeinschaft (SFB 515; 436UKR), Volkswagen–Stiftung and Interdisciplinary Center for Clinical Research at the University of Leipzig, (01KS9504, Project C5).

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Correspondence to Helmut Kettenmann.

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Grosche, J., Matyash, V., Möller, T. et al. Microdomains for neuron–glia interaction: parallel fiber signaling to Bergmann glial cells. Nat Neurosci 2, 139–143 (1999). https://doi.org/10.1038/5692

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