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Local calcium transients regulate the spontaneous motility of dendritic filopodia

Nature Neuroscience volume 8, pages 305–312 (2005)Cite this article

Abstract

During development, dendrites, and in particular dendritic filopodia, undergo extensive structural remodeling, presumably to help establish synaptic contacts. Here, we investigated the role of calcium signaling in dendritic plasticity by simultaneously recording calcium dynamics and filopodial growth in rat hippocampal slice cultures. Local calcium transients occurred in dendritic filopodia and shafts, often at putative synaptic sites. These events were highly correlated with filopodial motility: comparatively rare when individual filopodia emerged from the dendrite, they became more frequent after filopodia started growing, finally causing them to halt. Accordingly, an experimental reduction of the frequency of local calcium transients elicited filopodial growth and, conversely, calcium uncaging reduced filopodial motility. Our observations suggest that low levels of local calcium transients facilitate filopodial outgrowth, whereas high levels inhibit the formation of filopodia and stabilize newly formed ones. This process may facilitate synapse formation and may serve as a homeostatic mechanism distributing synapses evenly along developing dendrites.

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Figure 1: Local and global calcium transients occur in dendrites of developing hippocampal neurons.
Figure 2: Most dendritic calcium transients occur near synapses.
Figure 3: Local calcium transients are generated in filopodia and transmitted to the dendritic shaft.
Figure 4: Filopodial growth and calcium dynamics are correlated.
Figure 5: Uncaging of calcium in dendrites blocks filopodial motility.
Figure 6: Blockade of local calcium transients induces filopodial growth.

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Acknowledgements

We thank F. Siegel for performing data analysis; O. Momoh and N. Stöhr for preparation and maintenance of slice cultures; S. Eglen for help with the Monte Carlo statistics; and R. Wong and M. Hübener for critically reading the manuscript. This work was supported by the Max-Planck-Gesellschaft and the Schloessmann Foundation (C.L.).

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Authors and Affiliations

  1. Max Planck Institute of Neurobiology, Am Klopferspitz 18, Planegg-Martinsried, 82152, Germany

    Christian Lohmann, Alexei Finski & Tobias Bonhoeffer

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  1. Christian Lohmann
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  2. Alexei Finski
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  3. Tobias Bonhoeffer
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Corresponding author

Correspondence to Christian Lohmann.

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Supplementary information

Supplementary Fig. 1

Model for the regulation of filopodial growth by local calcium transients. (PDF 547 kb)

Supplementary Video 1

Local and global calcium transients. Local and global calcium transients in dendrites of a CA3 pyramidal neuron (real time). (MOV 614 kb)

Supplementary Video 2

Filopodial calcium transients. Three consecutive calcium transients are generated in a filopodium and spread into the dendritic shaft with some delay (3 x faster than real time). (MOV 408 kb)

Supplementary Video 3

Filopodial growth and calcium transients. Two filopodia grow during this recording. Calcium transients in the parent dendrite can be seen after the onset of growth, but not before (30 x faster than real time). (MOV 281 kb)

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Lohmann, C., Finski, A. & Bonhoeffer, T. Local calcium transients regulate the spontaneous motility of dendritic filopodia. Nat Neurosci 8, 305–312 (2005). https://doi.org/10.1038/nn1406

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