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Transmitter-evoked local calcium release stabilizes developing dendrites

Nature volume 418, pages 177–181 (2002)Cite this article

Abstract

In the central nervous system, dendritic arborizations of neurons undergo dynamic structural remodelling during development. Processes are elaborated, maintained or eliminated to attain the adult pattern of synaptic connections1,2,3. Although neuronal activity influences this remodelling4,5,6, it is not known how activity exerts its effects. Here we show that neurotransmission-evoked calcium (Ca2+) release from intracellular stores stabilizes dendrites during the period of synapse formation. Using a ballistic labelling method to load cells with Ca2+ indicator dyes7, we simultaneously monitored dendritic activity and structure in the intact retina. Two distinct patterns of spontaneous Ca2+ increases occurred in developing retinal ganglion cells—global increases throughout the arborization, and local ‘flashes’ of activity restricted to small dendritic segments. Blockade of local, but not global, activity caused rapid retraction of dendrites. This retraction was prevented locally by focal uncaging of caged Ca2+ that triggered Ca2+ release from internal stores. Thus, local Ca2+ release is a mechanism by which afferent activity can selectively and differentially regulate dendritic structure across the developing arborization.

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Figure 1: Developing dendrites of retinal ganglion cells exhibit global and local spontaneous [Ca2+]i increase.
Figure 2: Potential contact between a displaced amacrine cell (AC) neurite and a ganglion cell (GC) dendrite.
Figure 3: Dendrites retract when local activity is suppressed.
Figure 4: Ca2+-induced Ca2+ release prevents dendritic retraction.

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Acknowledgements

We thank J. Sanes, J. Lichtman, A. M. Craig and S. Eglen for comments on the manuscript, and J. Demas for assistance with ballistic loading of calcium indicators. This work was supported by NIH, NSF, DFG and the Plum foundation.

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Authors and Affiliations

  1. Department of Anatomy and Neurobiology, Washington University School of Medicine, 660 S. Euclid, St Louis, Missouri, 63110, USA

    Christian Lohmann, Karen L. Myhr & Rachel O. L. Wong

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  1. Christian Lohmann
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  3. Rachel O. L. Wong
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Correspondence to Rachel O. L. Wong.

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The authors declare that they have no competing financial interests.

Supplementary information

41586_2002_BFnature00850_MOESM1_ESM.mov

Mov1.MOV: Movie of local and global [Ca2+]i rises in a retinal ganglion cell from an E13 Chick. (time-lapse recording: 1 s movie = 45 s real time) (MOV 14490 kb)

41586_2002_BFnature00850_MOESM2_ESM.pdf

Additional data demonstrating that the Ca2+ buffering capacity of the Ca2+ indicator Oregon Green 488 BAPTA-1 dextran did not effect Ca2+ signals or regulation of dendritic plasticity. (PDF 47 kb)

41586_2002_BFnature00850_MOESM3_ESM.mov

Mov2.MOV: Movie showing contact formation between a neurite of an amacrine cell (AC) and a dendrite of a ganglion cell (GC). Both cells are labeled with OGB1. (time-lapse recording: 1 s movie = 90 s real time) (MOV 13827 kb)

41586_2002_BFnature00850_MOESM4_ESM.pdf

Mov2.MOV: Movie showing contact formation between a neurite of an amacrine cell (AC) and a dendrite of a ganglion cell (GC). Both cells are labeled with OGB1. (time-lapse recording: 1 s movie = 90 s real time) (PDF 114 kb)

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Lohmann, C., Myhr, K. & Wong, R. Transmitter-evoked local calcium release stabilizes developing dendrites. Nature 418, 177–181 (2002). https://doi.org/10.1038/nature00850

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