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The Journal of Neuroscience, February 1, 2001, 21(3):771-781

Synaptically Driven Calcium Transients via Nicotinic Receptors on Somatic Spines

Richard D. Shoop1, Karen T. Chang1, Mark H. Ellisman2, 3, and Darwin K. Berg1

Departments of 1 Biology and 2 Neurosciences and the 3 National Center for Microscopy and Imaging Research, University of California, San Diego, La Jolla, California 92093-0357

Dendritic spines commonly receive glutamatergic innervation at postsynaptic densities and compartmentalize calcium influx arising from synaptic signaling. Recently, it was shown that a class of nicotinic acetylcholine receptors containing alpha 7 subunits is concentrated on somatic spines emanating from chick ciliary ganglion neurons. The receptors have a high relative calcium permeability and contribute importantly to synaptic currents, although they appear to be excluded from postsynaptic densities. Here we show that low-frequency synaptic stimulation of the alpha 7-containing receptors induces calcium transients confined to the spines. High-frequency stimulation induces a transient calcium elevation in the spines and a more sustained cell-wide elevation. The high-frequency transient elevation again depends on alpha 7-containing receptors, whereas the sustained elevation can be triggered by other nicotinic receptors and depends on calcium release from internal stores and probably influx through voltage-gated L-type calcium channels as well. Retrograde axonal stimulation of the neurons at high frequency mimics synaptic stimulation in producing sustained cell-wide calcium increases that depend on L-type channels and release from internal stores, but it does not produce calcium transients in the spines. Thus frequent action potentials are sufficient to generate the cell-wide increases, but alpha 7-containing receptors are needed for spine-specific effects. Patch-clamp recording indicates that alpha 7-containing receptors preferentially desensitize at high-frequency stimulation, accounting for the inability of the stimulation to sustain high calcium levels in the spines. The spatial and temporal differences in the patterns of calcium elevation could enable the neurons to monitor their own firing histories for regulatory purposes.

Key words: nicotinic; spines; calcium; acetylcholine receptors; ciliary ganglion; alpha 7

Copyright © 2001 Society for Neuroscience  0270-6474/01/213771-11$05.00/0


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