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J Neurophysiol 82: 1124-1132, 1999;
0022-3077/99 $5.00
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The Journal of Neurophysiology Vol. 82 No. 3 September 1999, pp. 1124-1132
Copyright ©1999 by the American Physiological Society

Extracellular Calcium Regulates Responses of Both alpha 3- and alpha 7-Containing Nicotinic Receptors on Chick Ciliary Ganglion Neurons

Qing-Song Liu and Darwin K. Berg

Department of Biology, University of California, San Diego, La Jolla, California 92093

Liu, Qing-Song and Darwin K. Berg. Extracellular Calcium Regulates Responses of Both alpha 3- and alpha 7-Containing Nicotinic Receptors on Chick Ciliary Ganglion Neurons. J. Neurophysiol. 82: 1124-1132, 1999. Neuronal nicotinic receptors are generally both permeable to calcium and potentiated by it. We have examined acute calcium regulation of both native alpha 7-containing and the less abundant alpha 3-containing nicotinic receptors on chick ciliary ganglion neurons. Most of the receptors are concentrated on somatic spines tightly overlaid in situ by a large presynaptic calyx. Whole cell patch-clamp recording from dissociated neurons using perforated patch-clamp techniques indicates that the rapidly desensitizing nicotinic response of alpha 7-containing receptors achieves maximum amplitude in 2 mM calcium; both lower and higher concentrations of calcium are less effective. Barium and strontium but not magnesium can substitute for calcium in potentiating the response. Neither calcium current through the receptors nor calcium action at intracellular sites is necessary. These latter conclusions are supported by current-voltage analysis of the nicotine-induced response, ion substitution experiments, and internal perfusion of the cells with 1,2-bis-(2-aminophenoxy)-ethane-N,N,N',N'-tetraacetic acid (BAPTA) via a conventional patch pipette. Varying the agonist concentration indicates that some of the calcium-dependent enhancement may involve a shift in the dose-response curve for agonist binding, but much of the effect is also likely to involve increased receptor responsiveness. Blockade of alpha 7-containing receptors with alpha -bungarotoxin showed that the heteromeric alpha 3-containing nicotinic receptors also undergo calcium-dependent potentiation. Calcium did not have a major effect on the desensitization rate of either receptor class but did have a selective effect on the rise time of alpha 7-containing receptors. Analysis of stably transfected cells expressing an alpha 7 gene construct showed that the calcium potentiation observed for native receptors did not require neuron-specific modifications or components and that it could be seen with the natural agonist acetylcholine. Receptor dependence on extracellular calcium may provide a regulatory mechanism for constraining synaptic signaling, avoiding local depletion of external calcium, and limiting calcium buildup in postsynaptic compartments.




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