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The Journal of Neuroscience, January 15, 1999, 19(2):692-704

Neuronal Acetylcholine Receptors with 7 Subunits Are Concentrated on Somatic Spines for Synaptic Signaling in Embryonic Chick Ciliary Ganglia

Richard D. Shoop¹, Maryann E. Martone², Naoko Yamada², Mark H. Ellisman², and Darwin K. Berg¹

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

Nicotinic acetylcholine receptors containing 7 subunits are widely distributed in the vertebrate nervous system. In the chick ciliary ganglion such receptors generate large synaptic currents but appear to be excluded from postsynaptic densities on the cells. We show here that 7-containing receptors are concentrated on somatic spines in close proximity to putative sites of presynaptic transmitter release. Intermediate voltage electron microscopy on thick sections, together with tomographic reconstruction, permitted three-dimensional analysis of finger-like projections emanating from cell bodies. The projections were identified as spines based on their morphology, cytoskeletal content, and proximity to presynaptic elements. Both in situ and after ganglionic dissociation, the spines were grouped on the cell surface and tightly folded into mats. Immunogold labeling of receptors containing 7 subunits showed them to be preferentially concentrated on the somatic spines. Postsynaptic densities were present in vivo both on the soma near spines and occasionally on the spines themselves. Synaptic vesicle-filled projections from the presynaptic calyx were interdigitated among the spines. Moreover, the synaptic vesicles often abutted the membrane and sometimes included  profiles as if caught in an exocytotic event, even when no postsynaptic densities were juxtaposed on the spine. The results suggest several mechanisms for delivering transmitter to 7-containing receptors, and they support new ideas about synaptic signaling via spines. They also indicate that neurons must have specific mechanisms for targeting 7-containing receptors to desired locations.

Key words: nicotinic; acetylcholine; 7; ciliary ganglion; spines; receptors; neuronal; cholinergic; synaptic; calyx; presynaptic; tomography; immunogold; confocal; electron microscopy

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Copyright © 1999 Society for Neuroscience  0270-6474/99/192692-13$05.00/0

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